5,156
Views
24
CrossRef citations to date
0
Altmetric
Review Articles

Toxicity mechanisms of nanoparticles in the male reproductive system

, ORCID Icon, ORCID Icon, &
Pages 604-617 | Received 16 Jan 2021, Accepted 09 Apr 2021, Published online: 14 May 2021

References

  • Adebayo O, Akinloye O, Adaramoye O. 2018. Cerium oxide nanoparticle elicits oxidative stress, endocrine imbalance and lowers sperm characteristics in testes of Balb/c mice. Andrologia. 50(3):e12920.
  • Adler S, Basketter D, Creton S, Pelkonen O, van Benthem J, Zuang V, Andersen KE, Angers-Loustau A, Aptula A, Bal-Price A, et al. 2011. Alternative (non-animal) methods for cosmetics testing: current status and future prospects-2010. Arch Toxicol. 85(5):367–485.
  • Anway MD, Skinner MK. 2008. Epigenetic programming of the germ line: effects of endocrine disruptors on the development of transgenerational disease. Reprod Biomed Online. 16(1):23–25.
  • Bahadar H, Maqbool F, Niaz K, Abdollahi M. 2016. Toxicity of nanoparticles and an overview of current experimental models. Iran Biomed J. 20(1):1.
  • Bai Y, Zhang Y, Zhang J, Mu Q, Zhang W, Butch ER, Snyder SE, Yan B. 2010. Repeated administrations of carbon nanotubes in male mice cause reversible testis damage without affecting fertility. Nat Nanotechnol. 5(9):683–689.
  • Baki ME, Miresmaili SM, Pourentezari M, Amraii E, Yousefi V, Spenani HR, Talebi AR, Anvari M, Fazilati M, Fallah AA. 2014. Effects of silver nano-particles on sperm parameters, number of Leydig cells and sex hormones in rats. Iran J Reprod Med. 12(2):139.
  • Ban Z, Zhou Q, Sun A, Mu L, Hu X. 2018. Screening priority factors determining and predicting the reproductive toxicity of various nanoparticles. Environ Sci Technol. 52(17):9666–9676.
  • Barkalina N, Charalambous C, Jones C, Coward K. 2014. Nanotechnology in reproductive medicine: emerging applications of nanomaterials. Nanomedicine. 10(5):921–938.
  • Ben-David Makhluf S, Qasem R, Rubinstein S, Gedanken A, Breitbart H. 2006. Loading magnetic nanoparticles into sperm cells does not affect their functionality. Langmuir. 22(23):9480–9482.
  • Boisen AMZ, Shipley T, Jackson P, Hougaard KS, Wallin H, Yauk CL, Vogel U. 2012. NanoTiO2 (UV-Titan) does not induce ESTR mutations in the germline of prenatally exposed female mice. Part Fibre Toxicol. 9(1):19.
  • Braydich-Stolle L, Hussain S, Schlager JJ, Hofmann M-C. 2005. In vitro cytotoxicity of nanoparticles in mammalian germline stem cells. Toxicol Sci. 88(2):412–419.
  • Braydich-Stolle LK, Lucas B, Schrand A, Murdock RC, Lee T, Schlager JJ, Hussain SM, Hofmann M-C. 2010. Silver nanoparticles disrupt GDNF/Fyn kinase signaling in spermatogonial stem cells. Toxicol Sci. 116(2):577–589.
  • Brohi RD, Wang L, Talpur HS, Wu D, Khan FA, Bhattarai D, Rehman ZU, Farmanullah F, Huo LJ. 2017. Toxicity of nanoparticles on the reproductive system in animal models: a review. Front Pharmacol. 8:606.
  • Campos VF, de Leon PM, Komninou ER, Dellagostin OA, Deschamps JC, Seixas FK, Collares T. 2011. NanoSMGT: transgene transmission into bovine embryos using halloysite clay nanotubes or nanopolymer to improve transfection efficiency. Theriogenology. 76(8):1552–1560.
