ORIGINAL_ARTICLE
An update on the new achievements in the nanocapsulation of anthocyanins
Natural food pigments are commonly utilized for the improvement of the qualitative properties of foods and/or inhibit the development of chronic and degenerative diseases. Several studies have documented the beneficial health effects of natural food pigments, such as anthocyanins, chlorophylls, and carotenoids. These effects mainly depend on the stability, bioactivity, and bioavailability of these pigments. Various techniques have been used to encapsulate natural pigments. Anthocyanins are a member of flavonoid groups, which are responsible for attractive food colors. Due to the positive surface charge of anthocyanin molecules, they absorb light and gain color. The micro- and nano-encapsulation of ingredients using natural polymers are important techniques to improve their stability, solubility, and bioavailability. This review study aimed to elaborate on the recent advancement in the encapsulation of anthocyanin as an attractive natural pigment using five techniques, including coacervation, spray drying, liposomal system, electrospraying, and microwave-assisted encapsulation methods.
https://nmj.mums.ac.ir/article_14628_65ed42cc9194c86541fc915d166250c4.pdf
2020-04-01
87
97
10.22038/nmj.2020.07.001
Anthocyanins
Bioavailability
Bioactivity
Nano-encapsulation
Polymers
Davoud
Salarbashi
davoud.salarbashi2@gmail.com
1
Nanomedicine Research Center, Gonabad University of Medical Sciences, Gonabad, Iran
LEAD_AUTHOR
Javad
Bazeli
bazeli@yahoo.com
2
Department of Emergency Medicine, School of Nursing and Midwifery, Gonabad University of Medical Sciences, Gonabad, Iran
AUTHOR
Elham Fahmideh
Rad
3
Department of Applied Sciences, Applied Chemistry Section, Higher College of Technology (HCT), Muscat, Sultanate of Oman
AUTHOR
1.Gengatharan A, Dykes GA, Choo WS. Betalains: Natural plant pigments with potential application in functional foods. LWT-Food Sci and Technol. 2015; 64(2): 645-649.
1
2.Tang Y, Li X, Zhang B, Chen PX, Liu R, Tsao R. Characterisation of phenolics, betanins and antioxidant activities in seeds of three Chenopodium quinoa Willd. genotypes. Food Chem. 2015; 166: 380-388.
2
3.Azeredo HM. Betalains: properties, sources, applications, and stability–a review. Int J Food Sci & Technol. 2009; 44(12): 2365-2376.
3
4.Mohana D, Thippeswamy S, Abhishe R. Antioxidant, antibacterial, and ultraviolet-protective properties of carotenoids isolated from Micrococcus spp. Radiation Protection and Environment. 2013; 36(4): 168-174.
4
5.Butera D, Tesoriere L, Di Gaudio F, Bongiorno A, Allegra M, Pintaudi AM, Kohen R, Livrea M. Antioxidant activities of Sicilian prickly pear (Opuntia ficus indica) fruit extracts and reducing properties of its betalains: betanin and indicaxanthin. J Agr Food Chem. 2002; 50(23): 6895-6901.
5
6.Ravanfar R, Tamaddon AM, Niakousari M, Moein MR. Preservation of anthocyanins in solid lipid nanoparticles: Optimization of a microemulsion dilution method using the Placket–Burman and Box–Behnken designs. Food Chem. 2016; 199: 573-580.
6
7.Bell LN. Stability testing of nutraceuticals and functional foods. Handbook of nutraceuticals and functional foods: CRC Press; 2002. p. 504-519.
7
8.Gaonkar AG, Vasisht N, Khare AR, Sobel R. Microencapsulation in the food industry: a practical implementation guide: Elsevier; 2014.
8
9.Gutiérrez FJ, Albillos SM, Casas-Sanz E, Cruz Z, García-Estrada C, García-Guerra A, García-Reverter J, García-Suárez M, Gatón P, González-Ferrero C, Olabarrieta I, Olasagasti M, Rainieri S, Rivera-Patiño D, Rojo R, Romo-Hualde A, JoséSáiz-Abajo M, Musson M. Methods for the nanoencapsulation of β-carotene in the food sector. Trends Food Sci & Tech. 2013; 32(2): 73-83.
9
10.Gul K, Tak A, Singh A, Singh P, Yousuf B, Wani AA. Chemistry, encapsulation, and health benefits of β-carotene-A review. Cogent Food & Agriculture. 2015; 1(1): 1018696.
10
11.Rodriguez-Amaya DB. Update on natural food pigments-A mini-review on carotenoids, anthocyanins, and betalains. Food Res Int. 2018.
11
12.Horuz Tİ, Belibağlı KB. Nanoencapsulation by electrospinning to improve stability and water solubility of carotenoids extracted from tomato peels. Food Chem. 2018; 268: 86-93.
12
13.İnanç Horuz T, Belibağli KB. Nanoencapsulation of Carotenoids Extracted from Tomato Peels into Zein fibers by Electrospinning. J Sci Food and Agr. 2018. 99 (2): 759-766.
13
14.Pervaiz T, Songtao J, Faghihi F, Haider MS, Fang J. Naturally occurring anthocyanin structure, functions and biosynthetic pathway in fruit plants. J Plant Biochem Physiol. 2017; 5(2): 187.
14
15.Hou D-X. Potential mechanisms of cancer chemoprevention by anthocyanins. Curr Mol Med. 2003; 3(2): 149-159.
15
16.McDougall GJ, Fyffe S, Dobson P, Stewart D. Anthocyanins from red cabbage–stability to simulated gastrointestinal digestion. Phytochemistry. 2007; 68(9): 1285-1294.
16
17.Tall JM, Seeram NP, Zhao C, Nair MG, Meyer RA, Raja SN. Tart cherry anthocyanins suppress inflammation-induced pain behavior in rat. Behav Brain Res. 2004; 153(1): 181-188.
17
18.Schwarz M, Hillebrand S, Habben S, Degenhardt A, Winterhalter P. Application of high-speed countercurrent chromatography to the large-scale isolation of anthocyanins. Biochem Eng J. 2003; 14(3): 179-189.
18
19.Jones OG, McClements DJ. Functional biopolymer particles: design, fabrication, and applications. Comprehensive Reviews in Food Science and Food Safety. 2010; 9(4): 374-397.
19
20.Matalanis A, Jones OG, McClements DJ. Structured biopolymer-based delivery systems for encapsulation, protection, and release of lipophilic compounds. Food Hydr. 2011; 25(8): 1865-1880.
20
21.Fathi M, Emam-Djomeh Z, Sadeghi-Varkani A. Extraction, characterization and rheological study of the purified polysaccharide from Lallemantia ibrica seeds. Int J Biol Macromol. 2018; 120: 1265-1274.
21
22.Salehi E, Emam-Djomeh Z, Askari G, Fathi M. Opuntia ficus indica fruit gum: Extraction, characterization, antioxidant activity and functional properties. Carbohyd Polym. 2019; 206: 565-572.
22
23.Salehi E, Emam-Djomeh Z, Fathi M, Askari G. Opuntia ficus-indica Mucilage. Emerging Natural Hydrocolloids: Rheology and Functions. 2019.
23
24.de Vos P, Faas MM, Spasojevic M, Sikkema J. Encapsulation for preservation of functionality and targeted delivery of bioactive food components. Int dairy J. 2010; 20(4): 292-302.
24
25.Ko A, Lee JS, Sop Nam H, Gyu Lee H. Stabilization of black soybean anthocyanin by chitosan nanoencapsulation and copigmentation. J Food Biochem. 2017; 41(2): e12316.
25
26.Arroyo-Maya IJ, McClements DJ. Biopolymer nanoparticles as potential delivery systems for anthocyanins: Fabrication and properties. Food Res Int. 2015; 69: 1-8.
26
27.Sherahi MH, Fathi M, Zhandari F, Hashemi SMB, Rashidi A. Structural characterization and physicochemical properties of Descurainia sophia seed gum. Food Hydr. 2017; 66: 82-89.
27
28.Tiwari R, Takhistov P. Nanotechnology-enabled delivery systems for food functionalization and fortification. Nanotechnology research methods for foods and bioproducts Wiley-Blackwell, Oxford. 2012: 55-101.
28
29.de Moura SC, Berling CL, Germer SP, Alvim ID, Hubinger MD. Encapsulating anthocyanins from Hibiscus sabdariffa L. calyces by ionic gelation: Pigment stability during storage of microparticles. Food Chem. 2018; 241: 317-327.
29
30.Jafari S-M, Mahdavi-Khazaei K, Hemmati-Kakhki A. Microencapsulation of saffron petal anthocyanins with cress seed gum compared with Arabic gum through freeze drying. Carbohyd Polym. 2016; 140: 20-25.
30
31.Ge J, Yue P, Chi J, Liang J, Gao X. Formation and stability of anthocyanins-loaded nanocomplexes prepared with chitosan hydrochloride and carboxymethyl chitosan. Food Hydr. 2018; 74: 23-31.
31
32.Wise DL. Handbook of pharmaceutical controlled release technology: CRC Press; 2000.
32
33.Tan C, Selig MJ, Abbaspourrad A. Anthocyanin stabilization by chitosan-chondroitin sulfate polyelectrolyte complexation integrating catechin co-pigmentation. Carbohyd Polym. 2018; 181: 124-131.
33
34.Tan C, Celli GB, Selig MJ, Abbaspourrad A. Catechin modulates the copigmentation and encapsulation of anthocyanins in polyelectrolyte complexes (PECs) for natural colorant stabilization. Food Chem. 2018; 264: 342-349.
34
35.Tan C, Celli GB, Abbaspourrad A. Copigment-polyelectrolyte complexes (PECs) composite systems for anthocyanin stabilization. Food Hydr. 2018; 81: 371-9.
35
36.Yeo Y, Baek N, Park K. Microencapsulation methods for delivery of protein drugs. Biotechnol Bioproc Eng. 2001; 6(4): 213-230.
36
37.Nayak CA, Rastogi NK. Effect of selected additives on microencapsulation of anthocyanin by spray drying. Dry Technol. 2010; 28(12): 1396-1404.
37
38.Cho K, Wang X, Nie S, Shin DM. Therapeutic nanoparticles for drug delivery in cancer. Clin Cancer res. 2008; 14(5): 1310-1316.
38
39.Osorio C, Acevedo B, Hillebrand S, Carriazo J, Winterhalter P, Morales ALa. Microencapsulation by spray-drying of anthocyanin pigments from corozo (Bactris guineensis) fruit. J Agri Food Chem. 2010; 58(11): 6977-3685.
39
40.Huang X, Brazel CS. On the importance and mechanisms of burst release in matrix-controlled drug delivery systems. J ControlledRelease. 2001; 73(2-3): 121-136.
40
41.Siepmann J, Peppas N. Modeling of drug release from delivery systems based on hydroxypropyl methylcellulose (HPMC). Adv Drug Deliver Re. 2012; 64: 163-174.
41
42.Robert P, Gorena T, Romero N, Sepulveda E, Chavez J, Saenz C. Encapsulation of polyphenols and anthocyanins from pomegranate (Punica granatum) by spray drying. Int J Food SciTechnol. 2010; 45(7): 1386-1394.
42
43.Mahdavi SA, Jafari SM, Assadpour E, Ghorbani M. Storage stability of encapsulated barberry’s anthocyanin and its application in jelly formulation. J Food Eng. 2016; 181: 59-66.
43
44.Idham Z, Muhamad II, Sarmidi MR. Degradation kinetics and color stability of spray‐dried encapsulated anthocyanins from hibiscus sabdariffa l. J Food Proc Eng. 2012; 35(4): 522-542.
44
45.Reyes LF, Cisneros-Zevallos L. Degradation kinetics and colour of anthocyanins in aqueous extracts of purple-and red-flesh potatoes (Solanum tuberosum L.). Food Chem. 2007; 100(3): 885-894.
45
46.Idham Z, Muhamad II, MOHD SETAPAR SH, Sarmidi MR. Effect of thermal processes on roselle anthocyanins encapsulated in different polymer matrices. J Food Proc Pres. 2012; 36(2): 176-184.
46
47.Burin VM, Rossa PN, Ferreira‐Lima NE, Hillmann MC, Boirdignon‐Luiz MT. Anthocyanins: optimisation of extraction from Cabernet Sauvignon grapes, microcapsulation and stability in soft drink. Int J Food Sci Technol. 2011; 46(1): 186-193.
47
48.Wang W-D, Xu S-Y. Degradation kinetics of anthocyanins in blackberry juice and concentrate. J Food Eng. 2007; 82(3): 271-275.
48
49.Dangles O, Brouillard R. A spectroscopic method based on the anthocyanin copigmentation interaction and applied to the quantitative study of molecular complexes. Journal of the Chemical Society, Perkin Transactions 2. 1992 (2): 247-257.
49
50.Yousefi S, Emam-Djomeh Z, Mousavi M, Kobarfard F, Zbicinski I. Developing spray-dried powders containing anthocyanins of black raspberry juice encapsulated based on fenugreek gum. Adv Powder Technol. 2015; 26(2): 462-269.
50
51.Yousefi S, Emam-Djomeh Z, Mousavi S. Effect of carrier type and spray drying on the physicochemical properties of powdered and reconstituted pomegranate juice (Punica Granatum L.). J Food Sci Technol. 2011; 48(6): 677-684.
51
52.Chegini G, Ghobadian B. Spray dryer parameters for fruit juice drying. World J Agri Scie. 2007; 3(2): 230-236.
52
53.Ahmad M, Ashraf B, Gani A, Gani A. Microencapsulation of saffron anthocyanins using β glucan and β cyclodextrin: Microcapsule characterization, release behaviour & antioxidant potential during in-vitro digestion. Int J Biol Macromol. 2018; 109: 435-442.
53
54.Mueller D, Jung K, Winter M, Rogoll D, Melcher R, Kulozik U, Schwarz K, Richling E. Encapsulation of anthocyanins from bilberries–Effects on bioavailability and intestinal accessibility in humans. Food Chem. 2018; 248: 217-224.
54
55.Cai Y. Light stability of purple corn anthocyanins microencapsulated with different wall materials. 2018.
55
56.Xue J, Su F, Meng Y, Yurong G. Enhanced Stability of Red‐Fleshed Apple Anthocyanins by Copigmentation and Encapsulation. J the Sci Food and Agri. 2018.
56
57.da Fonseca Machado AP, Rezende CA, Rodrigues RA, Barbero GF, e Rosa PdTV, Martínez J. Encapsulation of anthocyanin-rich extract from blackberry residues by spray-drying, freeze-drying and supercritical antisolvent. Powder Technol. 2018; 340: 553-562.
57
58.Hao S, Wang Y, Wang B, Deng J, Liu X, Liu J. Rapid preparation of pH-sensitive polymeric nanoparticle with high loading capacity using electrospray for oral drug delivery. Mater Sci Eng: C. 2013; 33(8): 4562-4567.
58
59.Zhang S, Kawakami K. One-step preparation of chitosan solid nanoparticles by electrospray deposition. Int J Pharm. 2010; 397(1-2): 211-217.
59
60.Atay E, Fabra MJ, Martínez-Sanz M, Gomez-Mascaraque LG, Altan A, Lopez-Rubio A. Development and characterization of chitosan/gelatin electrosprayed microparticles as food grade delivery vehicles for anthocyanin extracts. Food Hydr. 2018; 77: 699-710.
60
61.Schafer V, von Briesen H, Andreesen R, Steffan A-M, Royer C, Troster S, Jorg K, Helga R. Phagocytosis of nanoparticles by human immunodeficiency virus (HlV)-infected macrophages: a possibility for antiviral drug targeting. Pharm Rese. 1992; 9(4): 541-546.
