Low-dose gold nanoparticles exert subtle endocrine-modulating effects on the ovarian steroidogenic pathway ex vivo independent of oxidative stress

References

• Alkilany AM, Murphy CJ. 2010. Toxicity and cellular uptake of gold nanoparticles: what we have learned so far? J Nanopart Res 12:2313–2333.
   PubMed Web of Science ®Google Scholar
• Arnida Janat-Amsbury MM, Ray A, Peterson CM, Ghandehari H. 2011. Geometry and surface characteristics of gold nanoparticles influence their biodistribution and uptake by macrophage. Eur J Pharm Biopharm 77:417–423.
   PubMed Web of Science ®Google Scholar
• Bischof JC, Goel R, Paciotti GF, Shah N, Visaria R. 2009. Biodistribution of TNF-[alpha]-coated gold nanoparticles in an in vivo model system. Nanomedicine 4:401–410.
   Google Scholar
• Cai J, Jones DP. 1998. Superoxide in apoptosis: mitochondrial generation triggered by cytochrome c loss. J Biol Chem 273:11401–11404.
   PubMed Web of Science ®Google Scholar
• Chen YS, Hung YC, Lin LW, Liau I, Hong MY, Huang GS. 2010. Size-dependent impairment of cognition in mice caused by the injection of gold nanoparticles. Nanotechnology 21(48):485102.
   Google Scholar
• Cho WS, Cho W, Jeong J, Choi M, Han BS, Shin HS, et al. 2010. Size-dependent tissue kinetics of PEG-coated gold nanoparticles. Toxicol Appl Pharmacol 245:116–123.
   PubMed Web of Science ®Google Scholar
• Craig ZR, Wang W, Flaws JA. 2011. Endocrine-disrupting chemicals in ovarian function: effects on steroidogenesis, metabolism and nuclear receptor signaling. Reproduction 142:633–646.
   PubMed Web of Science ®Google Scholar
• Diemer T, Allen JA, Hales KH, Hales DB. 2003. Reactive oxygen disrupts mitochondria in MA-10 tumor leydig cells and inhibits steroidogenic acute regulatory (StAR) protein and steroidogenesis. Endocrinology 144:2882–2891S.
   PubMed Web of Science ®Google Scholar
• Esch RK, Han LI, Karin K, Foarde KK, Ensor SD. 2010. Endotoxin contamination of engineered nanomaterials. Nanotoxicology 4:73–83.
   PubMed Web of Science ®Google Scholar
• Esmaeillou M, Moharamnejad M, Hsankhani R, Tehrani AA, Maadi H. 2013. Toxicity of ZnO nanoparticles in healthy adult mice. Environ Toxicol Pharmacol 35:67–71.
   PubMed Web of Science ®Google Scholar
• Gao G, Yuguan Z, Bing L, Zhao X, Zhang T, Sheng L, et al. 2012. Ovarian dysfunction and gene-expression characteristics of female mice caused by long-term exposure to titanium dioxide nanoparticles. J Hazard Mater 243:19–27.
   PubMed Web of Science ®Google Scholar
• Gao W, Xu K, Ji L, Tang B. 2011. Effect of gold nanoparticles on glutathione depletion-induced hydrogen peroxide generation and apoptosis in HL7702 cells. Toxicol Lett 205:86–95.
   PubMed Web of Science ®Google Scholar
• Hamada T, Watanabe G, Kokuho T, Taya K, Sasamoto S, Hasegawa Y, et al. 1989. Radioimmunoassay of inhibin in various mammals. J Endocrinol 122:697–704.
   PubMed Web of Science ®Google Scholar
• Harper SL, Carriere JL, Miller JM, Hutchinson JE, Maddux BLS, Tanguay RL. 2011. Systemic evaluation of nanomaterials toxicity: utility of standardized materials and rapid assays. ACS Nano 5:4688–4697.
   PubMed Web of Science ®Google Scholar
• Haseman JK, Bailer AJ, Kodell RL, Morris R, Portier K. 2001. Statistical issues in the analysis of low-dose endocrine disruptor data. Toxicol Sci 61:201–210.
   PubMed Web of Science ®Google Scholar
• Hinderliter PM, Minard KR, Orr G, Chrisler WB, Thrall BD, Pounds JG, et al. 2010. ISDD: A computational model of particle sedimentation, diffusion and target cell dosimetry for in vitro toxicity studies. Part Fibre Toxicol 7:36.
   PubMed Web of Science ®Google Scholar
• Ho HM, Oshima K, Watanabe G, Taya K, Strawn EY, Hutz RJ. 2006. TCDD increases inhibin A production by human luteinized granulosa cells in vitro. J Reprod Dev 52:523–528.
   PubMed Web of Science ®Google Scholar
• Hussain S, Vanoirbeek JA, Luyts K, De Vooght V, Verbeken E, Thomassen LC, et al. 2011. Lung exposure to nanoparticles modulates an asthmatic response in a mouse model. Eur Respir J 37:299–309.
   PubMed Web of Science ®Google Scholar
• Hutz RJ, Carvan MJ, Baldridge MG, Conley LK, Heiden TK. 2006. Environmental toxicants and effects on female reproductive function. Tren Reprod Bio 2:1–11.
   Google Scholar
• Kessler R. 2011. Engineered nanoparticles in consumer products. Environ Health Perspect 119:a120–a125.
   PubMed Web of Science ®Google Scholar
• Khlebtsov N, Dykman L. 2011. Biodistribution and toxicity of engineered gold nanoparticles: a review of in vitro and in vivo studies. Chem Soc Rev 40:1647–1671.
