Zinc Nanoparticles Ameliorate the Reproductive Toxicity Induced by Silver Nanoparticles in Male Rats

References

• Johnston HJ, Hutchison G, Christensen FM, Peters S, Hankin S, Stone V. A review of the in vivo and in vitro toxicity of silver and gold particulates: particle attributes and biological mechanisms responsible for the observed toxicity. Crit Rev Toxicol. 2010;40(4):328–346.
   PubMed Web of Science ®Google Scholar
• Silvestry-Rodriguez N, Sicairos-Ruelas EE, Gerba CP, Bright KR. Silver as a disinfectant. Rev Environ Contam Toxicol. 2007;191:23–45.
   PubMed Web of Science ®Google Scholar
• Marambio-Jones C, Hoek EMV. A review of the antibacterial effects of silver nanomaterials and potential implications for human health and the environment. J Nanoparticle Res. 2010;12:1531–1551.
   Web of Science ®Google Scholar
• Samuel U, Guggenbichler JP. Prevention of catheter-related infections: the potential of a new nano-silver impregnated catheter. Int J Antimicrob Agents. 2004;1:75–78.
   Google Scholar
• Kalishwaralal K, Barathmanikanth S, Pandian SR, Deepak V, Gurunathan S. Silver nano- a trove for retinal therapies. J Controlled Release. 2010;145(2):76–90.
   PubMedGoogle Scholar
• Sung JH, Ji JH, Park JD, et al. Subchronic inhalation toxicity of silver nanoparticles. Toxicol Sci. 2009;108:452–461.
   PubMed Web of Science ®Google Scholar
• Daniel SCGK, Tharmaraj V, Sironman TA, Pitchumani K. Toxicity and immunological activity of silver nanoparticles. Appl Clay Sci. 2010;48(4):547–551.
   Google Scholar
• Kruszewski M, Brzoska K, Brunborg G, et al. Toxicity of silver nanomaterials in higher eukaryotes. Advan Mol Toxicol. 2011;5:179–218.
   Google Scholar
• Wijnhoven SWP, Peijnenburg WJGM, Herberts CA, et al. Nano-silver-a review of available data and knowledge gaps in human and environmental risk assessment. Nanotoxicology. 2009;3(2):109–138.
   Web of Science ®Google Scholar
• Lankoff A, Sandberg WJ, Wegierek-Ciuk A, et al. The effect of agglomeration state of silver and titanium dioxide nanoparticles on cellular response in HepG2, A549 and THP-1 cells. Toxicol Lett. 2012;208(3):197–213.
   PubMedGoogle Scholar
• Castellini C, Ruggeri S, Mattioli S, Bernardini G, Macchioni L, Moretti E. Long-term effects of silver nanoparticles on reproductive activity of rabbit buck. Syst Biol Reprod Med. 2014;60(3):143–150.
   PubMed Web of Science ®Google Scholar
• Van der Zande M, Vandebriel RJ, Doren EV, Kramer E, Rivera ZH, Serrano-Rojero CS. Distribution, elimination and toxicity of silver nanoparticles and silver ions in rats after 28-day oral exposure. ACS Nano. 2012;6(8):7427–7442.
   PubMed Web of Science ®Google Scholar
• Garcia TX, Costa GMJ, Franc LR, Hofmann MC. Sub-acute intravenous administration of silver nanoparticles in male mice alters Leydig cell function and testosterone levels. Reprod Toxicol. 2014;45:59–70.
   PubMed Web of Science ®Google Scholar
• Braydich-Stolle LK, Lucas B, Schrand A, et al. Silver-nanoparticles disrupt GDNF/Fyn kinase signaling in spermatogonial stem cells. Toxicol Sci. 2010;116(2):577–589.
   PubMed Web of Science ®Google Scholar
• Zhang T, Wang L, Chen Q, Chen C. Cytotoxic potential of silver nanoparticles. Yonsei Med J. 2014;55(2):283–291.
   PubMed Web of Science ®Google Scholar
• Zhang XF, Choi Y, Han JW, et al. Differential nanoreprotoxicity of silver nanoparticles in male somatic cells and spermatogonial stem cells. Int J Nanomed. 2015;10:1335–1357.
   PubMed Web of Science ®Google Scholar
• Tiedemann D, Taylor U, Rehbock C, et al. Reprotoxicity of gold, silver, and gold-silver alloy nanoparticles on mammalian gametes. Analyst. 2014;139(5):931–942.
   PubMedGoogle Scholar
• Gromadzka-Ostrowska J, Dziendzikowska K, Lankoff A, et al. Silver nanoparticles effects on epididymal sperm in rats. Toxicol Lett. 2012;214(3):251–258.