61
62.Hwang JM, Kuo HC, Lin CT, Kao ES. Inhibitory effect of liposome-encapsulated anthocyanin on melanogenesis in human melanocytes. Pharml Biol. 2013 ;51(8): 941-947.
62
63. Guldiken B, Gibis M, Boyacioglu D, Capanoglu E, Weiss J. Impact of liposomal encapsulation on degradation of anthocyanins of black carrot extract by adding ascorbic acid. Food & Funct. 2017;8(3):1085-1093.
63
64.Zhao L, Temelli F, Chen L. Encapsulation of anthocyanin in liposomes using supercritical carbon dioxide: Effects of anthocyanin and sterol concentrations. J Funct Food. 2017; 34:159-167.
64
65.Desai KGH, Jin Park H. Recent developments in microencapsulation of food ingredients. Dry Technol. 2005; 23(7): 1361-1394.
65
66.Mohd Nawi N, Muhamad II, Mohd Marsin A. The physicochemical properties of microwave‐assisted encapsulated anthocyanins from Ipomoea batatas as affected by different wall materials. Food Sci Nut. 2015; 3(2): 91-99.
66
67.Haghi A, Amanifard N. Analysis of heat and mass transfer during microwave drying of food products. Braz J Chem Eng. 2008; 25(3): 491-501.
67
ORIGINAL_ARTICLE
Polymer-based nanoadjuvants for hepatitis C vaccine: The perspectives of immunologists
The hepatitis C virus (HCV) is an infection that affects the liver tissues in humans, leading to the development of effective prophylactic and therapeutic HCV vaccines to prevent a global epidemic. Scientists consider it challenging to produce a therapeutic vaccine for the treatment of hepatocellular carcinoma as opposed to a preventative vaccine. However, several drawbacks are involved with a peptide vaccine, including the low immunogenicity of the protein, significant instability, difficulty in delivery, and inefficient presentation of the antigens. Therefore, the investigation of adjuvants (i.e., immunomodulators) to enhance the efficacy of the vaccine is essential. Nanoparticles could potentially serve as vaccine delivery vehicles, acting as adjuvants for the effective transfer of antigens. The safety and effectiveness of nanoparticles and liposomes in modern vaccinology have also been confirmed. Biodegradable nanopolymers such as polyesters, polylactic acid and the copolymers, polyorthoesters, polyanhydrides, and polycarbonates are commonly used owing to their proper qualities in the combination or loading for the prevention of the degradation of the delivered antigens. The present study is specifically focused on the polymer-based nanoparticles that are mostly comprised a poly (amino acid) based copolymer and poly (D, L-lactic-co-glycolide), which could act as adjuvants or potential immunomodulators for the systems providing effective HCV vaccine delivery.
https://nmj.mums.ac.ir/article_14867_c1e0f5224b38c87b9a56f29b20d31e12.pdf
2020-04-01
98
107
10.22038/nmj.2020.07.002
Adjuvants
HCV
Nanoparticles
Vaccine
Piyachat
Evelyn Roopngam
1
Visiting Professor, Department of Biotechnology, University of Verona, Veneto, Italy
LEAD_AUTHOR
Tirawat
Wannatung
nettirawat@gmail.com
2
Faculty of Medical Technology, Western University, Kanchanaburi, Thailand, 71170
AUTHOR
1.Guobuzaite A, Chokshi S, Balciuniene L, Voinic A, Stikleryte A, Zagminas K. Viral clearance or persistence after acute hepatitis C infection: interim results from a prospective study. Medicina (Kaunas). 2008; 44(7):510-520.
1
2.Khan S, Rai MA, Khan A, Farooqui A, Kazmi SU, Ali SH. Prevalence of HCV and HIV infections in 2005-Earthquake-affected areas of Pakistan. BMC Infect Dis. 2008; 8: 147.
2
3.El-Hazmi MM. Prevalence of HBV, HCV, HIV-1, 2 and HTLV-I/II infections among blood donors in a teaching hospital in the Central region of Saudi Arabia. Saudi Med J. 2004; 25(1): 26-33.
3
4.Arichi T, Saito T, Major ME, Belyakov IM, Shirai M, Engelhard VH. Prophylactic DNA vaccine for hepatitis C virus (HCV) infection: HCV-specific cytotoxic T lymphocyte induction and protection from HCV-recombinant vaccinia infection in an HLA-A2.1 transgenic mouse model. Proc Natl Acad Sci U S A. 2000; 97(1): 297-302.
4
5.Op De Beeck A, Cocquerel L, Dubuisson J. Biogenesis of hepatitis C virus envelope glycoproteins. J Gen Virol. 2001; 82(Pt 11): 2589-2595.
5
6.Kapadia SB, Chisari FV. Hepatitis C virus RNA replication is regulated by host geranylgeranylation and fatty acids. Proc Natl Acad Sci U S A. 2005; 102(7): 2561-2566.
6
7.Moradpour D, Brass V, Gosert R, Wolk B, Blum HE. Hepatitis C: molecular virology and antiviral targets. Trends Mol Med. 2002; 8(10): 476-482.
7
8.Calvo Manuel E, Nieto Sanchez A, Espinos Perez D. [Interferon treatment in chronic HCV hepatitis and autoimmune hypothyroidism]. An Med Interna. 2000; 17(3): 164-165.
8
9.Hoofnagle JH, Seeff LB. Peginterferon and ribavirin for chronic hepatitis C. N Engl J Med. 2006; 355(23): 2444-2451.
9
10.Kallinowski B, Liehr H, Moeller B, Stremmel W, Wechsler JG, Wiese M. Combination therapy with interferon-alpha 2b and ribavirin for the treatment of relapse patients and non-responders with chronic HCV infection. Z Gastroenterol. 2001; 39(3): 199-204, 6.
10
11.Iino S, Tomita E, Kumada H, Suzuki H, Toyota J, Kiyosawa K. Prediction of treatment outcome with daily high-dose IFN alpha-2b plus ribavirin in patients with chronic hepatitis C with genotype 1b and high HCV RNA levels: relationship of baseline viral levels and viral dynamics during and after therapy. Hepatol Res. 2004; 30(2): 63-70.
11
12.Laguno M, Murillas J, Blanco JL, Martinez E, Miquel R, Sanchez-Tapias JM, et al. Peginterferon alfa-2b plus ribavirin compared with interferon alfa-2b plus ribavirin for treatment of HIV/HCV co-infected patients. AIDS. 2004;18(13):F27-36.
12
13.Allard L, Cheynet V, Oriol G, Gervasi G, Imbert-Laurenceau E, Mandrand B. Antigenicity of recombinant proteins after regioselective immobilization onto polyanhydride-based copolymers. Bioconjug Chem. 2004;15(3): 458-466.
13
14.Xie Y, Xu DZ, Lu ZM, Luo KX, Jia JD, Wang YM, et al. [The influence of HCV genotype on the IFN treatment of patients with chronic hepatitis C]. Zhonghua Gan Zang Bing Za Zhi. 2004; 12(2): 72-75.
14
15.Idrees S, Ashfaq UA, Idrees N. Development of global consensus sequence of HCV glycoproteins involved in viral entry. Theor Biol Med Model. 2013; 10: 24.
15
16.Bartosch B, Dubuisson J, Cosset FL. Infectious hepatitis C virus pseudo-particles containing functional E1-E2 envelope protein complexes. J Exp Med. 2003; 197(5): 633-642.
16
17.Nielsen SU, Bassendine MF, Burt AD, Bevitt DJ, Toms GL. Characterization of the genome and structural proteins of hepatitis C virus resolved from infected human liver. J Gen Virol. 2004; 85(Pt 6): 1497-1507.
17
18.Weiner AJ, Christopherson C, Hall JE, Bonino F, Saracco G, Brunetto MR, et al. Sequence variation in hepatitis C viral isolates. J Hepatol. 1991; 13 Suppl 4: S6-14.
18
19.Ashfaq UA, Qasim M, Yousaf MZ, Awan MT, Jahan S. Inhibition of HCV 3a genotype entry through host CD81 and HCV E2 antibodies. J Transl Med. 2011; 9: 194.
19
20.Flint M, McKeating JA. The role of the hepatitis C virus glycoproteins in infection. Rev Med Virol. 2000; 10(2): 101-117.
20
21.Scarselli E, Ansuini H, Cerino R, Roccasecca RM, Acali S, Filocamo G. The human scavenger receptor class B type I is a novel candidate receptor for the hepatitis C virus. EMBO J. 2002; 21(19): 5017-5025.
21
22.Gardner JP, Durso RJ, Arrigale RR, Donovan GP, Maddon PJ, Dragic T. L-SIGN (CD 209L) is a liver-specific capture receptor for hepatitis C virus. Proc Natl Acad Sci U S A. 2003; 100(8): 4498-4503.
22
23.Helle F, Dubuisson J. Hepatitis C virus entry into host cells. Cell Mol Life Sci. 2008; 65(1): 100-112.
23
24.Monazahian M, Bohme I, Bonk S, Koch A, Scholz C, Grethe S. Low density lipoprotein receptor as a candidate receptor for hepatitis C virus. J Med Virol. 1999; 57(3): 223-229.
24
25.Liu J, Zhu L, Zhang X, Lu M, Kong Y, Wang Y. Expression, purification, immunological characterization and application of Escherichia coli-derived hepatitis C virus E2 proteins. Biotechnol Appl Biochem. 2001; 34(Pt 2): 109-119.
25
26.Feinstone SM, Hu DJ, Major ME. Prospects for prophylactic and therapeutic vaccines against hepatitis C virus. Clin Infect Dis. 55 Suppl 1: S25-32.
26
27.Hung CF, Ma B, Monie A, Tsen SW, Wu TC. Therapeutic human papillomavirus vaccines: current clinical trials and future directions. Expert Opin Biol Ther. 2008; 8(4): 421-439.
27
28.Le Corre P, Rytting JH, Gajan V, Chevanne F, Le Verge R. In vitro controlled release kinetics of local anaesthetics from poly(D,L-lactide) and poly(lactide-co-glycolide) microspheres. J Microencapsul. 1997; 14(2): 243-255.
28
29.Vogel FR. Improving vaccine performance with adjuvants. Clin Infect Dis. 2000; 30 Suppl 3: S266-70.
29
30.Wu JY, Gardner BH, Kushner NN, Pozzi LA, Kensil CR, Cloutier PA, et al. Accessory cell requirements for saponin adjuvant-induced class I MHC antigen-restricted cytotoxic T-lymphocytes. Cell Immunol. 1994; 154(1): 393-406.
30
31.Dupuis M, Murphy TJ, Higgins D, Ugozzoli M, van Nest G, Ott G. Dendritic cells internalize vaccine adjuvant after intramuscular injection. Cell Immunol. 1998; 186(1): 18-27.
31
32.Kovacsovics-Bankowski M, Rock KL. A phagosome-to-cytosol pathway for exogenous antigens presented on MHC class I molecules. Science. 1995; 267(5195): 243-246.
32
33.Zhou F, Huang L. Liposome-mediated cytoplasmic delivery of proteins: an effective means of accessing the MHC class I-restricted antigen presentation pathway. Immunomethods. 1994; 4(3): 229-235.
33
34.Audibert FM, Lise LD. Adjuvants: current status, clinical perspectives and future prospects. Immunol Today. 1993; 14(6): 281-284.
34
35.Unkeless JC, Scigliano E, Freedman VH. Structure and function of human and murine receptors for IgG. Annu Rev Immunol. 1988; 6: 251-281.
35
36.Phillips NC, Emili A. Enhanced antibody response to liposome-associated protein antigens: preferential stimulation of IgG2a/b production. Vaccine. 1992; 10(3): 151-158.
36
37.Pardoll DM. Paracrine cytokine adjuvants in cancer immunotherapy. Annu Rev Immunol. 1995; 13: 399-415.
37
38.Jankovic D, Caspar P, Zweig M, Garcia-Moll M, Showalter SD, Vogel FR. Adsorption to aluminum hydroxide promotes the activity of IL-12 as an adjuvant for antibody as well as type 1 cytokine responses to HIV-1 gp120. J Immunol. 1997; 159(5): 2409-2417.
38
39.Holmgren J, Lycke N, Czerkinsky C. Cholera toxin and cholera B subunit as oral-mucosal adjuvant and antigen vector systems. Vaccine. 1993; 11(12): 1179-1184.
39
40.Xu-Amano J, Kiyono H, Jackson RJ, Staats HF, Fujihashi K, Burrows PD. Helper T cell subsets for immunoglobulin A responses: oral immunization with tetanus toxoid and cholera toxin as adjuvant selectively induces Th2 cells in mucosa associated tissues. J Exp Med. 1993; 178(4): 1309-1320.
40
41.Wilson AD, Robinson A, Irons L, Stokes CR. Adjuvant action of cholera toxin and pertussis toxin in the induction of IgA antibody response to orally administered antigen. Vaccine. 1993; 11(2): 113-118.
41
42.Lindsay DS, Parton R, Wardlaw AC. Adjuvant effect of pertussis toxin on the production of anti-ovalbumin IgE in mice and lack of direct correlation between PCA and ELISA. Int Arch Allergy Immunol. 1994; 105(3): 281-288.
42
43.Oyewumi MO, Kumar A, Cui Z. Nano-microparticles as immune adjuvants: correlating particle sizes and the resultant immune responses. Expert Rev Vaccines. 9(9): 1095-1107.
43
44.Ferreira SA, Gama FM, Vilanova M. Polymeric nanogels as vaccine delivery systems. Nanomedicine. 2013; 9(2): 159-173.
44
45.De Geest BG, Willart MA, Hammad H, Lambrecht BN, Pollard C, Bogaert P. Polymeric multilayer capsule-mediated vaccination induces protective immunity against cancer and viral infection. ACS Nano. 2012; 6(3): 2136-2149.
45
46.Zhuang Y, Ma Y, Wang C, Hai L, Yan C, Zhang Y. PEGylated cationic liposomes robustly augment vaccine-induced immune responses: Role of lymphatic trafficking and biodistribution. J Control Release. 2012; 159(1): 135-142.
46
47.Reddy ST, Swartz MA, Hubbell JA. Targeting dendritic cells with biomaterials: developing the next generation of vaccines. Trends Immunol. 2006; 27(12): 573-579.
47
48.Bobardt MD, Cheng G, de Witte L, Selvarajah S, Chatterji U, Sanders-Beer BE. Hepatitis C virus NS5A anchor peptide disrupts human immunodeficiency virus. Proc Natl Acad Sci U S A. 2008; 105(14): 5525-5530.
48
49.Cheng G, Montero A, Gastaminza P, Whitten-Bauer C, Wieland SF, Isogawa M. A virocidal amphipathic {alpha}-helical peptide that inhibits hepatitis C virus infection in vitro. Proc Natl Acad Sci U S A. 2008; 105(8): 3088-3093.
49
50.Zhang J, Mulvenon A, Makarov E, Wagoner J, Knibbe J, Kim JO. Antiviral peptide nanocomplexes as a potential therapeutic modality for HIV/HCV co-infection. Biomaterials. 2013; 34(15): 3846-3857.
50
51.Zhang J, Garrison JC, Poluektova LY, Bronich TK, Osna NA. Liver-targeted antiviral peptide nanocomplexes as potential anti-HCV therapeutics. Biomaterials. 2015; 70: 37-47.
51
52.Katare YK, Panda AK. Immunogenicity and lower dose requirement of polymer entrapped tetanus toxoid co-administered with alum. Vaccine. 2006; 24(17): 3599-3608.
52
53.Diwan M, Elamanchili P, Cao M, Samuel J. Dose sparing of CpG oligodeoxynucleotide vaccine adjuvants by nanoparticle delivery. Curr Drug Deliv. 2004; 1(4): 405-412.
53
54.Hamdy S, Haddadi A, Hung RW, Lavasanifar A. Targeting dendritic cells with nano-particulate PLGA cancer vaccine formulations. Adv Drug Deliv Rev. 63(10-11): 943-955.