  • Carriere M, Sauvaigo S, Douki T, Ravanat J-L. 2017. Impact of nanoparticles on DNA repair processes: current knowledge and working hypotheses. Mutagenesis. 32(1):203–213.
  • Castillo J, Simon L, de Mateo S, Lewis S, Oliva R. 2011. Protamine/DNA ratios and DNA damage in native and density gradient centrifuged sperm from infertile patients. J Androl. 32(3):324–332.
  • Chen Y, Xue Z, Zheng D, Xia K, Zhao Y, Liu T, Long Z, Xia J. 2003. Sodium chloride modified silica nanoparticles as a non-viral vector with a high efficiency of DNA transfer into cells. Curr Gene Ther. 3(3):273–279.
  • Chen L, Zheng L, Lv Y, Liu H, Wang G, Ren N, Liu D, Wang J, Boughton RI. 2010. Chemical assembly of silver nanoparticles on stainless steel for antimicrobial applications. Surf Coat Technol. 204(23):3871–3875.
  • Chou C-C, Hsiao H-Y, Hong Q-S, Chen C-H, Peng Y-W, Chen H-W, Yang P-C. 2008. Single-walled carbon nanotubes can induce pulmonary injury in mouse model. Nano Lett. 8(2):437–445.
  • Dagar G, Bagchi G. 2020. Nanoparticles as potential endocrine disruptive chemicals. In: NanoBioMedicine. Singapore: Springer; p. 411–429.
  • Del Vento F, Vermeulen M, Ucakar B, Poels J, Des Rieux A, Wyns C. 2019. Significant benefits of nanoparticles containing a necrosis inhibitor on mice testicular tissue autografts outcomes. Int J Mol Sci. 20(23):5833.
  • Dziendzikowska K, Krawczyńska A, Oczkowski M, Królikowski T, Brzóska K, Lankoff A, Dziendzikowski M, Stępkowski T, Kruszewski M, Gromadzka-Ostrowska J. 2016. Progressive effects of silver nanoparticles on hormonal regulation of reproduction in male rats. Toxicol Appl Pharmacol. 313:35–46.
  • Erdely A, Liston A, Salmen-Muniz R, Hulderman T, Young S-H, Zeidler-Erdely PC, Castranova V, Simeonova PP. 2011. Identification of systemic markers from a pulmonary carbon nanotube exposure. J Occup Environ Med. 53(6 Suppl.):S80–S86.
  • Gao G, Ze Y, Zhao X, Sang X, Zheng L, Ze X, Gui S, Sheng L, Sun Q, Hong J, et al. 2013. Titanium dioxide nanoparticle-induced testicular damage, spermatogenesis suppression, and gene expression alterations in male mice. J Hazard Mater. 258–259:133–143.
  • Golobič M, Jemec A, Drobne D, Romih T, Kasemets K, Kahru A. 2012. Upon exposure to Cu nanoparticles, accumulation of copper in the isopod Porcellio scaber is due to the dissolved Cu ions inside the digestive tract. Environ Sci Technol. 46(21):12112–12119.
  • Gopalan RC, Osman IF, Amani A, De Matas M, Anderson D. 2009. The effect of zinc oxide and titanium dioxide nanoparticles in the Comet assay with UVA photoactivation of human sperm and lymphocytes. Nanotoxicology. 3(1):33–39.
  • Gromadzka-Ostrowska J, Dziendzikowska K, Lankoff A, Dobrzyńska M, Instanes C, Brunborg G, Gajowik A, Radzikowska J, Wojewódzka M, Kruszewski M. 2012. Silver nanoparticles effects on epididymal sperm in rats. Toxicol Lett. 214(3):251–258.
  • Habas K, Brinkworth MH, Anderson D. 2018. Silver nanoparticle-mediated cellular responses in isolated primary Sertoli cells in vitro. Food Chem Toxicol. 116(Pt B):182–188.
