Endocrine disruptive effects of cadmium on steroidogenesis: Human adrenocortical carcinoma cell line NCI-H295R as a cellular model for reproductive toxicity testing

References

• WHO (World Health Organization). Cadmium. Environmental Health Criteria, No. 134. Geneva: WHO, 1992.
   Google Scholar
• IRPTC (International Register of Potentially Toxic Chemicals). IRPTC legal file 1986, vol. 1. Geneva: IRPTC, United Nations Environment Programme, 1986.
   Google Scholar
• Fried, K.W.; Rozman, K.K. Toxicity of selected chemicals. In Toxicology and Risk Assessment: A Comprehensive Introduction; Greim, H.; Snyder, R., Eds.; Chichester: John Wiley and Sons, Ltd., 2008; 513–655.
   Google Scholar
• ATSDR (Agency for Toxic Substances and Disease Research). Toxicological profile for cadmium. Atlanta: ATSDR, 1999.
   Google Scholar
• Massanyi, P.; Bardos, L.; Toman, R. Effects of cadmium on the testicular structure and the level of retinoids and β-carotene in testis in mice after an experimental administration. Pol. J. Nat. Sci. 2002, 10, 133–139.
   Google Scholar
• Joseph, P. Mechanisms of cadmium carcinogenesis. Toxicol. Appl. Pharmacol. 2009, 238, 272–279.
   PubMed Web of Science ®Google Scholar
• IARC (International Agency for Research on Cancer). Beryllium, Cadmium, Mercury and exposures in the glass manufacturing industry. Monographs on the Evaluation of the Carcinogenic Risks to Humans, vol. 58, Lyon: IARC Scientific Publications, 1993; 119–146.
   Google Scholar
• NTP (US National Toxicology Program). Ninth Report on Carcinogens. National Toxicology Program, Research Triangle Park (NC), 2000.
   Google Scholar
• Waalkes, M.P. Metal carcinogenesis. In Handbook of Heavy Metals in the Environment; Sarkar, B., Eds.; Marcel Dekker: New York, 2002; 121–146.
   Google Scholar
• Takiguchi, M.; Yoshihara, S. New Aspects of Cadmium as Endocrine Disruptor. Environ. Sci. 2006, 13(2), 107–116.
   PubMedGoogle Scholar
• Korenekova, B.; Skalicka, M.; Nad, P. Cadmium exposure of cattle after long-term emission from polluted area. Trace Elem. Electrolytes 2002, 19, 97–99.
   Web of Science ®Google Scholar
• Jancova, A.; Massanyi, P.; Nad, P.; Korenekova, B.; Skalicka, M.; Drabekova, J.; Balaz, I. Accumulation of heavy metals in selected organs of yellow-necked mouse. Ekologia (Slovak) 2005, 25, 19–26.
   Google Scholar
• Hammond, P.B.; Beliles, R.P. Metals. In Casarett and Doull's Toxicology; Doull, J.; Klaassen, C.D.; Amdur, M.O., Eds.; New York: Macmillan Publ. Co., Inc., 1980; 409–467.
   Google Scholar
• Chang, L.W.; Reuhl, K.B.; Wade, P.R. Pathological effects of cadmium poisoning. In Cadmium in the Environment, Part 1, A; Nriagu, J.O., Ed.; Wiley-Interscience Publishers: New York, 1981; 783–839.
   Google Scholar
• Friberg, L.; Kjellstrom, T.; Nordberg, G.F. Cadmium. In Handbook on the Toxicology of Metals; Friberg, L.; Nordberg, G.F.; Vouk, V., Eds.; Amsterdam: Elsevier Science Publishing, 1986; 131–183.
   Google Scholar
• Kukner, A.; Colakoglu, N.; Kara, H.; Oner, H.; Ozogul, C.; Ozan, E. Ultrastructural changes in the kidney of rats with acute exposure to cadmium and effects of exogenous metallothionein. Biol. Trace Elem. Res. 2007, 119, 137–146.
   PubMed Web of Science ®Google Scholar
• Massanyi, P.; Lukac, N.; Uhrin, V.; Toman, R.; Pivko, J.; Rafay, J.; Forgacs, Z.; Somosy, Z. Female reproductive toxicology of cadmium. Acta Biol. Hungarica 2007, 58, 287–299.
   PubMed Web of Science ®Google Scholar
• Paksy, K.; Varga, B.; Lazar, P. Cadmium interferes with steroid biosynthesis in rat granulose and luteal cells in vitro. BioMetals 1992, 5, 245–250.
   PubMed Web of Science ®Google Scholar
• Pant, N.; Upadhyay, G.; Pandey, S.; Mathur, N.; Saxena, D.K.; Srivastava, S.P. Lead and cadmium concentration in the seminal plasma of men in the general population: Correlation with sperm quality. Reprod. Toxicol. 2003, 17, 447–450.