   PubMed Web of Science ®Google Scholar
• Kimling J, Maier M, Okenve B, Kotaidis V, Ballot H, Plech A. 2006. Turkevich method for gold nanoparticle synthesis revisited. J Phys Chem B 110:15700–15777.
   PubMed Web of Science ®Google Scholar
• Larios-Rodriguez E, Rangel-Ayon C, Castillo SJ, Zavala G, Herrera-Urbina R. 2011. Bio-synthesis of gold nanoparticles by human epithelial cells, in vivo. Nanotechnology 22:355601.
   Google Scholar
• Li JJ, Lo SL, NG CT, Gurung RL, Hartono D, Hande MP, et al. 2011. Genomic instability of gold nanoparticles treated human lung fibroblast cells. Biomaterials 32:5515–5523.
   PubMed Web of Science ®Google Scholar
• Libutti SK, Paciotti GF, Byrnes AA, Alexander HR Jr, Gannon WE, Walker M, et al. 2010. Phase 1 and pharmacokinetic studies of CYT-6091, a novel PEGlyated colloidal gold-rhTNF nanomedicine. Clin Cancer Res 16:6139–6149.
   PubMed Web of Science ®Google Scholar
• Lui X, Qin D, Cui Y, Chen L, Li H, Chen Z, et al. 2010. The effect of calcium phosphate nanoparticles on hormone production and apoptosis in human granulosa cells. Reprod Biol Endocrinol 8:32.
   Google Scholar
• Miller MC 3rd, Mohrenweiser HW, Bell DA. 2001. Genetic variability in susceptibility and response to toxicants. Toxicol Lett 120:269–280.
   PubMed Web of Science ®Google Scholar
• Monopoli MP, Aberg C, Salvati A, Dawson A. 2012. Biomolecular coronas provide the biological identity of nanosized materials. Nat Nanotechnol 7:779–786.
   PubMed Web of Science ®Google Scholar
• Nel AE, Mädler L, Velegol D, Xia T, Hoek EM, Somasundaran P, et al. 2009. Understanding biophysicochemical interactions at the nano-bio interface. Nat Mater 8.
   Google Scholar
• Ngo YH, Li D, Simon GP, Garnier G. 2011. Paper surfaces functionalized by nanoparticles. Adv Colloid Interface Sci 163:23–38.
   PubMed Web of Science ®Google Scholar
• Pfaffl MW. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45.
   PubMed Web of Science ®Google Scholar
• Shumyantseva VV, Carrara S, Bavastrello V, Riley JD, Skryabin KG, Archakov AI, et al. 2005. Direct electron transfer between cytochrome P450scc and gold nanoparticles on screen-printed rhodium-graphite electrodes. Biosens Bioelectron 21:217–222.
   Google Scholar
• Stelzer RV, Hutz RJ. 2009. Gold nanoparticles enter rat ovarian granulosa cells and subcellular organelles, and alter in-vitro estrogen accumulation. J Reprod Develop 55:685–690.
   PubMed Web of Science ®Google Scholar
• Sung JH, Ji JH, Park JD, Song MY, Song KS, Hyeon RR, et al. 2011. Subchronic inhalation toxicity of gold nanoparticles. Part Fibre Toxicol 8:16.
   PubMed Web of Science ®Google Scholar
• Taylor CC, Terranova PF. 1996. Lipopolysaccharide inhibits in vitro luteinizing hormone-stimulated rat ovarian granulosa cell estradiol but not progesterone secretion. Biol Reprod 54:1390–1396.
   PubMed Web of Science ®Google Scholar
• Trkulja V, Lackovic Z. 2001. Vagal Influence on compensatory ovarian growth is important only briefly after hemicastration. Exp Biol Med 226:776–781.
   Google Scholar
• Truong L, Tilton SC, Zaikova T, Richman E, Waters KM, Hutchinson JE, et al. 2012. Surface functionalities of gold nanoparticles impact embryonic gene expression responses. Nanotoxicol Early Online 1–10. DOI: 10.3109/17435390.2011.648225.
   Google Scholar
• Tsai CY, Lu SL, Hu CW, Yeh CS, Lee GB, Lei HY. 2012. Size-dependent attenuation of TLR9 signaling by gold nanoparticles in macrophages. J Immunol 188:68–76.
   PubMed Web of Science ®Google Scholar
• Vandenberg LN, Colborn T, Hayes TB, Heindel JJ, Jacobs DR Jr, Lee D-H, et al. 2012. Hormones and endocrine-disrupting chemicals: low-dose effects and nonmonotonic dose responses. Endocr Rev 33:378–455.
   PubMed Web of Science ®Google Scholar
• Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, et al. 2002. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple control genes. Genome Biol 3:research0034.1–researc0034.11.
   PubMed Web of Science ®Google Scholar
• Wang J, Zhu X, Zhang X, Zhao Z, Liu H, George R, et al. 2011. Disruption of zebrafish (Danio rerio) reproduction upon chronic exposure to TiO2 nanoparticles. Chemosphere 83:461–467.
   PubMed Web of Science ®Google Scholar
• Woodrow Wilson International Center for Scholars: A nanotechnology consumer products inventory 2012. Available at http://www.nanotechproject.org/consumerproducts. Accessed on 1 March 2013.
   Google Scholar
• Yin R, Tian F, Frankenberger B, de Angelis MH, Stoeger T. 2010. Selection and evaluation of stable housekeeping genes for gene expression normalization in carbon nanoparticle-induced acute pulmonary inflammation in mice. Biochem Biophys Res Commun 399:531–536.
   Google Scholar
• Young JM, McNeilly AS. 2012. Inhibin removes the inhibitory effects of activin on steroid enzyme expression and androgen production by normal ovarian thecal cells. J Mol Endocrinol 48:49–60.
   Google Scholar