274
Views
38
CrossRef citations to date
0
Altmetric
Original Research

ZnO Nanoparticles Induced Male Reproductive Toxicity Based on the Effects on the Endoplasmic Reticulum Stress Signaling Pathway

, , , , , , & ORCID Icon show all
Pages 9563-9576 | Published online: 04 Dec 2019

References

  • Peters RJ, Bouwmeester H, Gottardo S, et al. Nanomaterials for products and application in agriculture, feed and food. TrendsFood Sci Tech. 2016;54:155–164.
  • Díez-Pascual AM, Díez-Vicente AL. ZnO-reinforced poly (3-hydroxybutyrate-co-3-hydroxyvalerate) bionanocomposites with antimicrobial function for food packaging. ACS Appl Mater Interfaces. 2014;6(12):9822–9834. doi:10.1021/am502261e24846876
  • Shi L-E, Li Z-H, Zheng W, Zhao Y-F, Jin Y-F, Tang Z-X. Synthesis, antibacterial activity, antibacterial mechanism and food applications of ZnO nanoparticles: a review. Food Addit Contam Part A. 2014;31(2):173–186. doi:10.1080/19440049.2013.865147
  • Liu R, Lal R. Potentials of engineered nanoparticles as fertilizers for increasing agronomic productions. Sci Total Environ. 2015;514:131–139. doi:10.1016/j.scitotenv.2015.01.10425659311
  • Liu Y, Nie Y, Wang J, et al. Mechanisms involved in the impact of engineered nanomaterials on the joint toxicity with environmental pollutants. Ecotoxicol Environ Saf. 2018;162:92–102. doi:10.1016/j.ecoenv.2018.06.07929990744
  • Wang C, Lu J, Zhou L, et al. Effects of long-term exposure to zinc oxide nanoparticles on development, zinc metabolism and biodistribution of minerals (Zn, Fe, Cu, Mn) in mice. PLoS One. 2016;11(10):e0164434. doi:10.1371/journal.pone.016443427732669
  • Gilbert B, Fakra SC, Xia T, Pokhrel S, Mädler L, Nel AE. The fate of ZnO nanoparticles administered to human bronchial epithelial cells. ACS Nano. 2012;6(6):4921–4930. doi:10.1021/nn300425a22646753
  • Han Z, Yan Q, Ge W, et al. Cytotoxic effects of ZnO nanoparticles on mouse testicular cells. Int J Nanomedicine. 2016;11:5187. doi:10.2147/IJN.S11144727785022
  • Chen P, Wang H, He M, Chen B, Yang B, Hu B. Size-dependent cytotoxicity study of ZnO nanoparticles in HepG2 cells. Ecotoxicol Environ Saf. 2019;171:337–346. doi:10.1016/j.ecoenv.2018.12.09630616150
  • Liu Q, Xu C, Ji G, et al. Sublethal effects of zinc oxide nanoparticles on male reproductive cells. Toxicol in Vitro. 2016;35:131–138. doi:10.1016/j.tiv.2016.05.01727247145
  • Esmaeillou M, Moharamnejad M, Hsankhani R, Tehrani AA, Maadi H. Toxicity of ZnO nanoparticles in healthy adult mice. Environ Toxicol Pharmacol. 2013;35(1):67–71. doi:10.1016/j.etap.2012.11.00323262039
  • Park H-S, Shin -S-S, Meang EH, et al. A 90-day study of subchronic oral toxicity of 20 nm, negatively charged zinc oxide nanoparticles in sprague dawley rats. Int J Nanomedicine. 2014;9(Suppl 2):79.25565828
  • Inhorn MC, Patrizio P. Infertility around the globe: new thinking on gender, reproductive technologies and global movements in the 21st century. Hum Reprod Update. 2015;21(4):411–426. doi:10.1093/humupd/dmv01625801630
  • Bisht S, Faiq M, Tolahunase M, Dada R. Oxidative stress and male infertility. Nat Rev Urol. 2017;14(8):470–485. doi:10.1038/nrurol.2017.6928508879
  • Lan Z, Yang W-X. Nanoparticles and spermatogenesis: how do nanoparticles affect spermatogenesis and penetrate the blood–testis barrier. Nanomedicine. 2012;7(4):579–596. doi:10.2217/nnm.12.2022471721
  • 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. doi:10.1111/ija.2009.32.issue-418217983
  • Mozaffari Z, Parivar K, Roodbari NH, Irani S. Histopathological evaluation of the toxic effects of zinc oxide (ZnO) nanoparticles on testicular tissue of NMRI adult mice. Adv Stud Biol. 2015;7:275–291. doi:10.12988/asb.2015.5425
  • Abbasalipourkabir R, Moradi H, Zarei S, et al. Toxicity of zinc oxide nanoparticles on adult male Wistar rats. Food Chem Toxicol. 2015;84:154–160. doi:10.1016/j.fct.2015.08.01926316185
  • Talebi AR, Khorsandi L, Moridian M. The effect of zinc oxide nanoparticles on mouse spermatogenesis. J Assist Reprod Genet. 2013;30(9):1203–1209. doi:10.1007/s10815-013-0078-y23949131
  • Saliani M, Jalal R, Goharshadi E. Mechanism of oxidative stress involved in the toxicity of ZnO nanoparticles against eukaryotic cells. Nanomed J. 2016;3(1):1–14.