54
55.Kovacsovics-Bankowski M, Clark K, Benacerraf B, Rock KL. Efficient major histocompatibility complex class I presentation of exogenous antigen upon phagocytosis by macrophages. Proc Natl Acad Sci U S A. 1993; 90(11): 4942-4946.
55
56.Cruz LJ, Tacken PJ, Fokkink R, Joosten B, Stuart MC, Albericio F. Targeted PLGA nano- but not microparticles specifically deliver antigen to human dendritic cells via DC-SIGN in vitro. J Control Release. 2010; 144(2): 118-126.
56
57.Panyam J, Labhasetwar V. Biodegradable nanoparticles for drug and gene delivery to cells and tissue. Adv Drug Deliv Rev. 2003; 55(3): 329-347.
57
58.Sarti F, Perera G, Hintzen F, Kotti K, Karageorgiou V, Kammona O. In vivo evidence of oral vaccination with PLGA nanoparticles containing the immunostimulant monophosphoryl lipid A. Biomaterials. 2011; 32(16): 4052-4057.
58
59.Jeon HJ, Jeong YI, Jang MK, Park YH, Nah JW. Effect of solvent on the preparation of surfactant-free poly(DL-lactide-co-glycolide) nanoparticles and norfloxacin release characteristics. Int J Pharm. 2000; 207(1-2): 99-108.
59
60.Shen H, Ackerman AL, Cody V, Giodini A, Hinson ER, Cresswell P. Enhanced and prolonged cross-presentation following endosomal escape of exogenous antigens encapsulated in biodegradable nanoparticles. Immunology. 2006; 117(1): 78-88.
60
61.Sharma C, Khan MA, Mohan T, Shrinet J, Latha N, Singh N. A synthetic chimeric peptide harboring human papillomavirus 16 cytotoxic T lymphocyte epitopes shows therapeutic potential in a murine model of cervical cancer. Immunol Res.58(1): 132-138.
61
62.Roopngam P, Liu K, Mei L, Zheng Y, Zhu X, Tsai HI. Hepatitis C virus E2 protein encapsulation into poly d, l-lactic-co-glycolide microspheres could induce mice cytotoxic T-cell response. Int J Nanomedicine. 2016; 11: 5361-5370.
62
63.Alonso MJ, Gupta RK, Min C, Siber GR, Langer R. Biodegradable microspheres as controlled-release tetanus toxoid delivery systems. Vaccine. 1994; 12(4): 299-306.
63
64.Boehm U, Klamp T, Groot M, Howard JC. Cellular responses to interferon-gamma. Annu Rev Immunol. 1997; 15: 749-795.
64
65.Whitmire JK, Tan JT, Whitton JL. Interferon-gamma acts directly on CD8+ T cells to increase their abundance during virus infection. J Exp Med. 2005; 201(7): 1053-1059.
65
66.Mocikat R, Braumuller H, Gumy A, Egeter O, Ziegler H, Reusch U. Natural killer cells activated by MHC class I(low) targets prime dendritic cells to induce protective CD8 T cell responses. Immunity. 2003; 19(4): 561-569.
66
67.Abd Ellah NH, Tawfeek HM, John J, Hetta HF. Nanomedicine as a future therapeutic approach for Hepatitis C virus. Nanomedicine (Lond). 2019; 14(11): 1471-1491.
67
68.Hekmat S, Siadat SD, Aghasadeghi MR, Sadat SM, Bahramali G, Aslani MM, et al. From in-silico immunogenicity verification to in vitro expression of recombinant Core-NS3 fusion protein of HCV. Bratislavske lekarske listy. 2017; 118(4): 189-195.
68
69.Sabet S, George MA, El-Shorbagy HM, Bassiony H, Farroh KY, Youssef T, et al. Gelatin nanoparticles enhance delivery of hepatitis C virus recombinant NS2 gene. PLoS One. 2017; 12(7): e0181723.
69
70.Lee H, Jeong JH, Park TG. PEG grafted polylysine with fusogenic peptide for gene delivery: high transfection efficiency with low cytotoxicity. J Control Release. 2002; 79(1-3): 283-2891.
70
71.Yang Y, Kuang Y, Liu Y, Li W, Jiang Z, Xiao L, et al. Immunogenicity of multiple-epitope antigen gene of HCV carried by novel biodegradable polymers. Comparative immunology, microbiology and infectious diseases. 2011; 34(1): 65-72.
71
72.Sepulveda-Crespo D, Jimenez JL, Gomez R, De La Mata FJ, Majano PL, Munoz-Fernandez MA. Polyanionic carbosilane dendrimers prevent hepatitis C virus infection in cell culture. Nanomedicine. 2017; 13(1): 49-58.
72
ORIGINAL_ARTICLE
Docetaxel delivery using folate-targeted liposomes: in vitro and in vivo studies
Objective(s): Folate-targeted liposomes have been well considered in folate receptor (FR) overexpressing cells including MCF-7 and 4T1 cells in vitro and in vivo. The objective of this study is to design an optimum folate targeted liposomal formulations which show the best liposome cell uptake to tumor cells.Material and Methods: In this study, we prepared and characterized different targeted formulations and a nontargeted form as a control. Physicochemical analysis showed that the liposomes had homogeneous population and appropriate size to accumulate to tumor sites through the enhanced permeation and retention (EPR) mechanism. Moreover, we compared the cell uptake of folate targeted liposomal docetaxel compared to nontargeted liposomes in vitro. Results: The in vitro drug release profile of the formulations at different time points showed none of the formulations did not has burst release. However, targeted liposomes accumulated in tumor tissue in vivo less than nontargeted formulations which could be attributed to their uptake by RES due to relatively greater size of targeted formulations. It is presumable that analyze the biodistribution process at longer time points and the molecular mechanisms behind the tissue accumulation could clear the issue. Conclusion: We conclude that success in vitro studies holds the promise of folate targeting strategy and in vivo study merits further investigations.
https://nmj.mums.ac.ir/article_14009_ad19994e2e45b9b5d59a39602af7bcb5.pdf
2020-04-01
108
114
10.22038/nmj.2020.07.003
Docetaxel Encapsulation
Folate Targeting
Liposomes
Tumor Drug Delivery
Roghayyeh
Vakili-Ghartavol
1
Department of Medical Nanotechnology, School of Advanced Technologies in Medicine, Tehran University of Medical Sciences, Tehran, Iran
AUTHOR
Mahmoud Reza
Jaafari
jafarimr@mums.ac.ir
2
Department of Pharmaceutical Nanotechnology, School of Pharmacy, Mashhad University of Medical Sciences, Mashhad, Iran
AUTHOR
Amin Reza
Nikpoor
nikpoora@gmail.com
3
Molecular Medicine Research Center Hormozgan Health Institute, Hormozgan University of Medical Sciences, Bandar Abbas, Iran
AUTHOR
Seyed Mahdi
Rezayat
rezayat@tums.ac.ir
4
Department of Medical Nanotechnology, School of Advanced Technologies in Medicine, Tehran University of Medical Sciences, Tehran, Iran
LEAD_AUTHOR
1. Pfirschke C, Engblom C, Rickelt S, Cortez-Retamozo V, Garris C, Pucci F, Yamazaki T, Poirier-Colame V, Newton A, Redouane Y, Lin Y, Wojtkiewicz G, Iwamoto Y, Mino-Kenudson M,Huynh T,Hynes R, Freeman G, Kroemer G, Zitvogel L, Weissleder R, Pittet M. Immunogenic chemotherapy sensitizes tumors to checkpoint blockade therapy. Immunity. 2016; 44: 343-354.
1
2. Cai X, Jia X, Gao W, Zhang K, Ma M, Wang S, Zheng Y, Shi J , Chen H. A Versatile Nanotheranostic Agent for Efficient Dual‐Mode Imaging Guided Synergistic Chemo‐Thermal Tumor Therapy. Adv Funct Mater. 2015; 25: 2520-2529.
2
3. Long D, Liu T, Tan L, Shi H, Liang P, Tang S, Yu J, Dou J, Meng X. Multisynergistic platform for tumor therapy by mild microwave irradiation-activated chemotherapy and enhanced ablation. ACS nano. 2016; 10: 9516-9528.
3
4. Zhang L, Su H, Cai J, Cheng D, Ma Y, Zhang J, Zhou C, Liu S, Shi H, Zhang Y, Zhang C. A multifunctional platform for tumor angiogenesis-targeted chemo-thermal therapy using polydopamine-coated gold nanorods. ACS nano. 2016; 10(11): 10404-10417.
4
5. Riviere K, Huang Z, Jerger K, Macaraeg N, Szoka Jr FC. Antitumor effect of folate-targeted liposomal doxorubicin in KB tumor-bearing mice after intravenous administration. J Drug Target. 2011; 19: 14-24.
5
6. Yi Q, Ma J, Kang K, Gu Z. Bioreducible nanocapsules for folic acid-assisted targeting and effective tumor-specific chemotherapy. Int J Nanomed. 2018; 13: 653.
6
7. Guo F, Yu M, Wang J, Tan F, Li N. Smart IR780 theranostic nanocarrier for tumor-specific therapy: hyperthermia-mediated bubble-generating and folate-targeted liposomes. ACS Appl Mater Interfaces. 2015; 7: 20556-20567.
7
8. Lu Y, Low PS. Folate-mediated delivery of macromolecular anticancer therapeutic agents. Adv. Drug Deliv Rev. 2012; 64: 342-352.
8
9. Leamon CP, Reddy JA. Folate-targeted chemotherapy. Adv Drug Deliv Rev. 2004; 56: 1127-1141.
9
10. Patil Y, Shmeeda H, Amitay Y, Ohana P, Kumar S, Gabizon A. Targeting of folate-conjugated liposomes with co-entrapped drugs to prostate cancer cells via prostate-specific membrane antigen (PSMA). Nanomedicine. 2018; 14: 1407-1416.
10
11. Patil Y, Amitay Y, Ohana P, Shmeeda H, Gabizon A. Targeting of pegylated liposomal mitomycin-C prodrug to the folate receptor of cancer cells: Intracellular activation and enhanced cytotoxicity. J Control Release. 2016; 225: 87-95.
11
12. Zhai G, Wu J, Xiang G, Mao W, Yu B, Li H, Piao L, Lee LJ, Lee, RJ. Preparation, characterization and pharmacokinetics of folate receptor-targeted liposomes for docetaxel delivery. J Nanosci Nanotechnol. 2009; 9: 2155-2161.
12
13. Kumar P, Huo P, Liu B. Formulation Strategies for Folate-Targeted Liposomes and Their Biomedical Applications. Pharmaceutics. 2019; 11: 381.
13
14. Goren D, Horowitz AT, Tzemach D, Tarshish M, Zalipsky S, Gabizon A. Nuclear delivery of doxorubicin via folate-targeted liposomes with bypass of multidrug-resistance efflux pump. Clin. Cancer Res. 2000; 6: 1949-1957.
14
15. Alibolandi M, Abnous K, Sadeghi F, Hosseinkhani H, Ramezani M, Hadizadeh F. Folate receptor-targeted multimodal polymersomes for delivery of quantum dots and doxorubicin to breast adenocarcinoma: in vitro and in vivo evaluation. Int J Pharm. 2016; 500: 162-178.
15
16. Nikpoor AR, Tavakkol-Afshari J, Gholizadeh Z, Sadri K, Babaei MH, Chamani J, Badiee A, Jalali SA, JaafarI MR. Nanoliposome-mediated targeting of antibodies to tumors: IVIG antibodies as a model. Int J Pharm. 2015; 495: 162-170.
16
17. Tanhaeian A, Jaafari MR, Ahmadi FS, Vakili‐Ghartavol R, Sekhavati MH. Secretory expression of a chimeric peptide in Lactococcus lactis: assessment of its cytotoxic activity and a deep view on its interaction with cell-surface glycosaminoglycans by molecular modeling. Probiotics & Antimicro Prot. 2019; 11: 1034-1041.
17
18. Nikpoor AR, Tavakkol-Afshari J, Sadri K, Jalali SA, Jaafari MR. Improved tumor accumulation and therapeutic efficacy of CTLA-4-blocking antibody using liposome-encapsulated antibody: In vitro and in vivo studies. Nanomedicine. 2017; 13: 2671-2682.
18
19. Zahmatkeshan M, Gheybi F, Rezayat SM, Jaafari MR. Improved drug delivery and therapeutic efficacy of PEgylated liposomal doxorubicin by targeting anti-HER2 peptide in murine breast tumor model. Eur J Pharm Sci. 2016; 86: 125-135.
19
20. Amin M, Bagheri M, Mansourian M, Jaafari MR, ten Hagen TL. Regulation of in vivo behavior of TAT-modified liposome by associated protein corona and avidity to tumor cells. Int J Nanomedicine. 2018; 13:7441.
20
21. Arabi L, Badiee A, Mosaffa F, Jaafari MR. Targeting CD44 expressing cancer cells with anti-CD44 monoclonal antibody improves cellular uptake and antitumor efficacy of liposomal doxorubicin. J Control Release. 2015; 220: 275-286.
21
22. Wang L, Li M, Zhang N. Folate-targeted docetaxel-lipid-based-nanosuspensions for active-targeted cancer therapy. Int J Nanomed. 2012; 7: 3281.
22
23. Awasthi V, Garcia D, Goins B, Phillips WT. Circulation and biodistribution profiles of long-circulating PEG-liposomes of various sizes in rabbits. Int J Pharm. 2003; 253: 121-132.
23
24. Fisher ML, Colic M, Rao MP, Lange FF. Effect of silica nanoparticle size on the stability of alumina/silica suspensions. J Am Ceram Soc. 2001; 84: 713-718.
24
25. Mozafari MR, Khosravi-Darani K, Borazan GG, Cui J, Pardakhty A, Yurdugul S. Encapsulation of food ingredients using nanoliposome technology. International Journal of Food Properties. 2008; 11: 833-844.