  • Habas K, Brinkworth MH, Anderson D. 2020. A male germ cell assay and supporting somatic cells: its application for the detection of phase specificity of genotoxins in vitro. J Toxicol Environ Health B Crit Rev. 23(3):91–106.
  • Han JW, Jeong J-K, Gurunathan S, Choi Y-J, Das J, Kwon D-N, Cho S-G, Park C, Seo HG, Park J-K, et al. 2016. Male- and female-derived somatic and germ cell-specific toxicity of silver nanoparticles in mouse. Nanotoxicology. 10(3):361–373.
  • Han Z, Yan Q, Ge W, Liu Z-G, Gurunathan S, De Felici M, Shen W, Zhang X-F. 2016. Cytotoxic effects of ZnO nanoparticles on mouse testicular cells. Int J Nanomedicine. 11:5187–5203.
  • Hansson GC. 2012. Role of mucus layers in gut infection and inflammation. Curr Opin Microbiol. 15(1):57–62.
  • Hong F, Li W, Ji J, Ze X, Diao E. 2020. Nanostructured titanium dioxide (TiO(2)) reduces sperm concentration involving disorder of meiosis and signal pathway. J Biomed Nanotechnol. 16(5):659–671.
  • Hong F, Wang Y, Zhou Y, Zhang Q, Ge Y, Chen M, Hong J, Wang L. 2016. Exposure to TiO2 nanoparticles induces immunological dysfunction in mouse testitis. J Agric Food Chem. 64(1):346–355.
  • Hong F, Zhao X, Si W, Ze Y, Wang L, Zhou Y, Hong J, Yu X, Sheng L, Liu D, et al. 2015. Decreased spermatogenesis led to alterations of testis-specific gene expression in male mice following nano-TiO2 exposure. J Hazard Mater. 300:718–728.
  • Hozyen HF, Khalil HMA, Ghandour RA, Al-Mokaddem AK, Amer MS, Azouz RA. 2020. Nano selenium protects against deltamethrin-induced reproductive toxicity in male rats. Toxicol Appl Pharmacol. 408:115274.
  • Huang C, Li B, Xu K, Liu D, Hu J, Yang Y, Nie H, Fan L, Zhu W. 2017. Decline in semen quality among 30,636 young Chinese men from 2001 to 2015. Fertil Steril. 107(1):83–88.e2.
  • Hussein MM, Ali HA, Saadeldin IM, Ahmed MM. 2016. Querectin alleviates zinc oxide nanoreprotoxicity in male albino rats. J Biochem Mol Toxicol. 30(10):489–496.
  • Iavicoli I, Fontana L, Leso V, Bergamaschi A. 2013. The effects of nanomaterials as endocrine disruptors. Int J Mol Sci. 14(8):16732–16801.
  • Iona S, Klinger F, Sisti R, Ciccalese R, Nunziata A, De Felici M. 2002. A comparative study of cytotoxic effects of N-ethyl-N-nitrosourea, adriamycin, and mono-2-ethylhexyl) phthalate on mouse primordial germ cells. Cell Biol Toxicol. 18(2):131–145.
  • Karimi S, Khorsandi L, Nejaddehbashi F. 2019. Protective effects of curcumin on testicular toxicity induced by titanium dioxide nanoparticles in mice. JBRA Assist Reprod. 23(4):344–351.
  • Kashiwada S. 2006. Distribution of nanoparticles in the see-through medaka (Oryzias latipes). Environ Health Perspect. 114(11):1697–1702.
  • Khan I, Saeed K, Khan I. 2019. Nanoparticles: properties, applications and toxicities. Arab J Chem. 12(7):908–931.
  • Khanna P, Ong C, Bay BH, Baeg GH. 2015. Nanotoxicity: an interplay of oxidative stress, inflammation and cell death. Nanomaterials (Basel). 5(3):1163–1180.
  • Kim D, Jeong YY, Jon S. 2010. A drug-loaded aptamer-gold nanoparticle bioconjugate for combined CT imaging and therapy of prostate cancer. ACS Nano. 4(7):3689–3696.