  • Song W, Zhang J, Guo J, et al. Role of the dissolved zinc ion and reactive oxygen species in cytotoxicity of ZnO nanoparticles. Toxicol Lett. 2010;199(3):389–397. doi:10.1016/j.toxlet.2010.10.00320934491
  • Brodsky JL, Skach WR. Protein folding and quality control in the endoplasmic reticulum: recent lessons from yeast and mammalian cell systems. Curr Opin Cell Biol. 2011;23(4):464–475. doi:10.1016/j.ceb.2011.05.00421664808
  • Wang M, Kaufman RJ. Protein misfolding in the endoplasmic reticulum as a conduit to human disease. Nature. 2016;529(7586):326. doi:10.1038/nature1704126791723
  • Kadowaki H, Nishitoh H. Endoplasmic reticulum quality control by garbage disposal. FEBS J. 2019;286(2):232–240. doi:10.1111/febs.2019.286.issue-229923316
  • Iurlaro R, Muñoz-Pinedo C. Cell death induced by endoplasmic reticulum stress. FEBS J. 2016;283(14):2640–2652. doi:10.1111/febs.1359826587781
  • Yang X, Shao H, Liu W, et al. Endoplasmic reticulum stress and oxidative stress are involved in ZnO nanoparticle-induced hepatotoxicity. Toxicol Lett. 2015;234(1):40–49. doi:10.1016/j.toxlet.2015.02.00425680694
  • Kuang H, Yang P, Yang L, Aguilar ZP, Xu H. Size dependent effect of ZnO nanoparticles on endoplasmic reticulum stress signaling pathway in murine liver. J Hazard Mater. 2016;317:119–126. doi:10.1016/j.jhazmat.2016.05.06327262279
  • Yin L, Dai Y, Cui Z, et al. The regulation of cellular apoptosis by the ROS-triggered PERK/EIF2alpha/chop pathway plays a vital role in bisphenol A-induced male reproductive toxicity. Toxicol Appl Pharmacol. 2017;314:98–108. doi:10.1016/j.taap.2016.11.01327894913
  • Kisin ER, Yanamala N, Farcas MT, et al. Abnormalities in the male reproductive system after exposure to diesel and biodiesel blend. Environ Mol Mutagen. 2015;56(2):265–276. doi:10.1002/em.v56.225327512
  • Shang L, Nienhaus K, Nienhaus GU. Engineered nanoparticles interacting with cells: size matters. J Nanobiotechnol. 2014;12(1):5. doi:10.1186/1477-3155-12-5
  • Hong F, Zhao X, Si W, et al. Decreased spermatogenesis led to alterations of testis-specific gene expression in male mice following nano-TiO2 exposure. J Hazard Mater. 2015;300:718–728. doi:10.1016/j.jhazmat.2015.08.01026296075
  • Lu X, Liu Y, Kong X, Lobie PE, Chen C, Zhu T. Nanotoxicity: a growing need for study in the endocrine system. Small. 2013;9(9–10):1654–1671. doi:10.1002/smll.20120151723401134
  • Baek M, Chung H-E, Yu J, et al. Pharmacokinetics, tissue distribution, and excretion of zinc oxide nanoparticles. Int J Nanomed. 2012;7:3081.
