La₂O₃ Nanoparticles Induce Reproductive Toxicity Mediated by the Nrf-2/ARE Signaling Pathway in Kunming Mice

References

• Espuche E, David L, Rochas C, et al. In situ generation of nanoparticulate lanthanum(III) oxide-polyimide films: characterization of nanoparticle formation and resulting polymer properties. Polymer. 2005;46(17):6657–6665. doi:10.1016/j.polymer.2005.05.020
   Web of Science ®Google Scholar
• Yue L, Ma C, Zhan X, White J, Xing B. Molecular mechanisms of maize seedling response to La2O3 NP exposure: water uptake, aquaporin gene expression and signal transduction. Environ Sci Nano. 2017;4(4):843–855. doi:10.1039/C6EN00487C
   Web of Science ®Google Scholar
• Gerber LC, Moser N, Luechinger NA, Stark WJ, Grass RN. Phosphate starvation as an antimicrobial strategy: the controllable toxicity of lanthanum oxide nanoparticles. Chem Commun. 2012;48(32):3869–3871. doi:10.1039/c2cc30903c
   PubMed Web of Science ®Google Scholar
• Brabu B, Haribabu S, Revathy M, et al. Biocompatibility studies on lanthanum oxide nanoparticles. Toxicol Res (Camb). 2015;4(4):1037–1044. doi:10.1039/C4TX00198B
   Web of Science ®Google Scholar
• Guha A, Basu A. Role of rare earth oxide nanoparticles (CeO2 and La2O3) in suppressing the photobleaching of fluorescent organic dyes. J Fluoresc. 2014;24(3):683–687. doi:10.1007/s10895-014-1375-224706286
   PubMed Web of Science ®Google Scholar
• Sisler JD, Pirela SV, Shaffer J, et al. Toxicological assessment of CoO and La2O3 metal oxide nanoparticles in human small airway epithelial cells. Toxicol Sci. 2016;150(2):418–428. doi:10.1093/toxsci/kfw00526769336
   PubMed Web of Science ®Google Scholar
• Giovanni M, Tay CY, Setyawati MI, et al. Toxicity profiling of water contextual zinc oxide, silver, and titanium dioxide nanoparticles in human oral and gastrointestinal cell systems. Environ Toxicol. 2016;30(12):1459–1469. doi:10.1002/tox.22015
   Web of Science ®Google Scholar
• Priester JH, Yuan G, Mielke RE, et al. Soybean susceptibility to manufactured nanomaterials with evidence for food quality and soil fertility interruption. Proc Natl Acad Sci. 2012;109(37):14734–14735. doi:10.1073/pnas.1205431109
   Web of Science ®Google Scholar
• Balusamy B, Taştan BE, Ergen SF, Uyar T, Tekinay T. Toxicity of lanthanum oxide (La2O3) nanoparticles in aquatic environments. Environ Sci Process Impacts. 2015;17(7):1265–1270. doi:10.1039/C5EM00035A26022751
   PubMed Web of Science ®Google Scholar
• Liu Y, Xu L, Dai Y. Phytotoxic effects of lanthanum oxide nanoparticles on maize (Zea mays L.). IOP conference series. Earth Environ Sci. 2018;113(1):013–020.