  • Kim JS, Yoon T-J, Yu KN, Kim BG, Park SJ, Kim HW, Lee KH, Park SB, Lee J-K, Cho MH. 2006. Toxicity and tissue distribution of magnetic nanoparticles in mice. Toxicol Sci. 89(1):338–347.
  • Knez J. 2013. Endocrine-disrupting chemicals and male reproductive health. Reprod Biomed Online. 26(5):440–448.
  • Koga K, Izumi G, Mor G, Fujii T, Osuga Y. 2014. Toll-like receptors at the maternal-fetal interface in normal pregnancy and pregnancy complications. Am J Reprod Immunol. 72(2):192–205.
  • Kong L, Gao X, Zhu J, Cheng K, Tang M. 2016. Mechanisms involved in reproductive toxicity caused by nickel nanoparticle in female rats. Environ Toxicol. 31(11):1674–1683.
  • Kong L, Hu W, Gao X, Wu Y, Xue Y, Cheng K, Tang M. 2019. Molecular mechanisms underlying nickel nanoparticle induced rat Sertoli-germ cells apoptosis. Sci Total Environ. 692:240–248.
  • Lan Z, Yang W-X. 2012. Nanoparticles and spermatogenesis: how do nanoparticles affect spermatogenesis and penetrate the blood–testis barrier. Nanomedicine (Lond). 7(4):579–596.
  • Leclerc L, Klein J-P, Forest V, Boudard D, Martini M, Pourchez J, Blanchin M-G, Cottier M. 2015. Testicular biodistribution of silica-gold nanoparticles after intramuscular injection in mice. Biomed Microdev. 17(4):66.
  • Lee J-H, Huh Y-M, Jun Y-w, Seo J-w, Jang J-t, Song H-T, Kim S, Cho E-J, Yoon H-G, Suh J-S, et al. 2007. Artificially engineered magnetic nanoparticles for ultra-sensitive molecular imaging. Nat Med. 13(1):95–99.
  • Lewinski N, Colvin V, Drezek R. 2008. Cytotoxicity of nanoparticles. Small. 4(1):26–49.
  • Li P-W, Kuo T-H, Chang J-H, Yeh J-M, Chan W-H. 2010. Induction of cytotoxicity and apoptosis in mouse blastocysts by silver nanoparticles. Toxicol Lett. 197(2):82–87.
  • Li X, Yang X, Yuwen L, Yang W, Weng L, Teng Z, Wang L. 2016. Evaluation of toxic effects of CdTe quantum dots on the reproductive system in adult male mice. Biomaterials. 96:24–32.
  • Lipskind ST, Gargiulo AR. 2013. Computer-assisted laparoscopy in fertility preservation and reproductive surgery. J Minim Invasive Gynecol. 20(4):435–445.
  • Liu Y, Li X, Xiao S, Liu X, Chen X, Xia Q, Lei S, Li H, Zhong Z, Xiao K. 2020. The effects of gold nanoparticles on Leydig cells and male reproductive function in mice. Int J Nanomedicine. 15:9499–9514.
  • Liu Q, Xu C, Ji G, Liu H, Mo Y, Tollerud DJ, Gu A, Zhang Q. 2016. Sublethal effects of zinc oxide nanoparticles on male reproductive cells. Toxicol In Vitro. 35:131–138.
  • Lopes IMD, de Oliveira IM, Bargi-Souza P, Cavallin MD, Kolc CSM, Khalil NM, Quináia SP, Romano MA, Romano RM. 2019. Effects of silver nanoparticle exposure to the testicular antioxidant system during the prepubertal rat stage. Chem Res Toxicol. 32(6):986–994.
  • Mahfouz R, Sharma R, Thiyagarajan A, Kale V, Gupta S, Sabanegh E, Agarwal A. 2010. Semen characteristics and sperm DNA fragmentation in infertile men with low and high levels of seminal reactive oxygen species. Fertil Steril. 94(6):2141–2146.