25
ORIGINAL_ARTICLE
In vitro and In vivo Investigation of poly(lactic acid)/hydroxyapatite nanoparticle scaffold containing nandrolone decanoate for the regeneration of critical-sized bone defects
Objective(s): Bone tissue engineering is aimed at the fabrication of bone graft to ameliorate bone defects without using autografts or allografts. Materials and Methods: In the present study, the coprecipitation method was used to prepare hydroxyapatite (HA) nanoparticles containing nandrolone. To do so, 12.5, 25, and 50 mg of nandrolone were loaded into poly(lactic acid) (PLA)/nano-HA, and the freeze casting method was used to fabricate porous scaffolds. The morphology, mechanical strength, wettability, porosity, degradation, blood compatibility, and cellular response of the scaffolds were evaluated using various tests. For further investigation, the developed scaffolds were incorporated into the rat calvaria defect model, and their effects on bone healing were evaluated. Results: The obtained results indicated that the fabricated scaffolds had the approximate porosity of 80% and compress strength of 6.5 MPa. Moreover, the prepared scaffolds had appropriate hydrophilicity, weight loss, and blood compatibility. Furthermore, the histopathological findings demonstrated that the defects filled with the PLA/nano-HA scaffolds containing 25 mg nandrolone healed better compared to the other study groups.Conclusion: Therefore, it was concluded that the scaffolds containing nandrolone could be used in bone regeneration.
https://nmj.mums.ac.ir/article_14202_84d69c22bd3bc015aa9d918fbb45e4e9.pdf
2020-04-01
115
123
10.22038/nmj.2020.07.004
Bone Healing
Freeze Casting Method
Hydroxyapatite
Nandrolone
Scaffold
Majid
Salehi
msalehi.te1392@gmail.com
1
Department of Tissue Engineering, School of Medicine, Shahroud University of Medical Sciences, Shahroud, Iran
AUTHOR
Arman
Ai
arman.ai@gmail.com
2
School of Medicine, Tehran University of Medical Sciences, Tehran, Iran
AUTHOR
Arian
Ehterami
arian.ehterami@srbiau.ac.ir
3
Department of Mechanical and Aerospace Engineering, Islamic Azad University, Science and Research Branch, Tehran, Iran
AUTHOR
Masoumeh
Einabadi
4
Department of Biology, Islamic Azad University, Jahrom Branch, Jahrom, Iran
AUTHOR
Alireza
Taslimi
alirezata13@gmail.com
5
Dentistry Student, Scientific Research Center, School of Dentistry, Tehran University of Medical Sciences, Tehran, Iran
AUTHOR
Armin
Ai
arianehterami@yahoo.com
6
Dentistry Student, Scientific Research Center, School of Dentistry, Tehran University of Medical Sciences, Tehran, Iran
LEAD_AUTHOR
Hamta
Akbarzadeh
hakbarzadeh@student.tums.ac.ir
7
Dentistry Student, Scientific Research Center, School of Dentistry, Tehran University of Medical Sciences, Tehran, Iran
AUTHOR
Ghazal Jabal
Ameli
8
Dentistry Student, Scientific Research Center, School of Dentistry, Tehran University of Medical Sciences, Tehran, Iran
AUTHOR
Saeed
Farzamfar
saeed.tums1991@gmail.com
9
Department of Tissue Engineering and Applied Cell Sciences, School of Advanced Technologies in Medicine, Tehran University of Medical Sciences, Tehran 1417755469, Iran
AUTHOR
Sadegh
Shirian
shirian@gmail.com
10
Department of Pathology, School of Veterinary Medicine, Shahrekord University, Shahrekord, Iran
AUTHOR
Nahal
Azimi
majidsalehiezd@yahoo.com
11
Dentistry Student, Scientific Research Center, School of Dentistry, Tehran University of Medical Sciences, Tehran, Iran
AUTHOR
Faezeh
Sadeghi
salehim@shmu.ac.ir
12
Dentistry Student, Scientific Research Center, School of Dentistry, Tehran University of Medical Sciences, Tehran, Iran
AUTHOR
Naghmeh
Bahrami
n-bahrami@sina.tums.ac.ir
13
Craniomaxillofacial Research Center, Tehran University of Medical Sciences, Tehran, Iran
AUTHOR
Arash
goodarzi
dvm.goodarzi86@yahoo.com
14
Department of Tissue Engineering, School of Advanced Technologies in Medicine, Fasa University of Medical Sciences, Fasa, Iran
AUTHOR
Jafar
Ai
15
Department of Tissue Engineering and Applied Cell Sciences, School of Advanced Technologies in Medicine, Tehran University of Medical Sciences, Tehran 1417755469, Iran
AUTHOR
1.Guo B, Glavas L, Albertsson A-C. Biodegradable and electrically conducting polymers for biomedical applications. Prog Polym Sci. 2013; 38(9): 1263-1286.
1
2.Nabavi MH, Salehi M, Ehterami A, Bastami F, Semyari H, Tehranchi M, Nabavi MA, Semyari H. A collagen-based hydrogel containing tacrolimus for bone tissue engineering. Drug Deliv Transl Res. 2019: 1-14.
2
3.Semyari H, Salehi M, Taleghani F, Ehterami A, Bastami F, Jalayer T, Semyari H, Hamed Nabavi M, Semyari H. Fabrication and characterization of collagen–hydroxyapatite-based composite scaffolds containing doxycycline via freeze-casting method for bone tissue engineering. J Biomater Appl. 2018; 33(4): 501-513.
3
4.Salehi M, Bastami F. Characterization of wet-electrospun poly (ε-caprolactone)/poly (L-lactic) acid with calcium phosphates coated with chitosan for bone engineering. RRR 2016;1(2):69-74.
4
5.Ehterami A, Kazemi M, Nazari B, Saraeian P, Azami M. Fabrication and characterization of highly porous barium titanate based scaffold coated by Gel/HA nanocomposite with high piezoelectric coefficient for bone tissue engineering applications. J Mech Behav Biomed Mater. 2018; 79: 195-202.
5
6.Deville S, Saiz E, Tomsia AP. Freeze casting of hydroxyapatite scaffolds for bone tissue engineering. Biomater. 2006; 27(32): 5480-5489.
6
7.Farzamfar S, Naseri-Nosar M, Sahrapeyma H, Ehterami A, Goodarzi A, Rahmati M, Ahmadi Lakalayeh G, Ghorbani S, Vaez A, Salehi M. Tetracycline hydrochloride-containing poly (ε-caprolactone)/poly lactic acid scaffold for bone tissue engineering application: in vitro and in vivo study. Int J Polym Mater. 2019; 68(8): 472-479.
7
8.Alexandre M, Beyer G, Henrist C, Cloots R, Rulmont A, Jérôme R, Dubois P. “One-Pot” Preparation of Polymer/Clay Nanocomposites Starting from Na+ Montmorillonite. 1. Melt Intercalation of Ethylene− Vinyl Acetate Copolymer. Chem Mater. 2001; 13(11): 3830-3832.
8
9.Lee JH, Park TG, Park HS, Lee DS, Lee YK, Yoon SC, Nam J-D. Thermal and mechanical characteristics of poly (L-lactic acid) nanocomposite scaffold. Biomater. 2003; 24(16): 2773-2778.
9
10.Samadian H, Salehi M, Farzamfar S, Vaez A, Ehterami A, Sahrapeyma H, Goodarzi A, Ghorbani S. In vitro and in vivo evaluation of electrospun cellulose acetate/gelatin/hydroxyapatite nanocomposite mats for wound dressing applications. Artif Cells Nanomed Biotechnol. 2018; 46(sup1): 964-974.
10
11.Kumta PN, Sfeir C, Lee D-H, Olton D, Choi D. Nanostructured calcium phosphates for biomedical applications: novel synthesis and characterization. Acta Biomater. 2005; 1(1): 65-83.
11
12.Matsumoto T, Okazaki M, Inoue M, Yamaguchi S, Kusunose T, Toyonaga T, Hamada Y, Takahashi J. Hydroxyapatite particles as a controlled release carrier of protein. Biomater. 2004; 25(17): 3807-3812.
12
13.Mizushima Y, Ikoma T, Tanaka J, Hoshi K, Ishihara T, Ogawa Y, Ueno A. Injectable porous hydroxyapatite microparticles as a new carrier for protein and lipophilic drugs. J Control Release. 2006; 110(2): 260-265.
13
14.Tamm T, Peld M. Computational study of cation substitutions in apatites. J Solid State Chem. 2006; 179(5): 1581-1587.
14
15.P Busardo F, Frati P, Di Sanzo M, Napoletano S, Pinchi E, Zaami S, Fineschi V. The impact of nandrolone decanoate on the central nervous system. Curr Neuropharmacol. 2015; 13(1):122-131.
15
16.Pardridge WM. 4 Serum bioavailability of sex steroid hormones. Best Pract Res Clin Endocrinol Metab. 1986; 15(2): 259-278.
16
17.Riezzo I, Turillazzi E, Bello S, Cantatore S, Cerretani D, Di Paolo M, Fiaschi AI, Frati P, Neri M, Pedretti M. Chronic nandrolone administration promotes oxidative stress, induction of pro-inflammatory cytokine and TNF-α mediated apoptosis in the kidneys of CD1 treated mice. Toxicol Appl Pharmacol. 2014; 280(1): 97-106.
17
18.Bahrke MS, Yesalis CE, Wright JE. Psychological and behavioural effects of endogenous testosterone and anabolic-androgenic steroids. Sports Med. 1996; 22(6): 367-390.
18
19.Buckley WE, Yesalis CE, Friedl KE, Anderson WA, Streit AL, Wright JE. Estimated prevalence of anabolic steroid use among male high school seniors. Jama. 1988; 260(23): 3441-3445.
19
20.Durant RH, Rickert VI, Ashworth CS, Newman C, Slavens G. Use of multiple drugs among adolescents who use anabolic steroids. N Engl J Med Overseas Ed 1993;328(13):922-926.
20
21.Kopera H. The history of anabolic steroids and a review of clinical experience with anabolic steroids. Acta Endocrinol. 1985; 110(3 Suppla): S11-S18.
21
22.Eklöf A-C, Thurelius A-M, Garle M, Rane A, Sjöqvist F. The anti-doping hot-line, a means to capture the abuse of doping agents in the Swedish society and a new service function in clinical pharmacology. Eur J Clin Pharmacol. 2003; 59(8-9): 571-577.
22
23.Verroken M. Ethical aspects and the prevalence of hormone abuse in sport. J Endocrinol. 2001; 170(1): 49-54.
23
24.Sun L, Pan J, Peng Y, Wu Y, Li J, Liu X, Qin Y, Bauman WA, Cardozo C, Zaidi M. Anabolic steroids reduce spinal cord injury-related bone loss in rats associated with increased Wnt signaling. J Spinal Cord Med. 2013; 36(6): 616-622.
24
25.Ahmad F, Yunus SM, Asghar A, Faruqi N. Influence of anabolic steroid on tibial fracture healing in rabbits–a study on experimental model. J Clin Diagn Res. 2013; 7(1): 93.
25
26.Salehi M, Naseri-Nosar M, Ebrahimi-Barough S, Nourani M, Vaez A, Farzamfar S, Ai J. Regeneration of sciatic nerve crush injury by a hydroxyapatite nanoparticle-containing collagen type I hydrogel. Jpn J Physiol. 2018; 68(5): 579-587.
26
27.Tanaka K, Shiga T, Katayama T. Fabrication of hydroxyapatite/PLA composite nanofiber by electrospinning. High Performance and Optimum Design of Structures and Materials II. 2016; 166: 371.
27
28.Shahrezaee M, Salehi M, Keshtkari S, Oryan A, Kamali A, Shekarchi B. In vitro and in vivo investigation of PLA/PCL scaffold coated with metformin-loaded gelatin nanocarriers in regeneration of critical-sized bone defects. Nanomed. 2018; 14(7): 2061-2073.
28
29.Hannink G, Arts JC. Bioresorbability, porosity and mechanical strength of bone substitutes: what is optimal for bone regeneration? Inj. 2011; 42: S22-S25.
29
30.Karp JM, Shoichet MS, Davies JE. Bone formation on two‐dimensional poly (DL‐lactide‐co‐glycolide)(PLGA) films and three‐dimensional PLGA tissue engineering scaffolds in vitro. J Biomed Mater Res A. 2003; 64(2): 388-396.
30
31.Bose S, Roy M, Bandyopadhyay A. Recent advances in bone tissue engineering scaffolds. Trends Biotechnol. 2012; 30(10): 546-554.
31
32.Bat E, Zhang Z, Feijen J, Grijpma DW, Poot AA. Biodegradable elastomers for biomedical applications and regenerative medicine. Regen Med. 2014; 9(3): 385-398.
32
33.Abbasian M, Massoumi B, Mohammad-Rezaei R, Samadian H, Jaymand M. Scaffolding polymeric biomaterials: Are naturally occurring biological macromolecules more appropriate for tissue engineering? Int J Biol Macromol. 2019.
33
34.Liao S, Cui F, Zhang W, Feng Q. Hierarchically biomimetic bone scaffold materials: nano‐HA/collagen/PLA composite. J Biomed Mater Res B. 2004; 69(2): 158-165.
34
35.Yoshikawa H, Myoui A. Bone tissue engineering with porous hydroxyapatite ceramics. Art Org. 2005; 8(3): 131-136.
35
36.Akindoyo JO, Beg MD, Ghazali S, Heim HP, Feldmann M. Effects of surface modification on dispersion, mechanical, thermal and dynamic mechanical properties of injection molded PLA-hydroxyapatite composites. Compos A. 2017; 103: 96-105.
36
37.Wu C, Ramaswamy Y, Zhu Y, Zheng R, Appleyard R, Howard A, Zreiqat H. The effect of mesoporous bioactive glass on the physiochemical, biological and drug-release properties of poly (DL-lactide-co-glycolide) films. Biomater. 2009; 30(12): 2199-2208.
37
38.Yuan J, Shen J, Kang IK. Fabrication of protein‐doped PLA composite nanofibrous scaffolds for tissue engineering. Polym Int. 2008; 57(10):1188-1193.
38
39.Fratzl P, Gupta H, Paschalis E, Roschger P. Structure and mechanical quality of the collagen–mineral nano-composite in bone. J Mater Chem. 2004; 14(14): 2115-2123.
39
40.Yuan H, Li Y, De Bruijn J, De Groot K, Zhang X. Tissue responses of calcium phosphate cement: a study in dogs. Biomater. 2000; 21(12): 1283-1290.
40
41.Kilpadi KL, Chang PL, Bellis SL. Hydroxylapatite binds more serum proteins, purified integrins, and osteoblast precursor cells than titanium or steel. J Biomed Mater Res A. 2001; 57(2): 258-267.
41
42.Karageorgiou V, Kaplan D. Porosity of 3D biomaterial scaffolds and osteogenesis. Biomater. 2005; 26(27): 5474-5491.
42
43.Boccaccio A, Uva AE, Fiorentino M, Bevilacqua V, Pappalettere C, Monno G. A Computational Approach to the Design of Scaffolds for Bone Tissue Engineering. Adv Biomater. 2018. p. 111-117.
43
44.Murphy CM, Haugh MG, O’Brien FJ. The effect of mean pore size on cell attachment, proliferation and migration in collagen–glycosaminoglycan scaffolds for bone tissue engineering. Biomater. 2010; 31(3): 461-466.
44
45.Ramesh N, Moratti SC, Dias GJ. Hydroxyapatite–polymer biocomposites for bone regeneration: A review of current trends. J Biomed Mater Res B. 2018; 106(5): 2046-2057.
45
46.Huyck L, Ampe C, Van Troys M. The XTT cell proliferation assay applied to cell layers embedded in three-dimensional matrix. Assay Drug Dev Technol. 2012; 10(4): 382-392.
46
47.Zeng Q, Hong W. The emerging role of the hippo pathway in cell contact inhibition, organ size control, and cancer development in mammals. Cancer cell. 2008; 13(3): 188-192.
47
48.Vannucci L, Brandi ML. Healing of the bone with anti-fracture drugs. Expert Opin Pharmacother. 2016; 17(17): 2267-2272.
48
49.Demling RH. Oxandrolone, an anabolic steroid, enhances the healing of a cutaneous wound in the rat. Wound Repair Regen. 2000; 8(2): 97-102.
49
50.Guimarães APFGM, Butezloff MM, Zamarioli A, Issa JPM, Volpon JB. Nandrolone decanoate appears to increase bone callus formation in young adult rats after a complete femoral fracture. Acta Cir Bras. 2017; 32(11): 924-934.
50
51.Ogasawara A, Nakajima A, Nakajima F, Goto K-i, Yamazaki M. Molecular basis for affected cartilage formation and bone union in fracture healing of the streptozotocin-induced diabetic rat. Bone. 2008; 43(5): 832-839.
51
52.Urabe K, Kim HJ, Sarkar G, Bronk JT, Bolander ME. Determination of the complete cDNA sequence of rat type II collagen and evaluation of distinct expression patterns of types IIA and IIB procollagen mRNAs during fracture repair in rats. Ortho Sci. 2003; 8(4): 585-590.
52
53.Pansieri JC, Esteves A, Junior WCR. Anabolic Steroids Effects on Bone Regeneration. Sport Sci. 2019; 7(3): 88-93.