   Google Scholar
• Ma Y, Zhang P, Zhang Z, et al. Origin of the different phytotoxicity and biotransformation of cerium and lanthanum oxide nanoparticles in cucumber. Nanotoxicology. 2015;9(2):9. doi:10.3109/17435390.2014.92134424289294
   PubMed Web of Science ®Google Scholar
• Servin AD, White JC. Nanotechnology in agriculture: next steps for understanding engineered nanoparticle exposure and risk. Nanoimpact. 2016;1:9–12. doi:10.1016/j.impact.2015.12.002
   Web of Science ®Google Scholar
• Roberto DLTR, Alia S, Joseph H, et al. Terrestrial trophic transfer of bulk and nanoparticle La2O3 does not depend on particle size. Environ Sci Technol. 2015;49(19):11866–11874. doi:10.1021/acs.est.5b0258326356537
   PubMed Web of Science ®Google Scholar
• Lim CH. Toxicity of two different sized lanthanum oxides in cultured cells and sprague-dawley rats. Toxicol Res. 2015;31(2):181–189. doi:10.5487/TR.2015.31.2.18126191385
   PubMedGoogle Scholar
• Shin SH, Lim CH, Kim YS, Lee YH, Kim SH, Kim JC. Twenty-eight-day repeated inhalation toxicity study of nano-sized lanthanum oxide in male sprague-dawley rats. Environ Toxicol. 2016;32(4):1226–40.27441813
   PubMed Web of Science ®Google Scholar
• Sisler JD, Li R, Mckinney W, et al. Differential pulmonary effects of CoO and La2O3 metal oxide nanoparticle responses during aerosolized inhalation in mice. Part Fibre Toxicol. 2016;13(1):42. doi:10.1186/s12989-016-0155-327527840
   PubMedGoogle Scholar
• Li R, Ji Z, C H C, et al. Surface interactions with compartmentalized cellular phosphates explain rare earth oxide nanoparticle hazard and provide opportunities for safer design. ACS Nano. 2014;8(2):1771–1783. doi:10.1021/nn406166n24417322
   PubMed Web of Science ®Google Scholar
• Sun QC, Wu Y, Zhao F, Wang JJ. Maresin 1 ameliorates lung Ischemia/Reperfusion injury by suppressing oxidative stress via activation of the Nrf-2-Mediated HO-1 signaling pathway. Oxid Med Cell Longev. 2017;1–12.
   Web of Science ®Google Scholar
• Wang J, Li N, Zheng L, et al. P38-Nrf-2 signaling pathway of oxidative stress in mice caused by nanoparticulate TiO2. Biol Trace Elem Res. 2011;140(2):186–197. doi:10.1007/s12011-010-8687-020422311
   PubMed Web of Science ®Google Scholar
• Bai D, Li Q, Xiong Y, et al. Editor’s highlight: effects of intraperitoneal injection of SnS2 flowers on mouse testicle. Toxicol Sci. 2017;161(2):388–400. doi:10.1093/toxsci/kfx220
   Web of Science ®Google Scholar
• Ahmmd SMA. Evaluating the effect of silver nanoparticles on testes of adult albino rats (Histological, immunohistochemical and biochemical study). J Mol Histol. 2016;48(1):1–19. doi:10.1007/s10735-016-9700-527787633
   PubMed Web of Science ®Google Scholar
• Boekelheide K, Shawna L, Kamin J. Role of Sertoli cells in injury-associated testicular germ cell apoptosis. Exp Biol Med. 2000;225(2):105–115. doi:10.1046/j.1525-1373.2000.22513.x
   PubMed Web of Science ®Google Scholar
• Yang H, Du L, Tian X, et al. Effects of nanoparticle size and gestational age on maternal biodistribution and toxicity of gold nanoparticles in pregnant mice. Toxicol Lett. 2014;230(1):10–18. doi:10.1016/j.toxlet.2014.07.03025102025
   PubMed Web of Science ®Google Scholar
• Grassian VH, Adamcakova-Dodd A, Pettibone JM, O’Shaughnessy PI, Thorne PS. Inflammatory response of mice to manufactured titanium dioxide nanoparticles: comparison of size effects through different exposure routes. Nanotoxicology. 2007;1(3):211–226. doi:10.1080/17435390701694295
   Web of Science ®Google Scholar
• Lu X, Tian Y, Zhao Q, Jin T, Xiao S, Fan X. Integrated metabonomics analysis of the size-response relationship of silica nanoparticles-induced toxicity in mice. Nanotechnology. 2011;22(5):055101. doi:10.1088/0957-4484/22/5/05510121178262
   PubMed Web of Science ®Google Scholar
• Khorsandi L, Orazizadeh M, Moradi-Gharibvand N, Hemadi M, Mansouri E. Beneficial effects of quercetin on titanium dioxide nanoparticles induced spermatogenesis defects in mice. Environ Sci Pollut Res Int. 2017;24(6):5595–5606. doi:10.1007/s11356-016-8325-228035607
   PubMed Web of Science ®Google Scholar
• 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
   PubMed Web of Science ®Google Scholar
• Sundarraj K, Manickam V, Raghunath A, et al. Repeated exposure to iron oxide nanoparticles causes testicular toxicity in mice. Environ Toxicol. 2016;32(2):594–608. doi:10.1002/tox.2226226991130
   PubMed Web of Science ®Google Scholar