  • Manin O, Nikolaev V, Kolomiĭtsev A, Lebedenko I. 2007. Comparative toxicological evaluation of domestic golden alloys for soldering. Stomatologiia (Mosk). 86(1):64–67.
  • Manke A, Wang L, Rojanasakul Y. 2013. Mechanisms of nanoparticle-induced oxidative stress and toxicity. Biomed Res Int. 2013:942916.
  • Massarsky A, Trudeau VL, Moon TW. 2014. Predicting the environmental impact of nanosilver. Environ Toxicol Pharmacol. 38(3):861–873.
  • Mathias FT, Romano RM, Kizys MM, Kasamatsu T, Giannocco G, Chiamolera MI, Dias-da-Silva MR, Romano MA. 2015. Daily exposure to silver nanoparticles during prepubertal development decreases adult sperm and reproductive parameters. Nanotoxicology. 9(1):64–70.
  • Miresmaeili SM, Halvaei I, Fesahat F, Fallah A, Nikonahad N, Taherinejad M. 2013. Evaluating the role of silver nanoparticles on acrosomal reaction and spermatogenic cells in rat. Iran J Reprod Med. 11(5):423–430.
  • Mohammad I. 2019. Gold nanoparticle: an efficient carrier for MCP I of Carica papaya seeds extract as an innovative male contraceptive in albino rats. J Drug Delivery Sci Technol. 52:942–956.
  • Morgan AM, Ibrahim MA, Noshy PA. 2017. Reproductive toxicity provoked by titanium dioxide nanoparticles and the ameliorative role of Tiron in adult male rats. Biochem Biophys Res Commun. 486(2):595–600.
  • Morishita Y, Yoshioka Y, Satoh H, Nojiri N, Nagano K, Abe Y, Kamada H, Tsunoda S-i, Nabeshi H, Yoshikawa T, et al. 2012. Distribution and histologic effects of intravenously administered amorphous nanosilica particles in the testes of mice. Biochem Biophys Res Commun. 420(2):297–301.
  • Negahdary M, Arefian Z, Dastjerdi HA, Ajdary M. 2015. Toxic effects of Mn2O3 nanoparticles on rat testis and sex hormone. J Nat Sci Biol Med. 6(2):335–339.
  • Nirmal NK, Awasthi KK, John PJ. 2017. Effects of nano-graphene oxide on testis, epididymis and fertility of wistar rats. Basic Clin Pharmacol Toxicol. 121(3):202–210.
  • Niska K, Zielinska E, Radomski MW, Inkielewicz-Stepniak I. 2018. Metal nanoparticles in dermatology and cosmetology: interactions with human skin cells. Chem Biol Interact. 295:38–51.
  • Olugbodi JO, David O, Oketa EN, Lawal B, Okoli BJ, Mtunzi F. 2020. Silver nanoparticles stimulates spermatogenesis impairments and hematological alterations in testis and epididymis of male rats. Molecules. 25(5):1063.
  • Ong C, Lee QY, Cai Y, Liu X, Ding J, Yung L-YL, Bay B-H, Baeg G-H. 2016. Silver nanoparticles disrupt germline stem cell maintenance in the Drosophila testis. Sci Rep. 6:20632.
  • Orazizadeh M, Daneshi E, Hashemitmar M, Absalan F, Khorsandi L. 2015. Protective effect of beta‐carotene against titanium dioxide nanoparticles induced apoptosis in mouse testicular tissue. Andrologia. 47(7):816–825.
  • Pawar K, Kaul G. 2014. Toxicity of titanium oxide nanoparticles causes functionality and DNA damage in buffalo (Bubalus bubalis) sperm in vitro. Toxicol Ind Health. 30(6):520–533.
  • Pérez-Labrada F, López-Vargas ER, Ortega-Ortiz H, Cadenas-Pliego G, Benavides-Mendoza A, Juárez-Maldonado A. 2019. Responses of tomato plants under saline stress to foliar application of copper nanoparticles. Plants. 8(6):151.