53
ORIGINAL_ARTICLE
Synergistic cellular toxicity and uptake effects of iodixanol conjugated to anionic linear globular dendrimer G2
Objective(s): Early diagnosis of cancer using noninvasive imaging techniques has been discussed in several recent studies. The present study aimed to assess the synergistic effects of iodixanol-conjugated polyethylene glycol (PEG)-citrate (anionic linear globular) dendrimer G2 on MCF-7 breast cancer cells and human embryonic kidney 293 (HEK293) cells. Materials and Methods: PEG-citrate dendrimer G2 was synthesized and purified. The product was characterized using atomic force microscopy (AFM), electron energy loss spectroscopy (EELS), dynamic light scattering (DLS). At the next stage, the product was conjugated to iodixanol, purified and lyophilized. The cytotoxic effects of the iodixanol, plain PEG-citrate dendrimer G2, and iodixanol-PEG-citrate dendrimer G2 complex were evaluated using methylthiazole-tetrazolium (MTT) assay on the MCF-7 and HEK293 cells. Inductively coupled plasma mass spectrometry (ICP MS) is a mass spectrometry technique, which applies inductively coupled plasma to ionize samples.Results: According to the obtained results, the uptake of PEG-citrate dendrimer G2 iodixanol increased significantly compared to iodixanol alone (P<0.05), indicating the importance of lack of significant in-vitro toxicity. Moreover, in the particle size and higher negative zeta potential confirmed the loading of iodixanol in dendrimer G2. Increase, the loading of iodixanol in dendrimer was confirmed by the chemical shifts in HNMR. Conclusion: Therefore, it was concluded that the addition of anionic linear globular dendrimer G2 to iodixanol affected the cellular uptake of the drug with no significant toxicity. Recent findings also confirmed that this novel complex could be applied as an effective cancer imaging agent for molecular biology and molecular imaging applications.
https://nmj.mums.ac.ir/article_14531_4935da6a8834738aebab4aa9b0a1eac5.pdf
2020-04-01
124
130
10.22038/nmj.2020.07.005
Cellular Toxicity
Iodixanol
Linear Globular Dendrimer
Mitra
Kiani
mitrakiani@yahoo.com
1
Department of Radiopharmacy, School of Pharmacy, Tehran University of Medical Sciences, Tehran, Iran
AUTHOR
Paria
Mojarrad
pariamojarrad@yahoo.com
2
School of Pharmacy, Tehran University of Medical Sciences, International Branch, Tehran, Iran
AUTHOR
Mehdi
Shafiee Ardestani
shafieeardestani@gmail.com
3
Department of Radiopharmacy, School of Pharmacy, Tehran University of Medical Sciences, Tehran, Iran
LEAD_AUTHOR
1. Siegel R L, Miller K D , Jemal A. Cancer statistics. CA Cancer J Clin. 2016; (66): 7-30.
1
2. Smith R A. Cancer screening in the United States, 2015: a review of current American cancer society guidelines and current issues in cancer screening. CA Cancer J Clin. 2015; (65): 30-54.
2
3. Imperiale T F. Multitarget stool DNA testing for colorectal-cancer screening. N Engl J Med. 2014; (370): 1287-1297.
3
4. Choi K. Effect of endoscopy screening on stage at gastric cancer diagnosis: results of the National Cancer Screening Programme in Korea. Br J Cancer. 2015; (112): 608-612.
4
5. Heitzer E, Ulz P , Geigl J B. Circulating tumor DNA as a liquid biopsy for cancer. Clin Chem. 2015; (61): 112-123.
5
6. Hussain T , Nguyen Q T. Molecular imaging for cancer diagnosis and surgery. Adv Drug Deliv Rev. 2014; (66): 90-100.
6
7. Chen H, Zhen Z, Todd T, Chu P K , Xie J. Nanoparticles for improving cancer diagnosis. Mater Sci Eng R Rep. 2013; (74): 35-69.
7
8. Sepúlveda-Crespo D, Gómez R, De La Mata F J, Jiménez J L , Muñoz-Fernández M Á. Polyanionic carbosilane dendrimer-conjugated antiviral drugs as efficient microbicides: Recent trends and developments in HIV treatment/therapy. Nanomedicine: nanotechnology, biology, and medicine. 2015; (11): 1481-1498.
8
9. Worley B V, Slomberg D L , Schoenfisch M H. Nitric oxide-releasing quaternary ammonium-modified poly (amidoamine) dendrimers as dual action antibacterial agents. Bioconjug Chem. 2014; (25): 918-927.
9
10. McNelles S A, Knight S D, Janzen N, Valliant J F , Adronov A. Synthesis, radiolabeling, and in vivo imaging of PEGylated high-generation polyester dendrimers. Biomacromolecules. 2015; (16): 3033-3041.
10
11. Luong D. PEGylated PAMAM dendrimers: Enhancing efficacy , mitigating toxicity for effective anticancer drug and gene delivery. Acta Biomater. 2016; (43): 14-29.
11
12. Bosman A, Janssen H , Meijer E. About dendrimers: structure, physical properties, and applications. Chem Rev. 1999; (99): 1665-1688.
12
13. Lee C C, MacKay J A, Fréchet J M , Szoka, F C. Designing dendrimers for biological applications. Nat Biotechnol. 2005; (23): 1517-1526.
13
14. Ardestani M S. Nanosilver based anionic linear globular dendrimer with a special significant antiretroviral activity. J Mater Sci Mater Med. 2015; (26): 179.
14
15. Mohammadzadeh P, Cohan R A, Ghoreishi S M, Bitarafan-Rajabi A , Ardestani M S. AS1411 Aptamer-Anionic Linear Globular Dendrimer G2-Iohexol Selective Nano-Theranostics. Sci Rep. 2017; (7).
15
16. Ghoreishi S M, Bitarafan-Rajabi A, Azar A D, Ardestani M S , Assadi. A Novel 99mTc-Radiolabeled Anionic Linear Globular PEG-Based Dendrimer-Chlorambucil: Non-Invasive Method for In-Vivo Biodistribution. Drug Res. 2017; (67): 149-155.
16
17. Abdoli A. Conjugated anionic PEG-citrate G2 dendrimer with multi-epitopic HIV-1 vaccine candidate enhance the cellular immune responses in mice. Artif Cells Nanomed Biotechnol. 2017; 1-7.
17
18. Chalmers N , Jackson R. Comparison of iodixanol and iohexol in renal impairment. Br J Radiol. 1999; (72): 701-703.
18
19. Heinrich M C, Häberle L, Müller V, Bautz W , Uder M. Nephrotoxicity of iso-osmolar iodixanol compared with nonionic low-osmolar contrast media: meta-analysis of randomized controlled trials. Radiol. 2009; (250): 68-86.
19
20. Stacul F. Contrast induced nephropathy: updated ESUR contrast media safety committee guidelines. Eur Radiol. 2011; (21): 2527-2541.
20
21. Berg K. J. Nephrotoxicity related to contrast media. Scan J Urol Nephrol. 2000; (34), 317-322.
21
22. Dillman J R, Strouse P J, Ellis J H, Cohan R H , Jan S C. Incidence and severity of acute allergic-like reactions to iv nonionic iodinated contrast material in children. American journal of roentgenology. 2007;(188): 1643-1647.
22
23. Haririan I. Anionic linear-globular dendrimer-cis-platinum (II) conjugates promote cytotoxicity in vitro against different cancer cell lines. Int J Nanomedicine. 20105; (63).
23
24. Namazi H, Adeli M. Dendrimers of citric acid and poly (ethylene glycol) as the new drug-delivery agents. Biomaterials. 2005; (26): 1175-1183.
24
25. Alavidjeh, M S. Anionic linear-globular dendrimers: biocompatible hybrid materials with potential uses in nanomedicine. J Mater Sci Mater Med. 2010; (21): 1121-1133.
25
26. Barzegar Behrooz A. Smart bomb AS1411 aptamer‐functionalized/PAMAM dendrimer nanocarriers for targeted drug delivery in the treatment of gastric cancer. Clin Exp Pharmacol Physiol. 2017; (44): 41-51.
26
27. Arokiaraj M C, Am Heart J. 2016.
27
28. Hainfeld J, Slatkin D, Focella T , Smilowitz H. Gold nanoparticles: a new X-ray contrast agent. Br J Radiol. 2006; (79): 248-253.
28
29. Kim J, Chhour P , Hsu J , Litt, H I , Ferrari V A , Popovtzer, R Cormode D P. Use of Nanoparticle Contrast Agents for Cell Tracking with Computed Tomography. Bioconjug Chem. 2017; (21): 1581–1597.
29
ORIGINAL_ARTICLE
Effect of the nanoliposomal formulations of rifampin and N-acetyl cysteine on staphylococcus epidermidis biofilm
Objective(s): Staphylococcus epidermidis is a common cause of medical device-associated infections due to biofilm formation, and its elimination is extremely challenging. Although rifampin efficacy against S. epidermidis biofilms has been confirmed, its use as a single agent may lead to resistance. As such, it is assumed that the combination of rifampin and N-acetylcysteine (NAC) could exert additive effects as a mucolytic agent. The present study aimed to use a liposomal system for the delivery of these compounds to bacterial biofilm.Materials and Methods: Liposomal formulations were prepared using the dehydration-rehydration method and characterized in terms of the size, zeta potential, and encapsulation efficacy. In addition, the ability of various formulations in the eradication of bacterial biofilm and inhibition of biofilm formation was assessed based on the optical density ratio. Results: The zeta potential of the liposomes was positive, and the mean size of these liposomal formulations was less than 200 nanometers. Liposomal rifampin was the most effective formulation against S. epidermidis, and the anti-biofilm activity of most of the formulations was concentration-dependent and time-dependent.Conclusion: According to the results, the rifampin-loaded liposomes were effective against S. epidermidis biofilm formation.
https://nmj.mums.ac.ir/article_14574_e572ab9f30c5001ff9612c72c6252f44.pdf
2020-04-01
131
137
10.22038/nmj.2020.07.006
Biofilm
Nanoliposomes
N-acetyl cysteine
Rifampin
Farzaneh
Bazrgari
bazrgarif911@mums.ac.ir
1
School of Pharmacy, Mashhad University of Medical Sciences, Mashhad, Iran
AUTHOR
Bahman
Khameneh
khamenehbagherib@mums.ac.ir
2
School of Pharmacy, Mashhad University of Medical Sciences, Mashhad, Iran
AUTHOR
Bibi Sedigheh
Fazly Bazzaz
3
Biotechnology Research Center, Pharmaceutical Technology Institute, Mashhad University of Medical Sciences, Mashhad, Iran
AUTHOR
Asma
Mahmoudi
mahmoudia912@mums.ac.ir
4
School of Pharmacy, Mashhad University of Medical Sciences, Mashhad, Iran
AUTHOR
Bizhan
Malaekeh-Nikouei
malaekehb@mums.ac.ir
5
Nanotechnology Research Center, Pharmaceutical Technology Institute, Mashhad University of Medical Sciences, Mashhad, Iran
LEAD_AUTHOR
1.Kloos WE, Bannerman TL. Update on clinical significance of coagulase-negative staphylococci. Clin Microbiol Rev. 1994; 7(1): 117-140.
1
2.Khameneh B, Diab R, Ghazvini K, Fazly Bazzaz BS. Breakthroughs in bacterial resistance mechanisms and the potential ways to combat them. Microb Pathog. 2016; 95 :32-42.
2
3.McCann MT, Gilmore BF, Gorman SP. Staphylococcus epidermidis device‐related infections: pathogenesis and clinical management. J Pharm Pharmacol. 2008; 60(12): 1551-1571.
3
4.Costerton WJ, Montanaro L, Balaban N, Arciola CR. Prospecting gene therapy of implant infections. Int J Artif Organs. 2009; 32(9): 689-695.
4
5.Perez-Giraldo C, Rodriguez-Benito A, Moran F, Hurtado C, Blanco M, Gomez-Garcia A. Influence of N-acetylcysteine on the formation of biofilm by Staphylococcus epidermidis. J Antimicrob Chemother. 1997; 39(5): 643-646.
5
6.Stey C, Steurer J, Bachmann S, Medici T, Tramer M. The effect of oral N-acetylcysteine in chronic bronchitis: a quantitative systematic review. Eur Respir J. 2000; 16(2): 253-262.
6
7.Olofsson A-C, Hermansson M, Elwing H. N-acetyl-L-cysteine affects growth, extracellular polysaccharide production, and bacterial biofilm formation on solid surfaces. Appl Environ Microbiol. 2003; 69(8): 4814-4822.
7
8.Moghadas-Sharif N, Fazly Bazzaz BS, Khameneh B, Malaekeh-Nikouei B. The effect of nanoliposomal formulations on Staphylococcus epidermidis biofilm. Drug Dev Ind Pharm. 2015; 41(3): 445-450.
8
9.Monzón M, Oteiza C, Leiva J, Amorena B. Synergy of different antibiotic combinations in biofilms of Staphylococcus epidermidis. Journal of Antimicrobial Chemotherapy. 2001; 48(6): 793-801.
9
10.Fazly Bazzaz BS, Khameneh B, Zarei H, Golmohammadzadeh S. Antibacterial efficacy of rifampin loaded solid lipid nanoparticles against Staphylococcus epidermidis biofilm. Microb Pathog. 2016; 93: 137-144.
10
11.Cheow WS, Hadinoto K. Lipid-polymer hybrid nanoparticles with rhamnolipid-triggered release capabilities as anti-biofilm drug delivery vehicles. Particuology. 2012; 10(3): 327-333.
11
12.Diab R, Khameneh B, Joubert O, Duval R. Insights in Nanoparticle-Bacterium Interactions: New Frontiers to Bypass Bacterial Resistance to Antibiotics. Curr Pharm Des. 2015; 21(28): 4095-4105.
12
13.Sharma A, Sharma US. Liposomes in drug delivery: progress and limitations. Int J Pharm. 1997; 154(2): 123-140.
13
14.Kim H-J, Gias ELM, Jones MN. The adsorption of cationic liposomes to Staphylococcus aureus biofilms. Colloids Surf A Physicochem Eng Asp. 1999; 149(1-3): 561-570.
14
15.Khameneh B, Iranshahy M, Ghandadi M, Ghoochi Atashbeyk D, Fazly Bazzaz BS, Iranshahi M. Investigation of the antibacterial activity and efflux pump inhibitory effect of co-loaded piperine and gentamicin nanoliposomes in methicillin-resistant Staphylococcus aureus. Drug Dev Ind Pharm. 2015; 41(6): 989-994.
15
16.Atashbeyk DG, Khameneh B, Tafaghodi M, Fazly Bazzaz BS. Eradication of methicillin-resistant Staphylococcus aureus infection by nanoliposomes loaded with gentamicin and oleic acid. Pharm Biol. 2014; 52(11): 1423-1428.
16
17.Forier K, Messiaen AS, Raemdonck K, Nelis H, De Smedt S, Demeester J, Coenye T, Braeckmans K. Probing the size limit for nanomedicine penetration into Burkholderia multivorans and Pseudomonas aeruginosa biofilms. J Control Release. 2014; 195: 21-28.
17
18.Sugano M, Morisaki H, Negishi Y, Endo-Takahashi Y, Kuwata H, Miyazaki T, Yamamoto M. Potential effect of cationic liposomes on interactions with oral bacterial cells and biofilms. J Liposome Res. 2016; 26(2): 156-162.
18
19.Nogueira E, Gomes AC, Preto A, Cavaco-Paulo A. Design of liposomal formulations for cell targeting. Colloids Surf B Biointerfaces. 2015; 136: 514-526.
19
20.Chiesa E, Monti L, Paganini C, Dorati R, Conti B, Modena T, Rossi A, Genta I. Polyethylene Glycol-Poly-Lactide-co-Glycolide Block Copolymer-Based Nanoparticles as a Potential Tool for Off-Label Use of N-Acetylcysteine in the Treatment of Diastrophic Dysplasia. J Pharm Sci. 2017; 106(12): 3631-3641.