• Hong F, Si W, Zhao X, et al. TiO2 nanoparticles exposure decreases spermatogenesis via biochemical dysfunctions in the testis of male mice. Agric Food Chemi. 2015;63(31):7084–7092. doi:10.1021/acs.jafc.5b02652
   PubMed Web of Science ®Google Scholar
• Iavicoli I, Fontana L, Leso V, Bergamaschi A. The effects of nanomaterials as endocrine disruptors. Int J Mol Sci. 2013;14(8):16732–16801. doi:10.3390/ijms14081673223949635
   PubMed Web of Science ®Google Scholar
• Xiong X, Zhong A, Xu H, Lobaccaro J-MA. Effect of cyanotoxins on the hypothalamic–pituitary–gonadal axis in male adult mouse. PLoS One. 2014;9(11):e106585–106594. doi:10.1371/journal.pone.010658525375936
   PubMed Web of Science ®Google Scholar
• Cheng Y-S, Dai D-Z, Dai Y. Testis dysfunction by isoproterenol is mediated by upregulating endothelin receptor A, leptin and protein kinase Cɛ and is attenuated by an endothelin receptor antagonist CPU0213. Reprod Toxicol. 2010;29(4):421–426. doi:10.1016/j.reprotox.2010.03.00120307649
   PubMed Web of Science ®Google Scholar
• G L L, Yu F, D Z D, et al. Endoplasmic reticulum stress mediating downregulated StAR and 3-beta-HSD and low plasma testosterone caused by hypoxia is attenuated by CPU86017-RS and nifedipine. J Biomed Sci. 2012;19(1):4–15. doi:10.1186/1423-0127-19-422226148
   PubMedGoogle Scholar
• Minutoli L, Micali A, Pisani A, et al. Flavocoxid protects against cadmium-induced disruption of the blood-testis barrier and improves testicular damage and germ cell impairment in mice. Toxicol Sci. 2015;148(1):311–329. doi:10.1093/toxsci/kfv18526424772
   PubMed Web of Science ®Google Scholar
• Orazizadeh M, Khorsandi L, Absalan F, et al. Effect of beta-carotene on titanium oxide nanoparticles-induced testicular toxicity in mice. J Assist Reprod Genet. 2014;31(5):561–568. doi:10.1007/s10815-014-0184-524515782
   PubMed Web of Science ®Google Scholar
• Hasegawa T, Zhao L, K M C, et al. Developmental roles of the steroidogenic acute regulatory protein (StAR) as revealed by StAR knockout mice. Mol Endocrinol. 2000;14(9):1462–1471. doi:10.1210/mend.14.9.051510976923
   PubMedGoogle Scholar
• Cao Z, Shao B, Xu F, et al. Protective effect of selenium on Aflatoxin B1-induced testicular toxicity in mice. Biol Trace Elem Res. 2017;180(2):233–238. doi:10.1007/s12011-017-0997-z28349382
   PubMed Web of Science ®Google Scholar
• Weisser J, Landreh L, Söder O, et al. Steroidogenesis and steroidogenic gene expression in postnatal fetal rat Leydig cells. Mol Cell Endocrinol. 2011;341(1–2):18–24. doi:10.1016/j.mce.2011.03.00821458522
   PubMed Web of Science ®Google Scholar
• Rosario B, Filippo M, Patrizia C, et al. Endurance exercise and conjugated linoleic acid (CLA) supplementation up-regulate CYP17A1 and stimulate testosterone biosynthesis. PLoS One. 2013;8(11):e79686–79696. doi:10.1371/journal.pone.007968624223995
   PubMed Web of Science ®Google Scholar
• Rukiye H, Sema U, Hacer H, et al. Protective effects of Ankaferd blood stopper on aspirin-induced oxidative mucosal damage in a rat model of gastric injury. Toxicol Ind Health. 2014;30(10):888–895. doi:10.1177/074823371246613423114375
   PubMed Web of Science ®Google Scholar
• Zhang H, Ji Z, Xia T, et al. Use of metal oxide nanoparticle band gap to develop a predictive paradigm for oxidative stress and acute pulmonary inflammation. ACS Nano. 2012;6(5):4349–4368. doi:10.1021/nn301008722502734
   PubMed Web of Science ®Google Scholar
• Suzanne Marie H, Ajay K, Sanjay S, et al. Bio-distribution and in vivo antioxidant effects of cerium oxide nanoparticles in mice. Environ Toxicol. 2013;28(2):107–118. doi:10.1002/tox.2070421618676
   PubMed Web of Science ®Google Scholar
• Tsugita M, Morimoto N, Nakayama M. SiO2 and TiO2 nanoparticles synergistically trigger macrophage inflammatory responses. Part Fibre Toxicol. 2017;14(1):11. doi:10.1186/s12989-017-0192-628399878
   PubMedGoogle Scholar
• Ren L, Zhang J, Zou Y, et al. Silica nanoparticles induce reversible damage of spermatogenic cells via RIPK1 signal pathways in C57 mice. Int J Nanomedicine. 2016;11:2251–2264. doi:10.2147/IJN.S10226827307728
   PubMed Web of Science ®Google Scholar
• Jeong J, Song T, Chatterjee N, et al. Developing adverse outcome pathways on silver nanoparticle-induced reproductive toxicity via oxidative stress in the nematode Caenorhabditis elegans using a Bayesian network model. Nanotoxicology. 2019;12(10):1182–97.