  • Pinho AR, Martins F, Costa MEV, Senos AM, Silva OA, Pereira ML, Rebelo S. 2020. In vitro cytotoxicity effects of zinc oxide nanoparticles on spermatogonia cells. Cells. 9(5):1081.
  • Pinho AR, Rebelo S, Pereira ML. 2020. The impact of zinc oxide nanoparticles on male (In) fertility. Materials. 13(4):849.
  • Rafiee Z, Khorsandi L, Nejad-Dehbashi F. 2019. Protective effect of zingerone against mouse testicular damage induced by zinc oxide nanoparticles. Environ Sci Pollut Res Int. 26(25):25814–25824.
  • Ritz C, Ruminski W, Hougaard KS, Wallin H, Vogel U, Yauk CL. 2011. Germline mutation rates in mice following in utero exposure to diesel exhaust particles by maternal inhalation. Mutat Res. 712(1–2):55–58.
  • Santonastaso M, Mottola F, Colacurci N, Iovine C, Pacifico S, Cammarota M, Cesaroni F, Rocco L. 2019. In vitro genotoxic effects of titanium dioxide nanoparticles (n‐TiO2) in human sperm cells. Mol Reprod Dev. 86(10):1369–1377.
  • Shalviri A, Cai P, Rauth AM, Henderson JT, Wu XY. 2012. Evaluation of new bi-functional terpolymeric nanoparticles for simultaneous in vivo optical imaging and chemotherapy of breast cancer. Drug Deliv Transl Res. 2(6):437–453.
  • Shen J, Yang D, Zhou X, Wang Y, Tang S, Yin H, Wang J, Chen R, Chen J. 2019. Role of autophagy in zinc oxide nanoparticles-induced apoptosis of mouse LEYDIG cells. Int J Mol Sci. 20(16):4042.
  • Sleiman HK, Romano RM, Oliveira CA, Romano MA. 2013. Effects of prepubertal exposure to silver nanoparticles on reproductive parameters in adult male Wistar rats. J Toxicol Environ Health A. 76(17):1023–1032.
  • Solier S, Pommier Y. 2014. The nuclear γ-H2AX apoptotic ring: implications for cancers and autoimmune diseases. Cell Mol Life Sci. 71(12):2289–2297.
  • Takeda K, Suzuki K-i, Ishihara A, Kubo-Irie M, Fujimoto R, Tabata M, Oshio S, Nihei Y, Ihara T, Sugamata M. 2009. Nanoparticles transferred from pregnant mice to their offspring can damage the genital and cranial nerve systems. J Health Sci. 55(1):95–102.
  • Tang Y, Chen B, Hong W, Chen L, Yao L, Zhao Y, Aguilar ZP, Xu H. 2019. ZnO nanoparticles induced male reproductive toxicity based on the effects on the endoplasmic reticulum stress signaling pathway. Int J Nanomedicine. 14:9563–9576.
  • Taylor U, Barchanski A, Garrels W, Klein S, Kues W, Barcikowski S, Rath D. 2012. Toxicity of gold nanoparticles on somatic and reproductive cells. Adv Exp Med Biol. 733:125–133.
  • Karpenko NA, Malukin YV, Koreneva EM, Klochkov VK, Kavok NS, Smolenko NP, Pochernyaeva SS. 2013. The effects of chronic intake of nanoparticles of cerium dioxide or gadolinium ortovanadate into aging male rats. Proceedings of the International Conference Nanomaterials: Applications and Properties; Sumy State University Publishing.
  • Tremellen K. 2008. Oxidative stress and male infertility—a clinical perspective. Hum Reprod Update. 14(3):243–258.
  • Wang E, Huang Y, Du Q, Sun Y. 2021. Alterations in reproductive parameters and gene expression in Balb/c mice testes after exposure to silver nanoparticles. Andrologia. 53(1):e13841.
  • Wang R, Song B, Wu J, Zhang Y, Chen A, Shao L. 2018. Potential adverse effects of nanoparticles on the reproductive system. Int J Nanomedicine. 13:8487–8506.