  • Gao G, Ze Y, Zhao X, et al. Titanium dioxide nanoparticle-induced testicular damage, spermatogenesis suppression, and gene expression alterations in male mice. J Hazard Mater. 2013;258:133–143. doi:10.1016/j.jhazmat.2013.04.04623721730
  • Toocheck C, Clister T, Shupe J, et al. Mouse spermatogenesis requires classical and nonclassical testosterone signaling. Biol Reprod. 2016;94(1):11. doi:10.1095/biolreprod.115.13206826607719
  • Chen R, Huo L, Shi X, et al. Endoplasmic reticulum stress induced by zinc oxide nanoparticles is an earlier biomarker for nanotoxicological evaluation. ACS Nano. 2014;8(3):2562–2574. doi:10.1021/nn406184r24490819
  • Schröder M, Kaufman RJ. The mammalian unfolded protein response. Annu Rev Biochem. 2005;74:739–789. doi:10.1146/annurev.biochem.73.011303.07413415952902
  • Zhu G, Lee AS. Role of the unfolded protein response, GRP78 and GRP94 in organ homeostasis. J Cell Physiol. 2015;230(7):1413–1420. doi:10.1002/jcp.2492325546813
  • Hetz C, Papa FR. The unfolded protein response and cell fate control. Mol Cell. 2018;69(2):169–181. doi:10.1016/j.molcel.2017.06.01729107536
  • Zhang Q, Liu J, Chen S, et al. Caspase-12 is involved in stretch-induced apoptosis mediated endoplasmic reticulum stress. Apoptosis. 2016;21(4):432–442. doi:10.1007/s10495-016-1217-626801321
  • Urano F, Wang X, Bertolotti A, et al. Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science. 2000;287(5453):664–666. doi:10.1126/science.287.5453.66410650002
  • Adams JM, Cory S. The BCL-2 arbiters of apoptosis and their growing role as cancer targets. Cell Death Differ. 2018;25(1):27. doi:10.1038/cdd.2017.161
  • Man SM, Kanneganti T-D. Converging roles of caspases in inflammasome activation, cell death and innate immunity. Nat Rev Immunol. 2016;16(1):7. doi:10.1038/nri.2015.726655628
  • Wang D. ZnO nanoparticle-induced oxidative stress triggers apoptosis by activating JNK signaling pathway in cultured primary astrocytes. Nanoscale Res Lett. 2014;9(1):12. doi:10.1186/1556-276X-9-58924400888
  • Duan P, Hu C, Quan C, et al. 4-Nonylphenol induces apoptosis, autophagy and necrosis in sertoli cells: involvement of ROS-mediated AMPK/AKT-mTOR and JNK pathways. Toxicology. 2016;341-343:28–40. doi:10.1016/j.tox.2016.01.00426804764
  • Eladak S, Moison D, Guerquin MJ, et al. Effects of environmental Bisphenol A exposures on germ cell development and Leydig cell function in the human fetal testis. PLoS One. 2018;13(1):e0191934. doi:10.1371/journal.pone.019193429385186
  • Li L, Mu X, Ye L, Ze Y, Hong F. Suppression of testosterone production by nanoparticulate TiO2 is associated with ERK1/2-PKA-PKC signaling pathways in rat primary cultured Leydig cells. Int J Nanomedicine. 2018;13:5909–5924. doi:10.2147/IJN.S17560830319256
  • West LA, Horvat RD, Roess DA, Barisas BG, Juengel JL, Niswender GD. Steroidogenic acute regulatory protein and peripheral-type benzodiazepine receptor associate at the mitochondrial membrane. Endocrinology. 2001;142(1):502–505. doi:10.1210/endo.142.1.805211145616
  • Wang H, Wang Q, Zhao X-F, et al. Cypermethrin exposure during puberty disrupts testosterone synthesis via downregulating StAR in mouse testes. Arch Toxicol. 2010;84(1):53–61. doi:10.1007/s00204-009-0479-y19862501
  • Hu M-C, Chiang EF-L, Tong S-K, et al. Regulation of steroidogenesis in transgenic mice and zebrafish. Mol Cell Endocrinol. 2001;171(1–2):9–14. doi:10.1016/S0303-7207(00)00385-311165005
  • Payne AH, Hales DB. Overview of steroidogenic enzymes in the pathway from cholesterol to active steroid hormones. Endocr Rev. 2004;25(6):947–970. doi:10.1210/er.2003-003015583024