   PubMed Web of Science ®Google Scholar
• Miresmaeili SM, Halvaei I, Fesahat F, Fallah A, Nikonahad N, Taherinejad M. Evaluating the role of silver nanoparticles on acrosomal reaction and spermatogenic cells in rat. Iran J Reprod Med. 2013;11(5):423–430.
   PubMedGoogle Scholar
• Osmond MJ, Mccall MJ. Zinc oxide nanoparticles in modern sunscreens: an analysis of potential exposure and hazard. Nanotoxicology. 2010;4(1):15–41.
   PubMed Web of Science ®Google Scholar
• Jiang J, Pi J, Cai J. The advancing of Zinc Oxide nanoparticles for biomedical applications. Bioinorg Chem Appl. 2018. doi:10.1155/2018/1062562
   PubMedGoogle Scholar
• Roy B, Baghel RPS, Mohanty TK. Zinc and male reproduction in domestic animals: a review. Indian J Anim Nutr. 2013;30(4):339–350.
   Google Scholar
• Dani V, Dhawan DK. Radioprotective role of zinc following single-dose radioiodine (131I) exposure to red blood cells of rats. Indian J Med Res. 2005;122(4):338–342.
   PubMedGoogle Scholar
• Malekirad AA, Oryan S, Fani A, et al. Study on clinical and biochemical toxicity biomarkers in a zinc-lead mine workers. Toxicol Ind Health. 2010;26(6):331–337.
   PubMed Web of Science ®Google Scholar
• Raajshreer K, Durairaj B. Evaluation of the anti-tyrosinase and antioxidant potential of Zinc Oxide nanoparticles synthesized from the brown seaweed – turbinaria conoides. Int J Appl Pharm. 2017;9(5):116–120.
   Google Scholar
• Essa SS, El-Saied EM, El-Tawil OS, Gamal IM, Abd EL-Rahman SS. Nanoparticles of zinc oxide defeat chlorpyrifos-induced immunotoxic effects and histopathological alterations. Veterinary World. 2019;12(3):440–448.
   PubMedGoogle Scholar
• Lee PC, Meisel D. Adsorption and surface-enhanced raman of dyes on silver and gold sols. J Phys Chem. 1982;86:3391–3395.
   Web of Science ®Google Scholar
• Tejamaya M, Romer I, Merrifield RC, Lead JR. Stability of citrate, PVP, and PEG coated silver nanoparticles in ecotoxicology media. Environ Sci Technol. 2012;46(13):7011–7017.
   PubMed Web of Science ®Google Scholar
• Kim YS, Song SY, Park JD, et al. Subchronic oral toxicity of silver nanoparticles. Particle and Fibre Toxicol. 2010;7(1):20–32.
   PubMedGoogle Scholar
• Kim YR, Park JI, Lee EJ, et al. Toxicity of 100 nm zinc oxide nanoparticles: a report of 90-day repeated oral administration in Sprague Dawley rats. Int J Nanomedicine. 2014;9(2):109–126.
   PubMedGoogle Scholar
• Bearden HJ, Fuquay JW. Semen evaluation. In: Bearden HJ, Fuquay JW, editors. Applied Animal Reproduction. 4th ed. Upper Saddle River, NJ: Prentice Hall; 1997:158–169.
   Google Scholar
• Łącka K, Kondracki S, Iwanina M, Wysokińska A. Assessment of stallion semen morphology using two different staining methods, microscopic techniques, and sample sizes. J Vet Res. 2016;60:99–104.
   Google Scholar
• Kondracki S, Wysokińska A, Kania M, Górski K. Application of two staining methods for sperm morphometric evaluation in domestic pigs. J Vet Res. 2017;61:345–349.
   PubMed Web of Science ®Google Scholar
• Beutler E, Duron O, Kelly BM. Improved method for the determination of blood glutathione. J Lab Clin Med. 1963;61:882–888.
   PubMed Web of Science ®Google Scholar
• Fossati P, Prencipe L, Berti G. Use of 3, 5-dichloro-2-hydroxybenzene sulfonic acid/4-aminophenazone chromogenic system in direct enzyme assay of uric acid in serum and urine. Clin Chem. 1980;26(2):227–231.
   PubMed Web of Science ®Google Scholar
• Livingstone DR, Garcia-Martinez P, Michel X, et al. Oxyradial production as a pollution-mediated mechanics of toxicity in the common mussel, Mytilus edulis, and other mollusks. Funct Ecol. 1990;4:415–424.