20
21.Waitz JA. Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically: National Committee for Clinical Laboratory Standards; 1990.
21
22.Pitts B, Hamilton MA, Zelver N, Stewart PS. A microtiter-plate screening method for biofilm disinfection and removal. J Microbiol Methods. 2003; 54(2): 269-276.
22
23.Gomez-Junyent J, Benavent E, Sierra Y, El Haj C, Soldevila L, Torrejon B, Rigo-Bonnin R, Tubau F, Ariza J, Murillo O. Efficacy of ceftolozane/tazobactam, alone and in combination with colistin, against multidrug-resistant Pseudomonas aeruginosa in an in vitro biofilm pharmacodynamic model. Int J Antimicrob Agents. 2019; 53(5): 612-619.
23
24.Liu L, Li JH, Zi SF, Liu FR, Deng C, Ao X, Zhang P. AgNP combined with quorum sensing inhibitor increased the antibiofilm effect on Pseudomonas aeruginosa. Appl Microbiol Biotechnol. 2019; 103(15): 6195-6204.
24
25.Zheng Z, Stewart PS. Penetration of rifampin through Staphylococcus epidermidis biofilms. Antimicrob Agents Chemother. 2002; 46(3): 900-903.
25
26.Cerca N, Martins S, Cerca F, Jefferson KK, Pier GB, Oliveira R, Azeredo J. Comparative assessment of antibiotic susceptibility of coagulase-negative staphylococci in biofilm versus planktonic culture as assessed by bacterial enumeration or rapid XTT colorimetry. Journal of Antimicrobial Chemotherapy. 2005; 56(2): 331-336.
26
27.Monzón M, Oteiza C, Leiva J, Lamata M, Amorena B. Biofilm testing of Staphylococcus epidermidis clinical isolates: low performance of vancomycin in relation to other antibiotics. Diagn Microbiol Infect Dis. 2002; 44(4): 319-324.
27
28.Monzón M, Oteiza C, Leiva J, Amorena B. Synergy of different antibiotic combinations in biofilms of Staphylococcus epidermidis. J Antimicrob Chemother. 2001; 48(6): 793-801.
28
29.Leite B, Gomes F, Teixeira P, Souza C, Pizzolitto E, Oliveira R. Staphylococcus epidermidis biofilms control by N-acetylcysteine and rifampicin. Am J Ther. 2013; 20(4): 322-328.
29
30.Aslam S, Trautner BW, Ramanathan V, Darouiche RO. Combination of tigecycline and N-acetylcysteine reduces biofilm-embedded bacteria on vascular catheters. Antimicrob Agents Chemother. 2007; 51(4): 1556-1558.
30
31.Ahmed K, Muiruri PW, Jones GH, Scott MJ, Jones MN. The effect of grafted poly (ethylene glycol) on the electrophoretic properties of phospholipid liposomes and their adsorption to bacterial biofilms. Colloids Surf A Physicochem Eng Asp. 2001; 194(1-3): 287-296.
31
ORIGINAL_ARTICLE
A novel three-dimensional printing of electroconductive scaffolds for bone cancer therapy application
Objective(s): Tissue engineering aims to achieve a tissue, which has highly interconnected porous microstructure concurrent with appropriate mechanical and biological properties. Materials and Methods: Therefore, the microstructure scaffolds are of great importance in this field. In the present study, an electroconductive poly-lactic acid (EC-PLA) filament used to fabricate a porous bone scaffold. For scaffolds model designed, solid-work software was used. Then, the designed modeled was transferred to simplify 3D to laminated with its G-Code file for fused deposition modeling (FDM) printer to create a scaffold with porosity around 65-75%. Two different shapes were designed and fabricated (cylindrical and cubic shape). The samples were coated with hydroxyapatite (HA) nanoparticle to enhance its chemical stability. In this study, the X-ray diffraction (XRD) confirmed that the EC-PLA is non-crystalized and scanning electron microscopy (SEM) used to present the apatite formation on the surface of porous scaffolds. The compression test, fracture toughness, and hardness were measured. The biological response in the physiological saline was performed to determine the rate of degradation of EC-PLA in phosphate buffer saline (PBS) and the apatite formation in the simulated body fluid (SBF) after 14 days. Results: Finally, the biocompatibility of the porous architecture was monitored using human gum (HuGu) cells. The ABAQUS modeling simulation was used to compare the experimental and analytical results. The obtained results showed that by applying force to both cylindrical and cubic scaffold, the Von Mises Stress (VMS) could withstand the scaffold mentioned above at 9.7-11 MPa. Conclusion: Therefore, it can be concluded that prepared porous scaffolds have a high potential in bone tissue engineering and probably the treatment of tumor-related bone defects as photothermal therapy. The porous EC-PLA scaffold was successfully fabricated and showed appropriate compressive strength (39.14 MPa), with controllable porosity of 60-70 %, which is a suitable candidate for replacing in bone tissues.
https://nmj.mums.ac.ir/article_15125_633cde7eb3bb66c1230af043119c534a.pdf
2020-04-01
138
148
10.22038/nmj.2020.07.007
Cell culture
Electroconductive Poly lacticacid
Scaffold
Tissue engineering
Marjan
Monshi
marjan.monshi2@iaun.ac.ir
1
Advanced Materials Research Centre, Department of Materials Science and Engineering, Najafabad Branch, Islamic Azad University, Najafabad, Iran
AUTHOR
Saeid
Esmaeili
2
Mechanical Engineering Department, Khomeinishahr Branch, Islamic Azad University, Khomeinishahr, Iran
AUTHOR
Amin
Kolooshani
amin_koloshani2@yahoo.com
3
Mechanical Engineering Department, Khomeinishahr Branch, Islamic Azad University, Khomeinishahr, Iran
AUTHOR
Bahareh Kamyab
Moghadas
4
Department of Chemical Engineering, Shiraz Branch, Islamic Azad University, Shiraz, Iran
LEAD_AUTHOR
Saeed
Saber-Samandari
5
New Technologies Research Center, Amirkabir University of Technology, Tehran, 15875-4413, Iran
AUTHOR
Amirsalar
Khandan
amirsalar.khandan@cc.emu.edu.tr
6
New Technologies Research Center, Amirkabir University of Technology, Tehran, 15875-4413, Iran
LEAD_AUTHOR
1. Saber-Samandari S, & Gross K A. Micromechanical properties of single crystal hydroxyapatite by nanoindentation. Acta Biomater. 2009; 5(6), 2206-2212.
1
2.Heydary H A, Karamian E, Poorazizi E, Heydaripour J, Khandan A. Electrospun of polymer/bioceramic nanocomposite as a new soft tissue for biomedical applications. . Asian Ceram. Soc. 2015; 3(4), 417-425.
2
3.Moghadas B K. Akbarzadeh A, Azadi M, Aghili A, Rad A S, Hallajian S. The morphological properties and biocompatibility studies of synthesized nanocomposite foam from modified polyethersulfone/graphene oxide using supercritical CO2. J Macromol Sci A. 2020; 1-10.
3
4.Kamyab Moghadas B, Azadi M. Fabrication of Nanocomposite Foam by Supercritical CO2 Technique for Application in Tissue Engineering. J Tiss Mater. 2019; 2(1), 23-32.
4
5. Aghdam H A, Sanatizadeh E, Motififard M, Aghadavoudi F, Saber-Samandari S, Esmaeili S, Khandan A. Effect of calcium silicate nanoparticle on the surface feature of calcium phosphates hybrid bio-nanocomposite using for bone substitute application. Powder Technol. 2020; 361, 917-929.
5
6.Costantini M, Colosi C, Mozetic P, Jaroszewicz J, Tosato A, Rainer A, Barbetta A. Correlation between porous texture and cell seeding efficiency of gas foaming and microfluidic foaming scaffolds. Mat Sci Eng C-Mater. 2016; 62, 668-677.
6
7. Farazin A, Aghdam H A, Motififard M, Aghadavoudi F, Kordjamshidi A, Saber-Samandari S, Khandan A. A polycaprolactone bio-nanocomposite bone substitute fabricated for femoral fracture approaches: Molecular dynamic and micro-mechanical Investigation. J Nanoanaly. 2019.
7
8. Tahririan M A, Motififard M, Omidian A, Aghdam H A, Esmaeali A. Relationship between bone mineral density and serum vitamin D with low energy hip and distal radius fractures: A case-control study. Arch Bone Joint Surg. 2017; 5(1), 22.
8
9. Kordjamshidi A, Saber-Samandari S, Nejad M G, Khandan A. Preparation of novel porous calcium silicate scaffold loaded by celecoxib drug-using freeze-drying technique: Fabrication, characterization and simulation. Ceram Int. 2019; 45(11), 14126-14135.
9
10. Datta S, Das A, Sasmal P, Bhutoria S, Roy Chowdhury A, Datta P. Alginate-poly (amino acid) extrusion printed scaffolds for tissue engineering applications. Int J Polym Mater Po. 2020; 69(2), 65-72.
10
11.Esmaeili S, Shahali M, Kordjamshidi A, Torkpoor Z, Namdari F, Samandari S S, Khandan A.An artificial blood vessel fabricated by 3D printing for pharmaceutical applications. Nanomed J. 2019; 6(3), 183-194.
11
12. Esmaeili S, Aghdam H A, Motififard M, Saber-Samandari S, Montazeran A H, Bigonah M, Khandan A. A porous polymeric–hydroxyapatite scaffold used for femur fractures treatment: fabrication, analysis, and simulation. Eur J Orthop Surg Traumatol. 2020; 30(1), 123-131.
12
13. Esmaeili S, Khandan A, Saber-Samandari S. Mechanical performance of three-dimensional bio-nano composite scaffolds designed with digital light processing for biomedical applications. Iran J Med Phys. 2018; 15, 328-328.
13
14. Khandan, A., & Ozada, N. Bredigite-Magnetite (Ca7MgSi4O16-Fe3O4) nanoparticles: A study on their magnetic properties. J Alloy Compd. 2017; 726, 729-736.
14
15.Khandan A, Ozada N, Saber-Samandari S, Nejad M G. On the mechanical and biological properties of bredigite-magnetite (Ca7MgSi4O16-Fe3O4) nanocomposite scaffolds. Ceram Int. 2018; 44(3), 3141-3148.
15
16.Serra T, Planell J A, Navarro M. High-resolution PLA-based composite scaffolds via 3-D printing technology. Acta biomater. 2013; 9(3), 5521-5530.
16
17. Stoppato M, Carletti E, Sidarovich V, Quattrone A, Unger R E, Kirkpatrick C J, Motta A. Influence of scaffold pore size on collagen I development: a new in vitro evaluation perspective. J Bioact Compat Pol. 2013; 28(1), 16-32.
17
18.Giordano R A, Wu B M, Borland S W, Cima L G, Sachs E M, Cima M J. Mechanical properties of dense polylactic acid structures fabricated by three-dimensional printing. J Biomat Sci, Polymer Edition. 1997; 8(1), 63-75.
18
19.Velioglu Z B, Pulat D, Demirbakan B, Ozcan B, Bayrak E, Erisken C. 3D-printed poly (lactic acid) scaffolds for trabecular bone repair and regeneration: scaffold and native bone characterization. Connect Tissue Res. 2019; 60(3), 274-282.
19
20.Fafenrot S, Grimmelsmann N, Wortmann M, Ehrmann A.Three-dimensional (3D) printing of polymer-metal hybrid materials by fused deposition modeling. Mater. 2017; 10(10), 1199.
20
21. Sahmani S, Saber-Samandari S, Shahali M, Yekta H J, Aghadavoudi F, Montazeran A H, Khandan A. Mechanical and biological performance of axially loaded novel bio-nano composite sandwich plate-type implant coated by biological polymer thin film. J Mech Behav Biomed. 2018; 88, 238-250.
21
22. Kenry L W, Loh K P, Lim C T. When stem cells meet graphene: opportunities and challenges in regenerative medicine. Biomaterials. 2018; 155, 236-250.
22
23.Bohner M, Lemaitre J.Can bioactivity be tested in vitro with the SBF solution?. Biomaterials, 2009; 30(12), 2175-2179.
23
24.Monfared R M, Ayatollahi M R, Isfahani R B. Synergistic effects of hybrid MWCNT/nano-silica on the tensile and tribological properties of woven carbon fabric epoxy composites. Theor Appl Fract Mec. 2018; 96, 272-284.
24
25. Moradi-Dastjerdi R, Behdinan K.Stability analysis of multifunctional smart sandwich plates with graphene nanocomposite and porous layers. Int J Mech Sci. 2020; 167, 105283.
25
26. Khandan A, Jazayeri H, Fahmy M D,Razavi M. Hydrogels: Types, structure, properties, and applications. Biomat Tiss Eng. 2017; 4(27), 143-69.
26
27.Ayatollahi M R, Moghimi Monfared R, Barbaz Isfahani R. Experimental investigation on tribological properties of carbon fabric composites: effects of carbon nanotubes and nano-silica. P I Mech Eng L-J Mat. 2019; 233(5), 874-884.
27
28. Montazeran A H, Saber Samandari S, Khandan A. Artificial intelligence investigation of three silicates bioceramics-magnetite bio-nano composite: Hyperthermia and biomedical applications. Nanomed J. 2018; 5(3), 163-171.
28
29. Joneidi Yekta H, Shahali M, Khorshidi S, Rezaei S, Montazeran AH, Samandari SS, Khandan A. Mathematically and experimentally defined porous bone scaffold produced for bone substitute application. Nanomed J. 2018; 5(4), 227-234.
29
30. Barbaz-I R. Experimental determining of the elastic modulus and strength of composites reinforced with two nanoparticles (Doctoral dissertation, MSc Thesis, School of Mechanical Engineering Iran University of Science and Technology, Tehran, Iran); 2014.
30
31. Karamian E, Nasehi A, Saber-Samandari S, Khandan A. Fabrication of hydroxyapatite-baghdadite nanocomposite scaffolds coated by PCL/Bioglass with polyurethane polymeric sponge technique. Nanomed J. 2017; 4(3), 177-183.
31
32. Khandan A, Karamian E, Bonakdarchian M. Mechanochemical synthesis evaluation of nanocrystalline bone-derived bioceramic powder using for bone tissue engineering. Dent Hypoth. 2014; 5(4), 155.
32
33.Salami MA, Kaveian F, Rafienia M, Saber-Samandari S, Khandan A,Naeimi M. Electrospun polycaprolactone/lignin-based nanocomposite as a novel tissue scaffold for biomedical applications. J. Medical Signals Sens. 2017; 7(4), 228.
33
34. Khandan A, Karamian E, Mehdikhani-Nahrkhalaji M, Mirmohammadi H, Farzadi A, Ozada N, Zamani K. Influence of spark plasma sintering and baghdadite powder on mechanical properties of hydroxyapatite. Proce Mat Sci. 2015; 11, 183-189.
34
35. Ghayour H, Abdellahi M, Nejad M G, Khandan A,Saber-Samandari S. Study of the effect of the Zn 2+ content on the anisotropy and specific absorption rate of the cobalt ferrite: the application of Co 1− x Zn x Fe 2 O 4 ferrite for magnetic hyperthermia. J Aust Ceram Soc. 2018; 54(2), 223-230.
35
36. Sahmani S, Shahali M, Nejad M G, Khandan A, Aghdam MM, Saber-Samandari S. Effect of copper oxide nanoparticles on electrical conductivity and cell viability of calcium phosphate scaffolds with improved mechanical strength for bone tissue engineering. Eur Phys J Plus. 2019; 134(1), 7.
36
37. Sahmani S, Khandan A, Esmaeili S, Saber-Samandari S, Nejad M G, Aghdam MM.Calcium phosphate-PLA scaffolds fabricated by fused deposition modeling technique for bone tissue applications: Fabrication, characterization, and simulation. Ceram Int. 2020; 46(2), 2447-2456.