   PubMed Web of Science ®Google Scholar
• Roychoudhury, S.; Massanyi, P.; Bulla, J.; Choudhury, M.D.; Lukac, N.; Filipejova, T.; Trandzik, J.; Toman, R.; Almasiova, V. Cadmium toxicity at low concentration on rabbit spermatozoa motility, morphology and membrane integrity in vitro. J. Environ. Sci. Health Pt. A 2010, 45(11), 1374–1383.
   Web of Science ®Google Scholar
• Ozawa, N.; Goda, N.; Makino, N.; Yamaguchi, T.; Yoshimura, Y.; Suematsu, M. Leydig cell-derived heme oxygenase-1 regulates apoptosis of premeiotic germ cells in response to stress. J. Clin. Invest. 2002, 109, 457–467.
   PubMed Web of Science ®Google Scholar
• Kim, J.; Soh, J. Cadmium-induced apoptosis is mediated by the translocation of AIF to the nucleus in rat testes. Toxicol. Lett. 2009, 188, 45–51.
   PubMed Web of Science ®Google Scholar
• Lafuente, A.; Cano, P.; Esquifino, A.I. Are cadmium effects on plasma gonadotropins, prolactin, ACTH, GH and TSH levels, dose-dependent? BioMetals 2003, 16, 243–250.
   PubMed Web of Science ®Google Scholar
• Lafuente, A.; González-Carracedo, A.; Romero, A.; Cano, P.; Esquifino, A.I. Cadmium exposure differentially modifies the circadian patterns of norepinephrine at the median eminence and plasma LH, FSH and testosterone levels. Toxicol. Lett. 2004, 146, 175–182.
   PubMed Web of Science ®Google Scholar
• Ji, Y.L.; Wang, H.; Liu, P.; Wang, Q.; Zhao, X.F.; Meng, X.H.; Yu, T.; Zhang, H.; Zhang, C.; Zhang, Y.; Xu, D.X. Pubertal cadmium exposure impairs testicular development and spermatogenesis via disrupting testicular testosterone synthesis in adult mice. Reprod. Toxicol. 2010, 29, 176–183.
   PubMed Web of Science ®Google Scholar
• Gunnarsson, D.; Svensson, M.; Selstam, G.; Nordberg, G. Pronounced induction of testicular PGF(2 alpha) and suppression of testosterone by cadmium prevention by zinc. Toxicology 2004, 200, 49–58.
   PubMed Web of Science ®Google Scholar
• Sen Gupta, R.; Kim, J.; Gomes, C.; Oh, S.; Park, J.; Im, W.B.; Seong, J.Y.; Ahn, R.S.; Kwon, H.B.; Soh, J. Effect of ascorbic acid supplementation on testicular steroidogenesis and germ cell death in cadmium-treated male rats. Mol. Cell. Endocrinol. 2004, 221, 57–66.
   PubMed Web of Science ®Google Scholar
• Hecker, M.; Giesy, J.P. Novel trends in endocrine disruptor testing: The H295R steroidogenesis assay for identification of inducers and inhibitors of hormone production. Anal. Bioanal. Chem. 2008, 390(1), 287–291.
   PubMed Web of Science ®Google Scholar
• Gazdar, A.F.; Oie, H.K.; Shackleton, C.H.; Chen, T.R.; Triche, T.J.; Myers, C.E.; Chrousos, G.P.; Brennan, M.F.; Stein, C.A.; La Rocca, R.V. Establishment and characterization of a human adrenocortical carcinoma cell line that expresses multiple pathways of steroid biosynthesis. Cancer Res. 1990, 50(17), 5488–5496.
   PubMed Web of Science ®Google Scholar
• Rainey, W.E.; Saner, K.; Schimmer, B.P. Adrenocortical cell lines. Mol. Cell. Endocrinol. 2004, 228, 23–28.
   PubMed Web of Science ®Google Scholar
• Hilscherova, K.; Jones, P.D.; Gracia, T.; Newsted, J.L.; Zhang, X.; Sanderson, J.T.; Yu, R.M.K.; Wu, R.S.S.; Giesy, J.P. Assessment of the effects of chemicals on the expression of ten steroidogenic genes in the H295R cell line using real-time PCR. Toxicol. Sci. 2004, 81(1), 78–89.
   PubMed Web of Science ®Google Scholar
• Zhang, X.; Yu, R.M.K.; Jones, P.D.; Lam, G.K.W.; Newsted, J.L.; Gracia, T.; Hecker, M.; Hilscherova, K.; Sanderson, J.T.; Wu, R.S.S.; Giesy, J.P. Quantitative RT-PCR methods for evaluating toxicant-induced effects on steroidogenesis using the H295R cell line. Environ. Sci. Technol. 2005, 39(8), 2777–2785.