   Web of Science ®Google Scholar
• Demetrious JA. Testosterone. In: Pesce AJ, Kapalan LA, editors. Methods in Clinical Chemistry. St Louis, MO, USA: Mosby; 1987:268.
   Google Scholar
• Beastall GH. Immunoassay in the clinical chemistry laboratory. Lab Pract. 1985;34:74–81.
   Google Scholar
• Tice RR, Agurell E, Anderson D, et al. Single cell gel/Comet assay: guidelines for in vitro and in vivo genetic toxicology testing. Environ Mol Mutagen. 2000;35(3):206–221.
   PubMed Web of Science ®Google Scholar
• Bancroft JD, Gamble M. Theory and Practice of Histological Techniques. 6th ed. Churchill Livingstone: Elsevier; 2008.
   Google Scholar
• Baki ME, Miresmaili SM, Pourentezari M, Amraii E, Yousefi V, Spenani HR. Effects of silver nano-particles on sperm parameters, number of Leydig cells, and sex hormones in rats. Iran J Reprod Med. 2014;12(2):139–144.
   PubMedGoogle Scholar
• Mathias FT, Romano RM, Kizys MM, Kasamatsu T, Giannòcco G, Chiamola MI. Daily exposure to silver nanoparticles during prepubertal development decreases adult sperm and reproductive parameters. Nanotoxicology. 2015;9(1):64–70.
   PubMed Web of Science ®Google Scholar
• Lafuente D, Garcia T, Blance J, Sánchez DJ, Sirvent JJ, Domingo JL. Effects of oral exposure to silver nanoparticles on the sperm of rats. Reprod Toxicol. 2016;60:133–139.
   PubMed Web of Science ®Google Scholar
• Fathi N, Hoseinipanah SM, Alizadeh Z, et al. The effect of silver nanoparticles on the reproductive system of adult male rats: a morphological, histological and DNA integrity study. Advan Clin Exp Med. 2019;28(3):299–305.
   PubMed Web of Science ®Google Scholar
• Carlson C, Hussain SM, Schrand AM, Braydich-Stolle LK, Hess KL, Jones RL. Unique cellular interaction of silver nanoparticles: size-dependent generation of reactive oxygen species. J Phys Chem B. 2008;112(43):13608–136019.
   PubMed Web of Science ®Google Scholar
• Sleiman HK, Romano RM, Oliveira CA, Romano MA. Effects of prepubertal exposure to silver nanoparticles on reproductive parameters in adult male Wistar rats. J Toxicol Environ Health A. 2013;76:1023–1032.
   PubMed Web of Science ®Google Scholar
• Birben E, Sahiner UM, Sackesen C, Erzurum S, Kalayci O. Oxidative stress and antioxidant defense. World Allergy Organ J. 2012;5(1):9–19.
   PubMedGoogle Scholar
• Kirkman HN, Rolfo M, Ferraris AM, Gaetani GF. Mechanisms of protection of catalase by NADPH. Kinetics and stoichiometry. J Biol Chem. 1999;274(20):13908–13914.
   PubMedGoogle Scholar
• Pena-Llopis S, Ferrando MD, Pena JB. Fish tolerance to organophosphate-induced oxidative stress is dependent on the glutathione metabolism and enhanced by N-acetylcysteine. Aquat Toxicol. 2003;65(4):337–360.
   PubMed Web of Science ®Google Scholar
• Zhang J, Shen H, Wang X, Wu J, Xue Y. Effects of chronic exposure of 2,4-dichlorophenol on the antioxidant system in liver of freshwater fish Carassius auratus. Chemosphere. 2004;55(2):167–174.
   PubMed Web of Science ®Google Scholar
• Liu Y, Wang JS, Wei Y, Zhang H, Xu M, Dai J. Induction of time-dependent oxidative stress and related transcriptional effects of perfluorododecanoic acid in zebrafish liver. Aquat Toxicol. 2008;89(4):242–250.
   PubMedGoogle Scholar
• Pandey S, Parvez S, Ansari RA, et al. Effects of exposure to multiple trace metals on biochemical, histological and ultrastructural features of gills of a freshwater fish, Channa punctata Bloch. Chem Biol Interact. 2008;174(3):183–192.
   PubMed Web of Science ®Google Scholar
• Nel A, Xia T, Mädler L, Li N. Toxic potential of materials at the nanolevel. Science. 2006;311(5761):622–627.