   Web of Science ®Google Scholar
• Du D, Yao L, Zhang R, et al. Protective effects of flavonoids from, Coreopsis tinctoria, Nutt. on experimental acute pancreatitis via Nrf-2/ARE-mediated antioxidant pathways. J Ethnopharmacol. 2018;224:261–272. doi:10.1016/j.jep.2018.06.00329870787
   PubMed Web of Science ®Google Scholar
• Yang SH, Yu LH, Li L, et al. Protective mechanism of sulforaphane on Cadmium-induced sertoli cell injury in mice testis via Nrf-2/ARE signaling pathway. Molecules. 2018;23(7):1774. doi:10.3390/molecules23071774
   PubMed Web of Science ®Google Scholar
• Yang SH, Long M, Yu LH, et al. Sulforaphane prevents testicular damage in kunming mice exposed to cadmium via activation of Nrf-2/ARE signaling pathways. Int J Mol Sci. 2016;17(10):1703. doi:10.3390/ijms17101703
   PubMed Web of Science ®Google Scholar
• Promsan S, Jaikumkao K, Pongchaidecha A, et al. Pinocembrin attenuates Gentamicin-induced nephrotoxicity in rats. Physiol Pharmacol. 2016;94(08):808–18.
   Google Scholar
• Feng S, Xu ZF, Wang F, et al. Sulforaphane prevents methylmercury-induced oxidative damage and excitotoxicity through activation of the Nrf2-ARE pathway. Mol Neurobiol. 2017;54(1):375–391. doi:10.1007/s12035-015-9643-y26742517
   PubMed Web of Science ®Google Scholar
• Long M, Yang SH, Shi W, et al. Protective effect of proanthocyanidin on mice Sertoli cell apoptosis induced by zearalenone via the Nrf-2/ARE signalling pathway. Environ Sci Pollut Res. 2017;24(1–4):1–10. doi:10.1007/s11356-017-0123-y
   PubMedGoogle Scholar
• Hedger PM. Immunophysiology and pathology of inflammation in the testis and epididymis. J Androl. 2011;32(6):625–640. doi:10.2164/jandrol.111.01298921764900
   PubMedGoogle Scholar
• Reyes JG, Farias JG, Eva M, et al. The hypoxic testicle: physiology and pathophysiology. Oxid Med Cell Longev. 2012;2012(18):929285.23056665
   PubMedGoogle Scholar
• Guo Y, Sun J, Li T, et al. Melatonin ameliorates restraint stress-induced oxidative stress and apoptosis in testicular cells via NF-κB/iNOS and Nrf2/HO-1 signaling pathway. Sci Rep. 2017;7(1):9599. doi:10.1038/s41598-017-09943-228851995
   PubMed Web of Science ®Google Scholar
• Jin HK, Sun W, Dong WH, Moon HJ, Lee J. iNSC suppress macrophage-induced inflammation by repressing COX-2. Vitro Cell Dev Biol Anim. 2015;51(2):157–164. doi:10.1007/s11626-014-9816-4
   PubMed Web of Science ®Google Scholar
• Zhuang Z, Ye G, Huang B. Kaempferol alleviates the interleukin-1β-induced inflammation in rat osteoarthritis chondrocytes via suppression of NF-κB. Int Med J Exp Clin Res. 2017;23:3925–3931.
   Google Scholar