Enhanced cytotoxicity of auraptene to prostate cancer cells by dextran-coated Fe3O4 nanoparticles

Document Type : Research Paper

Authors

1 Department of Pharmacognosy, School of Pharmacy, Mashhad University of Medical Sciences, Mashhad, Iran

2 Biotechnology Research Center, Pharmaceutical Technology Institute, Mashhad University of Medical Sciences, Mashhad, Iran

3 Targeted Drug Delivery Research Center, Pharmaceutical Technology Institute, Mashhad University of Medical Sciences, Mashhad, Iran

4 Department of Pharmaceutics, School of Pharmacy, Mashhad University of Medical Sciences, Mashhad, Iran

Abstract

Purpose: Auraptene (AUR) is a monoterpene coumarin compound with several biological activities specifically anti-cancer. The bioavailability of AUR in biological fluids is negligible, thus, the cytotoxicity of this compound for the target cells is low. Herein, the synthesis of AUR-coated Fe3O4 nanoparticles is presented as a strategy to increase the cytotoxicity of AUR on PC3, DU145, and LNCaP prostate cancer cells.

Methods: Fe3O4 nanoparticles were synthesized via co-precipitation method, coated with AUR and stabilized by dextran. They were characterized by X-ray diffraction spectroscopy (XRD), Fourier-transform infrared spectroscopy (FTIR), scanning electron microscopy (SEM), dynamic light scattering (DLS) analysis, and vibrating sample magnetometry (VSM). In vitro release test for coated nanoparticles was performed in both physiologic (pH= 7.4) and acidic (pH= 5.5) environments. Cytotoxicity for prostate cancer cells was evaluated by AlamarBlue assay and the results were analyzed by one-way and two-way ANOVA tests.

Results: Characterization outcomes represented the formation of magnetic nanoparticles with good crystalline structure, relatively spherical shape and superparamagnetic properties. AUR release profile from nanoparticles demonstrated that coated nanoparticles are able to inhibit burst release of this compound. AUR release was remarkably higher in acidic medium that can be advantageous for treating tumor regions. Cytotoxicity results indicated that AUR had a very low toxicity against prostate cancer cells at the tested concentrations. In contrast, AUR-coated Fe3O4 nanoparticles were significantly cytotoxic on all the cell lines.

Conclusion: The coating of AUR on the surface of Fe3O4 nanoparticles was a successful approach to enhance the efficacy and cytotoxicity of this compound.