   PubMed Web of Science ®Google Scholar
• Bressan E, Vindigni V, Ferroni L, et al. Silver nanoparticles and mitochondrial interaction. Int J Dentistry. 2013. doi:10.1155/2013/312747
   PubMedGoogle Scholar
• Yoshida Y, Itoh N, Saito Y, Hayakawa M, Niki E. Application of water-soluble radical initiator, 2, 2- azobis [2-(2-imidazolin- 2- yi) propane] dihydrochloride, to a study of oxidative stress. Free Radic Res. 2004;38(4):375–384.
   PubMed Web of Science ®Google Scholar
• Manin OI, Nikolaev VA, Kolomiitsev AA, Lebedenko I. Comparative toxicological evaluation of domestic golden alloys for soldering. Stoma Tologiia. 2007;86(1):64–67.
   Google Scholar
• Girotti AW. Mechanisms of lipid peroxidation. J Free Radic Biol Med. 1985;1(2):87–95.
   PubMedGoogle Scholar
• Arisha AM, Ahmed MM, Kamel MA, Attia YA, Hussein MMA. Morin ameliorates the testicular apoptosis, oxidative stress, and impact on blood-testis barrier induced by photo-extracellularly synthesized silver nanoparticles. Environ Sci Pollution Res. 2019;26(28):28749–28762.
   PubMed Web of Science ®Google Scholar
• Elsharkawy EE, Abd El-Nasser M, Kamaly HF. Silver nanoparticles testicular toxicity in rat. Environ Toxicol Pharmacol. 2019;70:103194.
   PubMedGoogle Scholar
• Egwurugwu JN, Ifedi CU, Uchefuna RC, Ezeokafor EN, Alagwu EA. Effects of zinc on male sex hormones and semen quality in rats. Niger J Physiol Sci. 2013;28(1):17–22.
   PubMedGoogle Scholar
• Faccio L, Da Silva AS, Tonin AA, et al. Serum levels of LH, FSH, estradiol and progesterone in female rats experimentally infected by Trypanosoma evansi. Exp Parasitol. 2013;135(1):110–115.
   PubMed Web of Science ®Google Scholar
• Rezaei-Zarchi S, Taghavi-Foumani H, Negahdary M. Effect of silver nanoparticles on the LH, FSH and testosterone hormones in male rat. J Babol Univ Med Sci. 2013;15(1):25–29.
   Google Scholar
• Trickler WJ, Burks S, Murdock RC, et al. Silver nanoparticle-induced Blood-Brain Barrier inflammation and increased permeability in primary rat brain micro-vessel endothelial cells. Toxicol Sci. 2010;118(1):160–170.
   PubMed Web of Science ®Google Scholar
• Liao W, McNutt MA, Zhu W. The comet assay: a sensitive method for detecting DNA damage in individual cells. Methods (San Diego, Calif). 2009;48(1):46–53.
   PubMed Web of Science ®Google Scholar
• AshaRani PV, Mun GK, Hande MP, Valiyaveettil S. Cytotoxicity and genotoxicity of silver nanoparticles in human cells. ACS Nano. 2009;3(2):279–290.
   PubMed Web of Science ®Google Scholar
• Singh R, Lillard JW. Nanoparticle-based targeted drug delivery. Exp Mol Pathol. 2009;86(3):215–223.
   PubMed Web of Science ®Google Scholar
• Yoshida S, Hiyoshi K, Ichinose T, et al. Effect of nanoparticles on the male reproductive system of mice. Int J Androl. 2009;32(4):337–342.
   PubMedGoogle Scholar
• Thakur M, Gupta H, Singh D, Mohanty I, Maheswari U, Vanage G. Histopathological and ultrastructural effects of nanoparticles on rat testis following 90 days (chronic study) of repeated oral administration. J Nanobiotechnol. 2014;12:42.
   PubMedGoogle Scholar
• El-Maddawy ZK, Abd El Naby WSH. Protective effects of zinc oxide nanoparticles against doxorubicin-induced testicular toxicity and DNA damage in male rats. Toxicol Res (Camb). 2019;8(5):654–662.
   PubMedGoogle Scholar
• Mohamed DA, Abdelrahman SA. The possible protective role of zinc oxide nanoparticles (ZnO-NPs) on testicular and epididymal structure and sperm parameters in nicotine-treated adult rats (a histological and biochemical study). Cell Tissue Res. 2018. doi:10.1007/s00441-018-2909-8
   PubMedGoogle Scholar
• Fathi M, Haydari M, Tanha T. Effects of zinc oxide nanoparticles on antioxidant status, serum enzymes activities, biochemical parameters and performance in broiler chickens. J Livestock Sci Technol. 2016;4(2):7–13.
   Google Scholar