Protective and modulatory effects of royal jelly used against the induced changes in silver nanoparticles on the hippocampus of male rats

Document Type: Research Paper

Authors

1 Department of Anatomy, School of Medicine, Rafsanjan University of Medical Sciences, Rafsanjan, Iran

2 Department of Anatomical Sciences, School of Medicine, Social Determinants of Health Research Center, Rafsanjan University of Medical Sciences, Rafsanjan, Iran

3 Department of Anatomical Sciences, School of Medicine, Rafsanjan University of Medical Sciences, Rafsanjan

4 Department of Immunology, School of Medicine, Kerman University of Medical Sciences, Kerman, Iran

5 Department of Immunology, Immunology of Infectious Disease Research Center, Rafsanjan University of Medical Sciences, Rafsanjan, Iran

6 Department of Anatomical Sciences, School of Medicine, Fertility and Infertility Research Center, Kermanshah University of Medical Sciences, Kermanshah, Iran

7 Department of Anatomical Sciences, School of Medicine, Kermanshah University of Medical Sciences, Kermanshah, Iran

8 Department of Physiology and Pharmacology, School of Medicine, Physiology-Pharmacology Research Center, Rafsanjan University of Medical Sciences, Rafsanjan, Iran

9 Department of Anatomical Sciences, School of Medicine, Immunology of Infectious Diseases Research Center, Rafsanjan University of Medical Sciences, Rafsanjan, Iran

Abstract

Objective (s): Silver nanoparticles (NPs) have attracted considerable attention owing to their important properties, including antimicrobial and anti-oxidative stress effects. However, high concentrations of silver NPs have been reported to have toxic effects. The present study aimed to evaluate the modulatory and protective effects of royal jelly (RJ) against the harmful effects of silver NPs on hippocampal functions, such as learning and memory.
Materials and Methods: This experimental study was conducted on 40 male Wistar rats. The animals were divided into four groups of 10, including the control group (no silver NPs and RJ), RJ group, silver NPs plus RJ, and silver NPs. Some functions of the hippocampus (e.g., learning and memory) were evaluated using Morris memory function tests for four consecutive days. In addition, the relative expression of TRPV1 was assessed using real-time polymerase chain reaction (RT-PCR). At the final stage, hippocampal tissues were collected for histological studies.
Results: Levels of learning and memory, relative gene expression ratio of TRPV1, and the histological changes in the hippocampus were significantly different in the groups receiving silver NPs compared to the groups administered with RJ.
Conclusion: According to the results, RJ may be the effective in the protection against the adverse effects of silver NPs and improve the function of the hippocampus.