Keywords

References

1. Siegel RL, Miller KD, Jemal A. Cancer Statistics, 2017. CA Cancer J Clin. 2017; 67(1): 7-30. 
2. Xu J, Zheng SL, Komiya A, Mychaleckyj JC, Isaacs SD, Hu JJ, et al. Germline mutations and sequence variants of the macrophage scavenger receptor 1 gene are associated with prostate cancer risk. Nat Genet. 2002; 32(2): 321-325. 
3. Nelson WG, De Marzo AM, Isaacs WB. Prostate cancer. N Engl J Med. 2003; 349(4): 366-381. 
4. Lee JC, Shin EA, Kim B, Kim BI, Chitsazian-Yazdi M, Iranshahi M, et al. Auraptene induces apoptosis via myeloid cell leukemia 1-mediated activation of caspases in PC3 and DU145 prostate cancer cells. Phytother Res. 2017; 31(6): 891-898. 
5. Soltani F, Mosaffa F, Iranshahi M, Karimi G, Malekaneh M, Haghighi F, et al. Auraptene from Ferula szowitsiana protects human peripheral lymphocytes against oxidative stress. Phytother Res. 2010; 24(1): 85-89. 
6. Kuroyanagi K, Kang MS, Goto T, Hirai S, Ohyama K, Kusudo T, et al. Citrus auraptene acts as an agonist for PPARs and enhances adiponectin production and MCP-1 reduction in 3T3-L1 adipocytes. Biochem Biophys Res Commun. 2008; 366(1): 219-225. 
7. Genovese S, Ashida H, Yamashita Y, Nakgano T, Ikeda M, Daishi S, et al. The interaction of auraptene and other oxyprenylated phenylpropanoids with glucose transporter type 4. Phytomedicine. 2017; 32: 74-79.
8. Nishimoto S, Muranaka A, Nishi K, Kadota A, Sugahara T. Immunomodulatory effects of Citrus fruit auraptene in vitro and in vivo. J Funct Foods. 2012; 4(4): 883-890. 
9. Askari VR, Baradaran Rahimi V, Rezaee SA, Boskabady MH. Auraptene regulates Th1/Th2/TReg balances, NF-kappaB nuclear localization and nitric oxide production in normal and Th2 provoked situations in human isolated lymphocytes. Phytomedicine. 2018; 43: 1-10. 
10. Fiorito S, Epifano F, Preziuso F, Cacciatore I, di Stefano A, Taddeo VA, et al. Natural oxyprenylated coumarins are modulators of melanogenesis. Eur J Med Chem. 2018; 152: 274-282. 
11. Niu X, Huang Z, Zhang L, Ren X, Wang J. Auraptene has the inhibitory property on murine T lymphocyte activation. Eur J Pharmacol. 2015; 750: 8-13.
12. Okuyama S, Minami S, Shimada N, Makihata N, Nakajima M, Furukawa Y. Anti-inflammatory and neuroprotective effects of auraptene, a Citrus coumarin, following cerebral global ischemia in mice. Eur J Pharmacol. 2013; 699: 118-123. 
13. Ghanbarabadi M, Iranshahi M, Amoueian S, Mehri S, Motamedshariaty VS, Mohajeri SA. Neuroprotective and memory enhancing effects of auraptene in a rat model of vascular dementia: Experimental study and histopathological evaluation. Neurosci Lett. 2016; 623: 13-21. 
14. Nakajima M, Shimizu R, Furuta K, Sugino M, Watanabe T, Aoki R, et al. Auraptene induces oligodendrocyte lineage precursor cells in a cuprizone-induced animal model of demyelination. Brain Res. 2016; 1639: 28-37. 
15. Kawabata K, Murakami A, Ohigashi H. Citrus auraptene targets translation of MMP-7 (matrilysin) via ERK1/2-dependent and mTOR-independent mechanism. FEBS Lett. 2006; 580(22): 5288-5294. 
16. Krishnan P, Yan KJ, Windler D, Tubbs J, Grand R, Li BD, et al. Citrus auraptene suppresses cyclin D1 and significantly delays N-methyl nitrosourea induced mammary carcinogenesis in female Sprague-Dawley rats. BMC Cancer. 2009; 9: 259. 
17. Krishnan P, Kleiner-Hancock H. Effects of auraptene on IGF-1 stimulated cell cycle progression in the human breast cancer cell line, MCF-7. Int J Breast Cancer. 2012; 2012: 502092. 
18. Tang M, Ogawa K, Asamoto M, Hokaiwado N, Seeni A, Suzuki S, et al. Protective effects of Citrus nobiletin and auraptene in transgenic rats developing adenocarcinoma of the prostate (TRAP) and human prostate carcinoma cells. Cancer Sci. 2007; 98(4): 471-477.
19. Chenthamara D, Subramaniam S, Ramakrishnan SG, Krishnaswamy S, Essa MM, Lin FH, et al. Therapeutic efficacy of nanoparticles and routes of administration. Biomater Res. 2019; 23(1): 20.20. Patra JK, Das G, Fraceto LF, Campos EVR, Rodriguez-Torres MDP, Acosta-Torres LS, et al. Nano based drug delivery systems: Recent developments and future prospects. J Nanobiotechnol. 2018; 16: 71. 
21. He X, Hwang HM. Nanotechnology in food science: Functionality, applicability, and safety assessment. J Food Drug Anal. 2016; 24: 671-681. 