   PubMed Web of Science ®Google Scholar
• OECD (Organization for Economic Cooperation and Development). H295R Steroidogenesis Assay, OECD Guideline for the Testing of Chemicals No. 456, Paris, 2011. Available at http://www.oecd-ilibrary.org/environment/test-no-456-h295r-steroidogenesis-assay_9789264122642-en (accessed Sep 2011).
   Google Scholar
• Hecker, M.; Newsted, J.L.; Murphy, M.B.; Higley, E.B.; Jones, P.D.; Wu, R.; Giesy, J.P. Human adrenocarcinoma (H295R) cells for rapid in vitro determination of effects on steroidogenesis: Hormone production. Toxicol. Appl. Pharmacol. 2006, 217, 114–124.
   PubMed Web of Science ®Google Scholar
• Knazicka, Z.; Lukac, N.; Forgacs, Z.; Tvrda, E.; Lukacova, J.; Slivkova, J.; Binkowski, Ł.; Massanyi, P. Effects of mercury on the steroidogenesis of human adrenocarcinoma (NCI-H295R) cell line. J. Environ. Sci. Health Pt. A 2013, 48, 348–353.
   PubMed Web of Science ®Google Scholar
• Mosmann, T. Rapid colorimetric assay for cellular growth and surrival: application to proliferation and cytotoxicity assays. J. Immunol. Methods 1983, 65(1–2), 55–63.
   PubMed Web of Science ®Google Scholar
• Danko, J.; Simon, F.; Artimova, J. Nomina anatomica veterinaria. UVLF: Kosice, Slovak Republic, 2011; 269.
   Google Scholar
• Sanderson, J.T. The steroid hormone biosynthesis pathway as a target for endocrine-disrupting chemicals: Review. Toxicol. Sci. 2006, 94(1), 3–21.
   PubMed Web of Science ®Google Scholar
• Paksy, K.; Rajczy, K.; Forgacs, Z.; Lazar, P.; Bernard, A.; Gati, I.; Kaali, G.S. Effect of cadmium on morphology and steroidogenesis of cultured human ovarian granulosa cells. J. Appl. Toxicol. 1997, 17, 321–327.
   PubMed Web of Science ®Google Scholar
• Nampoothiri, L.P.; Gupta, S. Simultaneous effect of lead and cadmium on granulosa cells: A cellular model for ovarian toxicity. Reprod. Toxicol. 2006, 21, 179–185.
   PubMed Web of Science ®Google Scholar
• Forgacs, Z.; Szivos-Racz, M.; Ocztos, G. Study the effects of hormone disruptors on H295R cell line. In Abstract in Hungarian. XVIII. Primer Prevencios Forum, Budapest, 19 May, 2011. Magyar Onkológia. 2011, 55(3), 220–221. Available at http://huon.hu/2011/55/3/0213/0213a.pdf (accessed June 2011).
   Google Scholar
• Ocztos, G.; Forgacs, Z.; Szivos-Racz, M. H295R Steroidogenesis assay for study endocrine disruptors and reproductive toxicants. In Abstract in Hungarian. Fiatal Higienikusok VII. Fóruma, Esztergom, 26–28 May, 2011. Egeszsegtudomany 2011, 55(2), 132–133. Available at http://egeszsegtudomany.higienikus.hu/cikk/2011-2/2011-2.pdf (accessed Aug 2011).
   Google Scholar
• Jolibois, L.S.Jr.; Burow, M.E.; Swan, K.F.; George, W.J.; Anderson, M.B.; Henson, M.C. Effects of cadmium cell viability, trophoblastic development, and expression of low density lipoprotein receptor transcripts in cultured human placental cells. Reprod. Toxicol. 1999, 13, 473–480.
   PubMed Web of Science ®Google Scholar
• Kawai, M.; Swan, K.F.; Green, A.E.; Edwards, D.E.; Anderson, M.B.; Henson, M.C. Placental endocrine disruption induced by cadmium: effects on P450 cholesterol side-chain cleavage and 3beta-hydroxysteroid dehydrogenase enzymes in cultured human trophoblasts. Biol. Reprod. 2002, 67, 178–183.
   PubMed Web of Science ®Google Scholar
• Piasek, M.; Laskey, J.W. Acute Cd exposure and ovarian steroidogenesis in cycling and pregnant rats. Reprod. Toxicol. 1994, 8, 495–507.
   PubMed Web of Science ®Google Scholar
• Paksy, K.; Varga, B.; Lazar, P. Zinc protection against cadmium-induced infertility in female rats. Effect of zinc and cadmium on the progesterone production of cultured granulosa cells. BioMetals 1997, 10, 27–35.