Keywords


1.Song JY, Kim BS. Rapid biological synthesis of silver nanoparticles using plant leaf extracts. Bioprocess Biosyst Eng. 2009; 32(1):79.
2.Sharma VK, Yngard RA, Lin Y. Silver nanoparticles: green synthesis and their antimicrobial activities. Adv Colloid Interface Sci. 2009; 145(1-2): 83-96.
3.AshaRani P, Low Kah Mun G, Hande MP, Valiyaveettil S. Cytotoxicity and genotoxicity of silver nanoparticles in human cells. ACS Nano. 2008; 3(2): 279-90.
4.Safaepour M, Shahverdi AR, Shahverdi HR, Khorramizadeh MR, Gohari AR. Green synthesis of small silver nanoparticles using geraniol and its cytotoxicity against fibrosarcoma-wehi 164. Avicenna J Med Biotechnol. 2009; 1(2): 111.
5.Arora S, Jain J, Rajwade J, Paknikar K. Cellular responses induced by silver nanoparticles: in vitro studies. Toxicol Lett. 2008; 179(2): 93-100.
6.Eom H-J, Choi J. p38 MAPK activation, DNA damage, cell cycle arrest and apoptosis as mechanisms of toxicity of silver nanoparticles in Jurkat T cells. Environ Sci Technol. 2010; 44(21): 8337-8342.
7.Walf AA, Frye CA. A review and update of mechanisms of estrogen in the hippocampus and amygdala for anxiety and depression behavior. Neuropsychopharmacologyl. 2006; 31(6): 1097.
8.Ho WS, Barrett D, Randall M. ‘Entourage’effects of N‐palmitoylethanolamide and N‐oleoylethanolamide on vasorelaxation to anandamide occur through TRPV1 receptors. Br J Pharmacol. 2008; 155(6): 837-846.
9.Guo H, Kouzuma Y, Yonekura M. Structures and properties of antioxidative peptides derived from royal jelly protein. Food Chemistryl. 2009; 113(1): 238-245.
10.Silici S, Ekmekcioglu O, Eraslan G, Demirtas A. Antioxidative effect of royal jelly in cisplatin-induced testes damage. Urologyl. 2009; 74(3): 545-551.
11.Spannhoff A, Kim YK, Raynal NJM, Gharibyan V, Su MB, Zhou YY, Li J, Castellano S, Sbardella G, Issa JPJ. Histone deacetylase inhibitor activity in royal jelly might facilitate caste switching in bees. EMBO Rep. 2011; 12(3): 238-243.
12.Zamani Z, Reisi P, Alaei H, Pilehvarian AA. Effect of royal jelly on spatial learning and memory in rat model of streptozotocin-induced sporadic alzheimer’s disease. Adv Biomed Res. 2012; 1.
13.Hattori N, Ohta S, Sakamoto T, Mishima S, Furukawa S. Royal jelly facilitates restoration of the cognitive ability in trimethyltin-intoxicated mice. Evid Based Complement Alternat Med. 2011; 2011.
14.Huang H, Li L, Shi W, Liu H, Yang J, Yuan X, Wu L. The multifunctional effects of nobiletin and its metabolites in vivo and in vitro. Evid Based Complement Alternat Med. 2016; 2016.
15.Ataei ML, Ebrahimzadeh-bideskan AR. The effects of nano-silver and garlic administration during pregnancy on neuron apoptosis in rat offspring hippocampus. Iran J Basic Med Sci. 2014; 17(6): 411.
16.Bromley-Brits K, Deng Y, Song W. Morris water maze test for learning and memory deficits in Alzheimer’s disease model mice. Journal of visualized experiments: J Vis Exp. 2011; (53).
17.Kappeler C, Dhenain M, Phan Dinh Tuy F, Saillour Y, Marty S, Fallet‐Bianco C, Souville I, Souil E, Pinard JM, Meyer G. Magnetic resonance imaging and histological studies of corpus callosal and hippocampal abnormalities linked to doublecortin deficiency. J Comp Neurol. 2007; 500(2): 239-254.
18.Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem. 2009; 55(4): 611-622.
19.Rahman M, Wang J, Patterson T, Saini U, Robinson B, Newport G, Murdock R, Schlager J, Hussain S, Ali S. Expression of genes related to oxidative stress in the mouse brain after exposure to silver-25 nanoparticles. Toxicol Lett. 2009; 187(1): 15-21.
20.Foldbjerg R, Olesen P, Hougaard M, Dang DA, Hoffmann HJ, Autrup H. PVP-coated silver nanoparticles and silver ions induce reactive oxygen species, apoptosis and necrosis in THP-1 monocytes. Toxicology lett. 2009; 190(2): 156-162.
21.Hattori N, Nomoto H, Fukumitsu H, Mishima S, Furukawa S. Royal jelly-induced neurite outgrowth from rat pheochromocytoma PC12 cells requires integrin signal independent of activation of extracellular signalregulated kinases. Biomed Res. 2007; 28(3): 139-146.
22.Gutteridge J. Lipid peroxidation and antioxidants as biomarkers of tissue damage. Clin Chem. 1995; 41(12): 1819-1828.
23.Zhao C-H, Liu H-Q, Cao R, Ji A-L, Zhang L, Wang F, Yang R-H. Effects of dietary fish oil on learning function and apoptosis of hippocampal pyramidal neurons in streptozotocin-diabetic rats. Brain Res. 2012; 1457: 33-43.
24.You I-J, Jung Y-H, Kim M-J, Kwon S-H, Hong S-I, Lee S-Y, Jang C-G. Alterations in the emotional and memory behavioral phenotypes of transient receptor potential vanilloid type 1-deficient mice are mediated by changes in expression of 5-HT1A, GABAA, and NMDA receptors. Neuropharmacologyl. 2012; 62(2): 1034-1043.
25.Zamani Z, Reisi P, Alaei H, Pilehvarian A. Effect of royal jelly on improving passive avoidance learning and spatial learning and memory in rats. SSU_Journalsl. 2012; 20(2): 211-219.