37
38. Wibowo A, Vyas C, Cooper G, Qulub F, Suratman R, Mahyuddin A I, Bartolo P. 3D Printing of Polycaprolactone–Polyaniline Electroactive Scaffolds for Bone Tissue Engineering. Materials, 2020; 13(3), 512.
38
39. Potnuru A,Tadesse Y. Investigation of polylactide and carbon nanocomposite filament for 3D printing. Prog Add Manu. 2019; 4(1), 23-41.
39
40. Amanjani A R, Zandi R, Samandari S S. Determination of anterior femoral bowing to length ratio in Iranian population. Pajoohandeh J. 2020; 24(1), 0-0.
40
41.Saber-Samandari S, Mohammadi-Aghdam M, Saber-Samandari S. A novel magnetic bifunctional nanocomposite scaffold for photothermal therapy and tissue engineering. Int J Biol Macromol. 2019; 138, 810-818.
41
42. Bidgoli M R, Alemzadeh I, Tamjid E, Khafaji M,Vossoughi M. Fabrication of hierarchically porous silk fibroin-bioactive glass composite scaffold via indirect 3D printing: Effect of particle size on physico-mechanical properties and in vitro cellular behavior. Mat Sci Eng C-Mater. 2019; 103, 109688.
42
43. Maghsoudlou M A, Nassireslami E, Saber-Samandar S, Khandan A. Bone regeneration using bio-nanocomposite tissue reinforced with bioactive nanoparticles for femoral defect applications in medicine. Avicenna J. Med. Biotechno. 2020; (2).
43
44.Maghsoudlou M A, Isfahani R B, Saber-Samandari S, Sadighi M. Effect of interphase, curvature, and agglomeration of SWCNTs on mechanical properties of polymer-based nanocomposites: Experimental and numerical investigations. Compos Part B-Eng. 2019; 175, 107119.
44
45.Tamjidi S, Esmaeili H, Moghadas B K. Application of magnetic adsorbents for the removal of heavy metals from wastewater: a review study. Materials Research Express. 2019; 6(10), 102004.
45
46.Rad A S, Samipour V, Movaghgharnezhad S, Mirabi A, Shahavi M H, Moghadas B K. X12N12 (X= Al, B) clusters for protection of vitamin C; molecular modeling investigation. Surf Interf, 2019; 15, 30-37.
46
47. Shokri‐Oojghaz R, Moradi‐Dastjerdi R, Mohammadi H, Behdinan K. Stress distributions in nanocomposite sandwich cylinders reinforced by aggregated carbon nanotube. Polym Composite. 2019; 40(S2), E1918-E1927.
47
48. Pourasghar A, Moradi‐Dastjerdi R, Yas M H, Ghorbanpour Arani A, Kamarian S. Three‐dimensional analysis of carbon nanotube‐reinforced cylindrical shells with temperature‐dependent properties under thermal environment. Polym Composite. 2018; 39(4), 1161-1171.
48
ORIGINAL_ARTICLE
Evaluation of protein corona formation and anticancer efficiency of curcumin-loaded zwitterionic silica nanoparticles
Objective(s): Study and development of antifouling nanosystem for conjugation of drugs were attracting great attention in recent years. The present study aimed to develop novel curcumin-loaded silica nanoparticles containing zwitterionic coating as an antifouling system to provide protein corona free nanoformulations for curcumin. Materials and Methods: Silica nanoparticles were prepared using the Stöber method, and mono- and bi-functionalized nanoparticles were obtained by modifying the surface of the bare silica nanoparticles with (3-aminopropyl)triethoxysilane (APTES), polyethylene glycol amine, APTES with sulfobetaine, and polyethylene glycol amine with sulfobetaine. Nanoparticle characterization, curcumin release, and measurement of protein corona inhibition were performed after incubation in the human plasma and MTT assay to confirm the stability and efficiency of the nanoparticles. Results: The presence of the sulfobetaine group could influence the curcumin loading capacity of the silica nanoparticles. The results of sodium dodecyl sulfate-polyacrylamide gel electrophoresis indicated no significant protein adsorption on the curcumin-loaded, zwitterionic-coated nanoparticles compared to the other nanoparticles. In addition, the MTT assay confirmed the cytotoxicity of the curcumin-loaded sulfobetaine-APTES-silica nanoparticles on MCF-7 cancer cells.Conclusion: Our findings confirmed the effects of the zwitterionic coating on the physicochemical properties of the nanoparticles. These findings play a key role in the development of novel nanoparticles for drug delivery applications.
https://nmj.mums.ac.ir/article_15123_eab66abd85cc243358df7cfcde03057e.pdf
2020-04-01
149
157
10.22038/nmj.2020.07.008
Curcumin
Functionalized Nanoparticles
Protein Corona
Silica Nanoparticles
Zwitterionic Coating
Shokoofeh
Maghari
sh.maghari@gmail.com
1
Department of Phytochemistry, Medicinal Plants and Drugs Research Institute, Shahid Beheshti University, Tehran, Iran
AUTHOR
Alireza
Ghassempour
a-ghassempour@sbu.ac.ir
2
Department of Phytochemistry, Medicinal Plants and Drugs Research Institute, Shahid Beheshti University, Tehran, Iran
LEAD_AUTHOR
1.Falconieri M, Adamo M, Monasterolo C, Bergonzi M, Coronnello M, Bilia A. New Dendrimer-Based Nanoparticles Enhance Curcumin Solubility. Planta Med. 2016; 22; 83(05): 420–425.
1
2.Gomes CA, Girão da Cruz T, Andrade JL, Milhazes N, Borges F, Marques MPM. Anticancer Activity of Phenolic Acids of Natural or Synthetic Origin: A Structure−Activity Study. J Med Chem. 2003; 46(25): 5395–5401.
2
3.Chakraborti S, Dhar G, Dwivedi V, Das A, Poddar A, Chakraborti G, Basu G, Chakrabarti P, Surolia A, Bhattacharyya B. Stable and Potent Analogues Derived from the Modification of the Dicarbonyl Moiety of Curcumin. Biochemistry. 2013; 52(42): 7449–7460.
3
4.Yang X, Li Z, Wang N, Li L, Song L, He T, Sun L, Wang Z, Wu Q, Luo N, Yi C. Curcumin-Encapsulated Polymeric Micelles Suppress the Development of Colon Cancer In Vitro and In Vivo. Sci Rep. 2015; 5(1): 10322.
4
5.Siviero A, Gallo E, Maggini V, Gori L, Mugelli A, Firenzuoli F, Vannacci A. Curcumin, a golden spice with a low bioavailability. Journal of Herbal Medicine. 2015; 5(2): 57–70.
5
6.Hsu C-H, Cheng A-L. CLINICAL STUDIES WITH CURCUMIN. In: Aggarwal BB, Surh Y-J, Shishodia S, editors. The Molecular Targets and Therapeutic Uses of Curcumin in Health and Disease Boston, MA: Springer US; 2007, p. 471–480. Available from: http://link.springer.com/10.1007/978-0-387-46401-5_21
6
7.Anand P, Kunnumakkara AB, Newman RA, Aggarwal BB. Bioavailability of Curcumin: Problems and Promises. Mol Pharmaceutics. 2007; 4(6): 807–818.
7
8.Thu Huong LT, Nam NH, Doan DH, My Nhung HT, Quang BT, Nam PH, Thong P.Q, Phuc N.X, Thu H.P. Folate attached, curcumin loaded Fe3O4 nanoparticles: A novel multifunctional drug delivery system for cancer treatment. Materials Chemistry and Physics. 2016; 172: 98–104.
8
9.Magro M, Campos R, Baratella D, Lima G, Holà K, Divoky C, Stollberger R, Malina O, Aparicio C, Zoppellaro G, Zbořil R. A Magnetically Drivable Nanovehicle for Curcumin with Antioxidant Capacity and MRI Relaxation Properties. Chem Eur J. 2014; 20(37): 11913–11920.
9
10.Manju S, Sharma CP, Sreenivasan K. Targeted coadministration of sparingly soluble paclitaxel and curcumin into cancer cells by surface engineered magnetic nanoparticles. J Mater Chem. 2011; 21(39): 15708.
10
11.Yallapu MM, Ebeling MC, Khan S, Sundram V, Chauhan N, Gupta BK, Puumala SE, Jaggi M, Chauhan SC. Novel Curcumin-Loaded Magnetic Nanoparticles for Pancreatic Cancer Treatment. Molecular Cancer Therapeutics. 2013; 12(8): 1471–1480.
11
12.Nh G, Li J. Targeted Theranostic Approach for Glioma Using Dendrimer-Based Curcumin Nanoparticle. J Nanomed Nanotechnol. 2016; 7(4). https://www.omicsonline.org/open-access/targeted-theranostic-approach-for-glioma-using-dendrimerbasedcurcumin-nanoparticle-2157-7439-1000393.php?aid=77685
12
13.Pillai JJ, Thulasidasan AKT, Anto RJ, Devika NC, Ashwanikumar N, Kumar GSV. Curcumin entrapped folic acid conjugated PLGA–PEG nanoparticles exhibit enhanced anticancer activity by site specific delivery. RSC Adv. 2015; 5(32): 25518–25524.
13
14.Salem M, Xia Y, Allan A, Rohani S, Gillies ER. Curcumin-loaded, folic acid-functionalized magnetite particles for targeted drug delivery. RSC Adv. 2015; 5(47): 37521–37532.
14
15.Lynch I, Dawson KA. Protein-nanoparticle interactions. Nano Today. 2008; 3(1–2): 40–47.
15
16.Salvati A, Pitek AS, Monopoli MP, Prapainop K, Bombelli FB, Hristov DR, Kelly PM, Åberg C, Mahon E, Dawson KA. Transferrin-functionalized nanoparticles lose their targeting capabilities when a biomolecule corona adsorbs on the surface. Nature Nanotech. 2013; 8(2): 137–143.
16
17.Efremova NV, Sheth SR, Leckband DE. Protein-Induced Changes in Poly(ethylene glycol) Brushes: Molecular Weight and Temperature Dependence. Langmuir. 2001 ; 17(24): 7628–7636.
17
18.Kim HR, Andrieux K, Delomenie C, Chacun H, Appel M, Desmaële D, Taran F, Georgin D, Couvreur P, Taverna M. Analysis of plasma protein adsorption onto PEGylated nanoparticles by complementary methods: 2-DE, CE and Protein Lab-on-chip® system. Electrophoresis. 2007; 28(13): 2252–2261.
18
19.Pozzi D, Colapicchioni V, Caracciolo G, Piovesana S, Capriotti AL, Palchetti S, De Grossi S, Riccioli A, Amenitsch H, Laganà A. Effect of polyethyleneglycol (PEG) chain length on the bio–nano-interactions between PEGylated lipid nanoparticles and biological fluids: from nanostructure to uptake in cancer cells. Nanoscale. 2014; 6(5): 2782.
19
20.Estephan ZG, Schlenoff PS, Schlenoff JB. Zwitteration As an Alternative to PEGylation. Langmuir. 2011; 27(11): 6794–6800.
20
21.Estephan ZG, Jaber JA, Schlenoff JB. Zwitterion-Stabilized Silica Nanoparticles: Toward Nonstick Nano. Langmuir. 2010; 26(22): 16884–16889.
21
22.Safavi-Sohi R, Maghari S, Raoufi M, Jalali SA, Hajipour MJ, Ghassempour A, Mahmoudi M. Bypassing Protein Corona Issue on Active Targeting: Zwitterionic Coatings Dictate Specific Interactions of Targeting Moieties and Cell Receptors. ACS Appl Mater Interfaces. 2016; 8(35): 22808–22818.
22
23.Huang J, Xu W. Zwitterionic monomer graft copolymerization onto polyurethane surface through a PEG spacer. Applied Surface Science. 2010; 256(12): 3921–3927.
23
24.Liu J, Xu T, Gong M, Yu F, Fu Y. Fundamental studies of novel inorganic–organic charged zwitterionic hybrids. Journal of Membrane Science. 2006; 283(1–2): 190–200.
24
25.Xie M, Shi H, Ma K, Shen H, Li B, Shen S, Wang X, Jin Y. Hybrid nanoparticles for drug delivery and bioimaging: Mesoporous silica nanoparticles functionalized with carboxyl groups and a near-infrared fluorescent dye. Journal of Colloid and Interface Science. 2013; 395: 306–314.
25
26.Wu X, Wu M, Zhao JX. Recent development of silica nanoparticles as delivery vectors for cancer imaging and therapy. Nanomedicine: Nanotechnology, Biology and Medicine. 2014; 10(2): 297–312.
26
27.He Q, Shi J. Mesoporous silica nanoparticle based nano drug delivery systems: synthesis, controlled drug release and delivery, pharmacokinetics and biocompatibility. J Mater Chem. 2011; 21(16): 5845.
27
28.Kurniawan A, Gunawan F, Nugraha AT, Ismadji S, Wang M-J. Biocompatibility and drug release behavior of curcumin conjugated gold nanoparticles from aminosilane-functionalized electrospun poly( N -vinyl-2-pyrrolidone) fibers. International Journal of Pharmaceutics. 2017; 516(1–2): 158–169.
28
29.Kotcherlakota R, Barui AK, Prashar S, Fajardo M, Briones D, Rodríguez-Diéguez A, Patra CR, Gómez-Ruiz S. Curcumin loaded mesoporous silica: an effective drug delivery system for cancer treatment. Biomater Sci. 2016; 4(3): 448–459.
29
30.Stöber W, Fink A, Bohn E. Controlled growth of monodisperse silica spheres in the micron size range. Journal of Colloid and Interface Science. 1968; 26(1): 62–69.
30
31.Kong Z-L, Kuo H-P, Johnson A, Wu L-C, Chang KLB. Curcumin-Loaded Mesoporous Silica Nanoparticles Markedly Enhanced Cytotoxicity in Hepatocellular Carcinoma Cells. IJMS. 2019; 20(12): 2918.
31
ORIGINAL_ARTICLE
The protective effects of curcumin and curmumin nanomicelle against cirrhotic cardiomyopathy in bile duct-ligated rats
Objective(s): Cirrhotic cardiomyopathy refers to cardiac muscle dysfunction caused by liver cirrhosis. Seemingly, free radicals and inflammatory factors play a critical role in the pathophysiology of cardiomyopathy. Curcumin has the anti-inflammatory, antioxidant, and anticancer properties . However, the therapeutic indications of this compound are limited due to its low absorption, rapid metabolism, and low bioavailability. Curcumin nanomicelle is a form of nanoparticle developed to overcome the poor kinetic profile of curcumin and enhance its bioavailability and therapeutic effects. The present study aimed to develop an experimental model of cirrhosis induced by biliary duct ligation in rats. Materials and Methods: The animals were kept until 28 days after the bile duct ligation and received curcumin or curcumin nanomicelle via oral gavage at various doses during days 7-28. After the intervention, the effects of curcumin and curcumin nanomicelle on cardiovascular function, some inflammatory and antioxidant biomarkers, and histopathological changes were assessed. Results: According to the findings, cardiac electrophysiology function and contractile force improved only in the curcumin nanomicelle groups. In addition, curcumin nanomicelle significantly reduced inflammatory factors and increased antioxidant enzymes. In the histopathological studies, cardiac tissue damage and destruction were observed to decrease in the curcumin nanomicelle groups. Conclusion: Therefore, it was concluded that curcumin nanomicelle plays a protective role in cirrhotic cardiomyopathy by reducing inflammatory and oxidative factors and improving the cardiac function. Furthermore, curcumin nanomicelle exhibited more significant therapeutic effects compared to the curcumin treatment groups.
https://nmj.mums.ac.ir/article_15149_a753e6ba3a7c72890b755913c883fbaa.pdf
2020-04-01
158
169
10.22038/nmj.2020.07.009
Cirrhosis
Cardiomyopathy
Curcumin
Nanomicelle
Inflammation
Mohammad
Sheibani
mohammad.sheibani89@gmail.com
1
Department of Pharmacology, School of Medicine, Tehran University of Medical Sciences, Tehran, Iran
AUTHOR
Ahmad Reza
Dehpour
2
Department of Pharmacology, School of Medicine, Tehran University of Medical Sciences, Tehran, Iran
AUTHOR
Sadaf
Nezamoleslami
sadaf.nezamoleslami@yahoo.com
3
Department of Pharmacology, School of Medicine, Tehran University of Medical Sciences, Tehran, Iran
AUTHOR
Seyedeh Elaheh
Mousavi
mousavielaheh90@gmail.com
4
Department of Pharmacology, School of Medicine, Tehran University of Medical Sciences, Tehran, Iran
AUTHOR
Mahmoud Reza
Jafari
JafariMR@mums.ac.ir
5
Department of Pharmaceutics, Mashhad University of Medical Sciences, Mashhad, Iran
AUTHOR
Seyed Mahdi
Rezayat Sorkhabadi
epouyan@hotmail.com
6
Department of Pharmacology, School of Medicine, Tehran University of Medical Sciences, Tehran, Iran
LEAD_AUTHOR
1.Davies M. The cardiomyopathies: an overview. Heart. 2000; 83(4): 469-674.