22. Jeevanandam J, Barhoum A, Chan YS, Dufresne A, Danquah MK. Review on nanoparticles and nanostructured materials: History, sources, toxicity and regulations. Beilstein J Nanotechnol. 2018; 9: 1050-1074. 
23. Rao PV, Nallappan D, Madhavi K, Rahman S, Jun Wei L, Gan SH. Phytochemicals and biogenic metallic nanoparticles as anticancer agents. Oxid Med Cell Longev. 2016; 2016: 3685671. 
24. Hernández-Hernández AA, Aguirre-Álvarez G, Cariño-Cortés R, Mendoza-Huizar LH, Jiménez-Alvarado R. Iron oxide nanoparticles: Synthesis, functionalization, and applications in diagnosis and treatment of cancer. Chem Pap. 2020; 74: 3809-3824. 
25. Wu W, Wu Z, Yu T, Jiang C, Kim WS. Recent progress on magnetic iron oxide nanoparticles: Synthesis, surface functional strategies and biomedical applications. Sci Technol Adv Mater. 2015; 16: 023501. 
26. Vangijzegem T, Stanicki D, Boutry S, Paternoster Q, Vander Elst L, Muller RN, et al. VSION as high field MRI T1 contrast agent: Evidence of their potential as positive contrast agent for magnetic resonance angiography. Nanotechnology. 2018; 29: 265103. 
27. Pham HN, Pham THG, Nguyen DT, Phan QT, Le TTH, Ha PT, et al. Magnetic inductive heating of organs of mouse models treated by copolymer coated Fe3O4 nanoparticles. Adv Nat Sci Nanosci Nanotechnol. 2017; 8: 025013. 
28. Gupta AK, Gupta M. Synthesis and surface engineering of iron oxide nanoparticles for biomedical applications. Biomaterials. 2005; 26: 3995-4021. 
29. Vangijzegem T, Stanicki D, Laurent S. Magnetic iron oxide nanoparticles for drug delivery: Applications and characteristics. Expert Opin Drug Deliv. 2019; 16: 69-78. 
30. Parveen S, Misra R, Sahoo SK. Nanoparticles: A boon to drug delivery, therapeutics, diagnostics and imaging. Nanomedicine. 2012; 8: 147-166. 
31. Teja AS, Koh PY. Synthesis, properties, and applications of magnetic iron oxide nanoparticles. Prog Cryst Growth Charact Mater. 2009; 55: 22-45. 
32. Laurent S, Forge D, Port M, Roch A, Robic C, Vander Elst L, et al. Magnetic iron oxide nanoparticles: Synthesis, stabilization, vectorization, physicochemical characterizations, and biological applications. Chem Rev. 2008; 108: 2064-2110. 
33. Ali A, Zafar H, Zia M, Ul Haq I, Phull AR, Ali JS, et al. Synthesis, characterization, applications, and challenges of iron oxide nanoparticles. Nanotechnol Sci Appl. 2016; 9: 49-67.
34. Zamani H, Rastegari B, Varamini M. Antioxidant and anti-cancer activity of Dunaliella salina extract and oral drug delivery potential via nano-based formulations of gum Arabic coated magnetite nanoparticles. J Drug Deliv Sci Technol. 2019; 54: 101278. 
35. Soshnikova YM, Roman SG, Chebotareva NA, Baum OI, Obrezkova MV, Gillis RB, et al. Starch-modified magnetite nanoparticles for impregnation into cartilage. J Nanopart Res. 2013; 15: 2092. 
36. Nadeem M, Ahmad M, Akhtar MS, Shaari A, Riaz S, Naseem S, et al. Magnetic properties of polyvinyl alcohol and doxorubicine loaded iron oxide nanoparticles for anticancer drug delivery applications. PloS One. 2016; 11(6): e0158084. 
37. Viali WR, da Silva Nunes E, dos Santos CC, da Silva SW, Aragón FH, Coaquira JAH, et al. PEGylation of SPIONs by polycondensation reactions: A new strategy to improve colloidal stability in biological media. J Nanopart Res. 2013; 15: 1824. 
38. Tai MF, Lai CW, Abdul Hamid SB. Facile synthesis polyethylene glycol coated magnetite nanoparticles for high colloidal stability. J Nanomater. 2016; 2016: 8612505.
39. Zeinali S, Nasirimoghaddam S, Sabbaghi S. Investigation of the synthesis of chitosan coated iron oxide nanoparticles under different experimental conditions. Int J Nanosci Nanotechnol. 2016; 12(3): 183-190. 
40. Unsoy G, Yalcin S, Khodadust R, Gunduz G, Gunduz U. Synthesis optimization and characterization of chitosan-coated iron oxide nanoparticles produced for biomedical applications. J Nanopart Res. 2012; 14: 964. 
41. Shagholani H, Ghoreishi SM. Investigation of tannic acid cross-linked onto magnetite nanoparticles for applying in drug delivery systems. J Drug Deliv Sci Technol. 2017; 39: 88-94. 
42. Regmi R, Gumber V, Subba Rao V, Kohli I, Black C, Sudakar C, et al. Discrepancy between different estimates of the hydrodynamic diameter of polymer-coated iron oxide nanoparticles in solution. J Nanopart Res. 2011; 13: 6869-6875. 