  • Wang AZ, Bagalkot V, Vasilliou CC, Gu F, Alexis F, Zhang L, Shaikh M, Yuet K, Cima MJ, Langer R, et al. 2008. Superparamagnetic iron oxide nanoparticle–aptamer bioconjugates for combined prostate cancer imaging and therapy. ChemMedChem. 3(9):1311–1315.
  • Wells PG, Bhuller Y, Chen CS, Jeng W, Kasapinovic S, Kennedy JC, Kim PM, Laposa RR, McCallum GP, Nicol CJ, et al. 2005. Molecular and biochemical mechanisms in teratogenesis involving reactive oxygen species. Toxicol Appl Pharmacol. 207(2 Suppl.):354–366.
  • Wiwanitkit V, Sereemaspun A, Rojanathanes R. 2009. Effect of gold nanoparticles on spermatozoa: the first world report. Fertil Steril. 91(1):e7–e8.
  • Xia X, Wang L, Yang X, Hu Y, Liu Q. 2020. Acute damage to the sperm quality and spermatogenesis in male mice exposed to curcumin-loaded nanoparticles. Int J Nanomedicine. 15:1853–1862.
  • Xu Y, Wang N, Yu Y, Li Y, Li YB, Yu YB, Zhou XQ, Sun ZW. 2014. Exposure to silica nanoparticles causes reversible damage of the spermatogenic process in mice. PLoS One. 9(7):e101572.
  • Yan S-Q, Xing R, Zhou Y-F, Li K-L, Su Y-Y, Qiu J-F, Zhang Y-H, Zhang K-Q, He Y, Lu X-P, et al. 2016. Reproductive toxicity and gender differences induced by cadmium telluride quantum dots in an invertebrate model organism. Sci Rep. 6(1):34182.
  • Yauk C, Polyzos A, Rowan-Carroll A, Somers CM, Godschalk RW, Van Schooten FJ, Berndt ML, Pogribny IP, Koturbash I, Williams A, et al. 2008. Germ-line mutations, DNA damage, and global hypermethylation in mice exposed to particulate air pollution in an urban/industrial location. Proc Natl Acad Sci U S A. 105(2):605–610.
  • Yoshida S, Hiyoshi K, Ichinose T, Takano H, Oshio S, Sugawara I, Takeda K, Shibamoto T. 2009. Effect of nanoparticles on the male reproductive system of mice. Int J Androl. 32(4):337–342.
  • Yoshida S, Hiyoshi K, Oshio S, Takano H, Takeda K, Ichinose T. 2010. Effects of fetal exposure to carbon nanoparticles on reproductive function in male offspring. Fertil Steril. 93(5):1695–1699.
  • Zhang XF, Gurunathan S, Kim JH. 2015. Effects of silver nanoparticles on neonatal testis development in mice. Int J Nanomedicine. 10:6243–6256.
  • Zhang X, Yue Z, Zhang H, Liu L, Zhou X. 2020. Repeated administrations of Mn3O4 nanoparticles cause testis damage and fertility decrease through PPAR-signaling pathway. Nanotoxicology. 14(3):326–340.
  • Zhang D, Zhang Z, Wu Y, Fu K, Chen Y, Li W, Chu M. 2019. Systematic evaluation of graphene quantum dot toxicity to male mouse sexual behaviors, reproductive and offspring health. Biomaterials. 194:215–232.
  • Zhao H, Gu W, Ye L, Yang H. 2014. Biodistribution of PAMAM dendrimer conjugated magnetic nanoparticles in mice. J Mater Sci Mater Med. 25(3):769–776.
  • Zhao X, Sheng L, Wang L, Hong J, Yu X, Sang X, Sun Q, Ze Y, Hong F. 2014. RETRACTED ARTICLE: mechanisms of nanosized titanium dioxide-induced testicular oxidative stress and apoptosis in male mice. Part Fibre Toxicol. 11(1):47.