1
2.Wexler R, Elton T, Pleister A, Feldman D. Cardiomyopathy: an overview. Am Fam Physician. 2009; 79(9): 778-784.
2
3.Wong F. Cirrhotic cardiomyopathy. Hepatol Int. 2009; 3(1): 294-304.
3
4.Møller S, Lee SS. Cirrhotic cardiomyopathy. J Hepatol. 2018; 69(4): 958--960.
4
5.Møller S, Bernardi M. Interactions of the heart and the liver. Eur Heart J. 2013; 34(36): 2804-2811.
5
6.Regan TJ, Levinson GE, Oldewurtel HA, Frank MJ, Weisse AB, Moschos CB. Ventricular function in noncardiacs with alcoholic fatty liver: role of ethanol in the production of cardiomyopathy. J Clin Invest. 1969; 48(2): 397-407.
6
7.Ingles AC, Hernandez I, Garcia-Estan J, Quesada T, Carbonell LF. Limited cardiac preload reserve in conscious cirrhotic rats. Am J Physiol Heart Circ Physiol. 1991; 260(6): H1912-H7.
7
8.Pacher P, Bátkai S, Kunos G. Cirrhotic cardiomyopathy: an endocannabinoid connection? Br J Pharmacol. 2005; 146(3): 313-314.
8
9.Chayanupatkul M, Liangpunsakul S. Cirrhotic cardiomyopathy: review of pathophysiology and treatment. Hepatol Int. 2014; 8(3): 308-315.
9
10.Liu H, Song D, Lee SS. Cirrhotic cardiomyopathy. Gastroenterol Clin Biol. 2002; 26: 842–847.
10
11.Gaskari SA, Honar H, Lee SS. Therapy insight: cirrhotic cardiomyopathy. Nat Clin Pract Gastroenterol Hepatol. 2006; 3(6): 329-337.
11
12.van Obbergh L, Vallieres Y, Blaise G. Cardiac modifications occurring in the ascitic rat with biliary cirrhosis are nitric oxide related. J Hepatol. 1996; 24(6):747-452.
12
13.Ward CA, Liu H, Lee SS. Altered cellular calcium regulatory systems in a rat model of cirrhotic cardiomyopathy. Gastroenterology. 2001; 121(5):1209-218.
13
14.Kountouras J, Billing BH, Scheuer PJ. Prolonged bile duct obstruction: a new experimental model for cirrhosis in the rat. Br J Exp Pathol. 1984; 65(3): 305-311.
14
15.Chainani-Wu N. Safety and anti-inflammatory activity of curcumin: a component of tumeric (Curcuma longa). Int J Complement Altern Med. 2003; 9(1): 161-168.
15
16.Ammon HP, Wahl MA. Pharmacology of Curcuma longa. Planta medica. 1991; 57(01): 1-7.
16
17.Nisenberg O. Targeted Overexpression of S-adenosylmethionine Decarboxylase in Murine Hearts. 2003.
17
18.Foti MC. Antioxidant properties of phenols. J Pharm Pharmacol. 2007; 59(12): 1673-1685.
18
19.Kapakos G, Youreva V, Srivastava AK. Cardiovascular protection by curcumin: molecular aspects. Indian J Biochem Biophys. 2012; 49(5): 306-315.
19
20.Yu W, Wu J, Cai F, Xiang J, Zha W, Fan D. Curcumin alleviates diabetic cardiomyopathy in experimental diabetic rats. PLoS One. 2012; 7(12): e52013.
20
21.Hewlings SJ, Kalman DS. Curcumin: a review of its’ effects on human health. Foods. 2017; 22; 6(10). pii: E92.
21
22.Lavan DA, McGuire T, Langer R. Small-scale systems for in vivo drug delivery. Nat. Biotechnol. 2003; 21(10): 1184-1191.
22
23.Cavalcanti A, Shirinzadeh B, Freitas Jr RA, Hogg T. Nanorobot architecture for medical target identification. Nanotechnology. 2007; 19(1): 015103.
23
24.Mitra AK, Cholkar K, Mandal A. Emerging nanotechnologies for diagnostics, drug delivery and medical devices: William Andrew; 2017.
24
25.Rezayat S. The protective effect of nano-curcumin in experimental model of acute pancreatitis: The involvement of TLR4/NF-kB pathway. Nanomed J. 2018; 5(3): 138-143.
25
26.Dolati S, Ahmadi M, Aghebti-Maleki L, Nikmaram A, Marofi F, Rikhtegar R. Nanocurcumin is a potential novel therapy for multiple sclerosis by influencing inflammatory mediators. Pharmacol Rep. 2018; 70(6): 1158-1167.
26
27.Tarcin O, Basaranoglu M, Tahan V, Tahan G, Sücüllü I, Yilmaz N. Time course of collagen peak in bile duct-ligated rats. BMC Gastroenterol. 2011;11(1): 45.
27
28.Mani AR, Ippolito S, Ollosson R, Moore KP. Nitration of cardiac proteins is associated with abnormal cardiac chronotropic responses in rats with biliary cirrhosis. Hepatology. 2006; 43(4): 847-856.
28
29.Garrido M, Escobar C, Zamora C, Rejas C, Varas J, Párraga M, et al. Bile duct ligature in young rats: A revisited animal model for biliary atresia. Eur J Histochem. 2017; 61(3): 2803.
29
30.Yang Y, Chen B, Chen Y, Zu B, Yi B, Lu K. A comparison of two common bile duct ligation methods to establish hepatopulmonary syndrome animal models. Lab Anim. 2015; 49(1): 71-79.
30
31.Gaskari SA, Liu H, Moezi L, Li Y, Baik SK, Lee SS. Role of endocannabinoids in the pathogenesis of cirrhotic cardiomyopathy in bile duct‐ligated rats. Br J Pharmacol. 2005; 146(3): 315-323.
31
32.Bruck R, Ashkenazi M, Weiss S, Goldiner I, Shapiro H, Aeed H. Prevention of liver cirrhosis in rats by curcumin. Liver Int. 2007; 27(3): 373-383.
32
33.Li L, Duan M, Chen W, Jiang A, Li X, Yang J, et al. The spleen in liver cirrhosis: revisiting an old enemy with novel targets. J Transl Med. 2017; 15(1): 111.
33
34.Moore K, Roberts LJ. Measurement of lipid peroxidation. Free Radic Res. 1998; 28(6): 659-671.
34
35.Ohkawa H, Ohishi N, Yagi K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem. 1979; 95(2): 351-358.
35
36.Ighodaro O, Akinloye O. First line defence antioxidants-superoxide dismutase (SOD), catalase (CAT) and glutathione peroxidase (GPX): Their fundamental role in the entire antioxidant defence grid. Alex J Med. 2018; 54(4): 287-293.
36
37.Haq MM, Legha SS, Choksi J, Hortobagyi GN, Benjamin RS, Ewer M. Doxorubicin‐induced congestive heart failure in adults. Cancer. 1985; 56(6): 1361-1365.
37
38.Yarmohmmadi F, Rahimi N, Faghir-Ghanesefat H, Javadian N, Abdollahi A, Pasalar P. Protective effects of agmatine on doxorubicin-induced chronic cardiotoxicity in rat. Eur J Pharmacol. 2017; 796: 39-44.
38
39.Sheibani M, Nezamoleslami S, Faghir-Ghanesefat H, hossein Emami A, Dehpour AR. Cardioprotective effects of dapsone against doxorubicin-induced cardiotoxicity in rats. Cancer Chemother Pharmacol. 2020:1-9.
39
40.Radu R, Bold A, Pop O, Mălăescu D, Gheorghişor I, Mogoantă L. Histological and immunohistochemical changes of the myocardium in dilated cardiomyopathy. Rom J Morphol Embryol. 2012; 53(2): 269-275.
40
41.Timoh T, Protano M, Wagman G, Bloom M, Vittorio T, editors. A perspective on cirrhotic cardiomyopathy. Transplantation proceedings; 2011: Elsevier.
41
42.Gassanov N, Caglayan E, Semmo N, Massenkeil G, Er F. Cirrhotic cardiomyopathy: a cardiologist’s perspective. World J Gastroenterol. 2014; 20(42): 15492-15498.
42
43.Møller S, Hove JD, Dixen U, Bendtsen F. New insights into cirrhotic cardiomyopathy. Int J Cardiol. 2013; 167(4): 1101-1108.
43
44.Liu H, Lee SS. Nuclear factor‐κB inhibition improves myocardial contractility in rats with cirrhotic cardiomyopathy. Liver Int. 2008; 28(5): 640-648.
44
45.Sánchez-Fidalgo S, Cárdeno A, Villegas I, Talero E, de la Lastra CA. Dietary supplementation of resveratrol attenuates chronic colonic inflammation in mice. Eur J Pharmacol. 2010; 633(1-3): 78-84.
45
46.Bereswill S, Muñoz M, Fischer A, Plickert R, Haag L-M, Otto B, et al. Anti-inflammatory effects of resveratrol, curcumin and simvastatin in acute small intestinal inflammation. PloS one. 2010; 3;5(12): e15099..
46
47.Mošovská S, Petáková P, Kaliňák M, Mikulajová A. Antioxidant properties of curcuminoids isolated from Curcuma longa L. Acta Chimica Slovaca. 2016; 9(2): 130-135.
47
48.Menon VP, Sudheer AR. Antioxidant and anti-inflammatory properties of curcumin. The molecular targets and therapeutic uses of curcumin in health and disease: Springer; 2007. p. 105-125.
48
49.Jurenka JS. Anti-inflammatory properties of curcumin, a major constituent of Curcuma longa: a review of preclinical and clinical research. Alternative medicine review. 2009; 14(2).
49
50.Hatamipour M, Sahebkar A, Alavizadeh SH, Dorri M, Jaafari MR. Novel nanomicelle formulation to enhance bioavailability and stability of curcuminoids. Iran J Basic Med Sci. 2019; 22(3): 282-289.
50
51.Javadi M, Khadem Haghighian H, Goodarzy S, Abbasi M, Nassiri‐Asl M. Effect of curcumin nanomicelle on the clinical symptoms of patients with rheumatoid arthritis: A randomized, double‐blind, controlled trial. Int J Rheum Dis. 2019; 22(10): 1857-1862.
51
52.Sundar Dhilip Kumar S, Houreld NN, Abrahamse H. Therapeutic potential and recent advances of curcumin in the treatment of aging-associated diseases. Molecules. 2018; 23(4): 835.
52
53.Rahimi HR, Nedaeinia R, Shamloo AS, Nikdoust S, Oskuee RK. Novel delivery system for natural products: Nano-curcumin formulations. Avicenna J Phytomed. 2016 Jul-Aug; 6(4): 383-398.
53
54.Fourlas CA, Alexopoulou AA. Cirrhotic cardiomyopathy. Hellenic J Cardiol. 2004; 45:114-120.
54
55.Karagiannakis DS, Vlachogiannakos J, Anastasiadis G, Vafiadis-Zouboulis I, Ladas SD. Frequency and severity of cirrhotic cardiomyopathy and its possible relationship with bacterial endotoxemia. Dig Dis Sci. 2013; 58(10): 3029-3036.
55
56.Behrendt P, Preusse-Prange A, Klüter T, Haake M, Rolauffs B, Grodzinsky A. IL-10 reduces apoptosis and extracellular matrix degradation after injurious compression of mature articular cartilage. Osteoarthritis Cartilage. 2016; 24(11): 1981-1988.
56
57.Hofstetter C, Flondor M, Hoegl S, Muhl H, Zwissler B. Interleukin-10 aerosol reduces proinflammatory mediators in bronchoalveolar fluid of endotoxemic rat. Crit Care Med. 2005; 33(10): 2317-2322.
57
58.Hellenbrand DJ, Reichl KA, Travis BJ, Filipp ME, Khalil AS, Pulito DJ. Sustained interleukin-10 delivery reduces inflammation and improves motor function after spinal cord injury. J Neuroinflammation. 2019; 16(1): 93.
58
59.Khan J, Noboru N, Young A, Thomas D. Pro and anti-inflammatory cytokine levels (TNF-α, IL-1β, IL-6 and IL-10) in rat model of neuroma. Pathophysiology. 2017; 24(3): 155-159.
59
60.Mu W, Ouyang X, Agarwal A, Zhang L, Long DA, Cruz PE, et al. IL-10 suppresses chemokines, inflammation, and fibrosis in a model of chronic renal disease. J Am Soc Nephrol. 2005; 16(12): 3651-3660.
60
61.Amirshahrokhi K, Ghazi-Khansari M, Mohammadi-Farani A, Karimian G. Effect of captopril on TNF-α and IL-10 in the livers of bile duct ligated rats. Iranian J Immunol. 2010; 7(4): 247-251.
61
62.Niki E. Lipid peroxidation products as oxidative stress biomarkers. Biofactors. 2008; 34(2): 171-180.
62
63.Gaweł S, Wardas M, Niedworok E, Wardas P. Malondialdehyde (MDA) as a lipid peroxidation marker. Wiadomosci lekarskie (Warsaw, Poland: 1960). 2004; 57(9-10): 453-455.
63
64.Wolf G. The discovery of the antioxidant function of vitamin E: the contribution of Henry A. Mattill. J Nutr. 2005; 135(3): 363-366.
64
65.Lobo V, Patil A, Phatak A, Chandra N. Free radicals, antioxidants and functional foods: Impact on human health. Pharmacognosy reviews. 2010; 4(8): 118.
65
66.Espinosa-Diez C, Miguel V, Mennerich D, Kietzmann T, Sánchez-Pérez P, Cadenas S, et al. Antioxidant responses and cellular adjustments to oxidative stress. Redox biology. 2015; 6: 183-197.
66
67.Hwang C, Sinskey AJ, Lodish HF. Oxidized redox state of glutathione in the endoplasmic reticulum. Science. 1992; 257(5076): 1496-502.
67
68.Wang X-L, Li T, Li J-H, Miao S-Y, Xiao X-Z. The effects of resveratrol on inflammation and oxidative stress in a rat model of chronic obstructive pulmonary disease. Molecules. 2017; 22(9): 1529.
68
69.Lebovitz RM, Zhang H, Vogel H, Cartwright J, Dionne L, Lu N. Neurodegeneration, myocardial injury, and perinatal death in mitochondrial superoxide dismutase-deficient mice. Proceedings of the National Academy of Sciences. 1996; 93(18): 9782-9787.
69