43. Unterweger H, Dézsi L, Matuszak J, Janko C, Poettler M, Jordan J, et al. Dextran-coated superparamagnetic iron oxide nanoparticles for magnetic resonance imaging: Evaluation of size-dependent imaging properties, storage stability and safety. Int J Nanomedicine. 2018; 13: 1899-1915.
44. Liu G, Hong RY, Guo L, Liu GH, Feng B, Li YG. Exothermic effect of dextran-coated Fe3O4 magnetic fluid and its compatibility with blood. Colloid Surf A Physicochem Eng Asp. 2011; 380: 327-333. 
45. Tartaj P, Morales MP, Veintemillas-Verdaguer S, Gonzalez-Carreno T, Serna CJ. Synthesis, properties and biomedical applications of magnetic nanoparticles. In: Buschow KHJ, editor. Handbook of Magnetic Materials. Amsterdam, Netherlands: Elsevier; 2006. p. 403.
46. U.S. Department of Health and Human Services, Food and Drug Administration, Center for Drug Evaluation and Research. Extended release oral dosage forms: Development, evaluation, and application of in vitro/in vivo correlations. FDA Marylannd 1997; pp. 1-27.
47. Lakay E. Superparamagnetic iron oxide based nanoparticles for the separation and recovery of precious metals from solution [dissertation]. Stellenbosch, University of Stellenbosch. 2009.
48. Haw CY, Chia CH, Zakaria S, Mohamed F, Radiman S, Teh CH, et al. Morphological studies of randomized dispersion magnetite nanoclusters coated with silica. Ceram Int. 2011; 37(2): 451-64. 
49. Rajesh Kumar S, Priyatharshni S, Babu VN, Mangalaraj D, Viswanathan C, Kannan S, et al. Quercetin conjugated superparamagnetic magnetite nanoparticles for in-vitro analysis of breast cancer cell lines for chemotherapy applications. J Colloid Interface Sci. 2014; 436: 234-242. 
50. Daneshmand S, Jaafari MR, Movaffagh J, Malaekeh-Nikouei B, Iranshahi M, Seyedian Moghaddam A, et al. Preparation, characterization, and optimization of auraptene-loaded solid lipid nanoparticles as a natural anti-inflammatory agent: In vivo and in vitro evaluations. Colloids Surf B Biointerfaces. 2018; 164: 332-339. 
51. Almahy HA, Alagimi AA. Coumarins from the roots of Cleme Viscosa (L.) antimicrobial and cytotoxic studies. Arab J Chem. 2012; 5: 241-244. doi: 10.1016/j.arabjc.2011.03.019
52. Riddick TM. Control of colloid stability through zeta potential. Wynnewood, USA: Livingston Publishing Co.; 1968.
53. Carmen Bautista M, Bomati-Miguel O, del Puerto Morales M, Serna CJ, Veintemillas-Verdaguer S. Surface characterisation of dextran-coated iron oxide nanoparticles prepared by laser pyrolysis and coprecipitation. J Magn Magn Mater. 2005; 293: 20-27. 
54. Fu W, Yang H, Hari B, Liu S, Li M, Zou G. Preparation and characteristics of core–shell structure cobalt/silica nanoparticles. Mater Chem Phys. 2006; 100: 246-250. 
55. Woo K, Hong J. Surface modification of hydrophobic iron oxide nanoparticles for clinical applications. IEEE Trans Magn. 2005; 41: 4137-4139. 
56. Costa P, Sousa Lobo JM. Modeling and comparison of dissolution profiles. Eur J Pharm Sci. 2001; 13: 123-133.
57. Sato A, Itcho N, Ishiguro H, Okamoto D, Kobayashi N, Kawai K, et al. Magnetic nanoparticles of Fe3O4 enhance docetaxel-induced prostate cancer cell death. Int J Nanomedicine. 2013; 8: 3151-3160. 
58. Khorramizadeh MR, Esmail-Nazari Z, Zarei-Ghaane Z, Shakibaie M, Mollazadeh-Moghaddam K, Iranshahi M, et al. Umbelliprenin-coated Fe3O4 magnetite nanoparticles: Antiproliferation evaluation on human fibrosarcoma cell line (HT-1080). Mater Sci Eng C. 2010; 30: 1038-1042. 
59. Mohtashami L, Ghows N, Tayarani-Najaran Z, Iranshahi M. Galbanic acid-coated Fe3O4 magnetic nanoparticles with enhanced cytotoxicity to prostate cancer cells. Planta Med. 2019; 85: 169-178. 
60. Yallapu MM, Othman SF, Curtis ET, Bauer NA, Chauhan N, Kumar D, et al. Curcumin-loaded magnetic nanoparticles for breast cancer therapeutics and imaging applications. Int J Nanomedicine. 2012; 7: 1761-1779. 
61. Verma NK, Crosbie-Staunton K, Satti A, Gallagher S, Ryan KB, Doody T, et al. Magnetic core-shell nanoparticles for drug delivery by nebulization. J Nanobiotechnol. 2013; 11: 1. 
62. Shahabadi N, Akbari A, Karampour F, Falsafi M. Cytotoxicity and antibacterial activities of new chemically synthesized magnetic nanoparticles containing eugenol. J Drug Deliv Sci Technol. 2019; 49: 113-122. 
Nanomedicine Journal
Volume 9, Issue 1
January 2022
Pages 77-86

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