   PubMed Web of Science ®Google Scholar
• Varga, B.; Zsolnai, B.; Paksy, K.; Naray, M.; Ungvary, G. Age dependent accumulation of cadmium in the human ovary. Reprod. Toxicol. 1993, 7, 225–228.
   PubMed Web of Science ®Google Scholar
• Powlin, S.S.; Keng, P.C.; Miller, R.K. Toxicity of cadmium in human trophoblast cells (JAR choriocarcinoma): role of calmodulin and the calmodulin inhibitor, zaldaride maleate. Toxicol. Appl. Pharmacol. 1997, 144, 225–234.
   PubMed Web of Science ®Google Scholar
• Massanyi, P.; Uhrin, V.; Sirotkin, A.V.; Paksy, K.; Forgacs, Z.; Toman, R.; Kovacik, J. Effects of cadmium on ultrastructure and steroidogenesis in cultured porcine ovarian granulosa cells. Acta Vet. Brno 2000, 69, 101–106.
   Web of Science ®Google Scholar
• Veldhuis, J.D.; Klase, P.A.; Demers, L.M.; Chafouleas, J.G. Mechanism subserving calcium´s modulation of luteinizing hormone action in isolated swine granulosa cells. Endocrinol. 1984, 114, 441–449.
   PubMed Web of Science ®Google Scholar
• Henson, M.C.; Chedrese, P.J. Endocrine disruption by cadmium, a common environmental toxicant with paradoxical effects on reproduction. Exp. Biol. Med. (Maywood) 2004, 229, 383–392.
   PubMed Web of Science ®Google Scholar
• Smida, A.D.; Valderrama, X.P.; Agostini, M.C.; Furlan, M.A.; Chendrese, J. Cadmium stimulates transcription of the cytochrome P450 side chain cleavage gene in genetically modified stable porcine granulosa cells. Biol. Reprod. 2004, 70, 25–31.
   PubMed Web of Science ®Google Scholar
• Terracio, L.; Nachtigal, M. Oncogenecity of rat prostate cells transformed in vitro with cadmium chloride. Arch. Toxicol. 1988, 61, 450–456.
   PubMed Web of Science ®Google Scholar
• Beyersmann, D.; Hechtenburg, S. Cadmium, gene regulation, and cellular signaling in mammalian cells. Toxicol. Appl. Pharmacol. 1997, 144, 247–261.
   PubMed Web of Science ®Google Scholar
• Laskey, J.W.; Phelps, P.V. Effect of cadmium and other metal cations on in vitro Leydig cell testosterone production. Toxicol. Appl. Pharmacol. 1991, 108, 296–306.
   PubMed Web of Science ®Google Scholar
• Zeng, X.; Jin, T.; Ahou, Y.; Nordberg, G.F. Changes of serum sex hormone levels and MT mRNA expression in rats orally exposed to cadmium. Toxicology 2003, 186, 109–118.
   PubMed Web of Science ®Google Scholar
• Davidson, J.S.; Franco, S.E.; Millar, R.P. Stimulation by Mn2+ and inhibition by Cd2+, Zn2+, Ni2+ and Co2+ ions of luteinizing hormone exocytosis at an intracellular site. Endocrinol. 1993, 132(6), 2654–2658.
   PubMed Web of Science ®Google Scholar
• Lafuente, A.; Marquez, N.; Piquero, S.; Esquifino, A.I. Cadmium affects the episodic luteinizing hormone secretion in male rats: possible age-dependent effects. Toxicol. Lett. 1999, 104, 27–33.
   PubMed Web of Science ®Google Scholar
• Lafuente, A.; Marquez, N.; Perez-Lorenzo, M.; Pazo, D.; Esquifino, A.I. Pubertal and postpubertal cadmium exposure differentially affects the hypothalamic-pituitary-testicular axis function in the rat. Food Chem. Toxicol. 2000, 38, 913–923.
   PubMed Web of Science ®Google Scholar
• Clark, J.I.; Jimenez, B.; Evans, S.L.; Barrow, R.; Winfree, M.; Mrotek, J.J. Cadmium-induced sexual dysfunction does not in vivo increased hepatic metabolism of testosterone nor increased circulating levels of corticosterone. Physiol. Behav. 1994, 56, 975–981.
   PubMed Web of Science ®Google Scholar
• Laskey, J.W.; Rehnberg, G.L.; Laws, S.C.; Hein, J.F. Reproductive effects of low acute doses of cadmium chloride in adult male rats. Toxicol. Appl. Pharmacol. 1984, 73, 250–255.
   PubMed Web of Science ®Google Scholar
• Singhal, R.L.; Merali, Z.; Hardina, P.D. Aspects of the biochemical toxicology of cadmium. Fed. Proc. 1976, 35, 75–80.
   PubMedGoogle Scholar
• Han, X.Y.; Xu, Z.R.; Wang, Y.Z.; Du, W.L. Effects of cadmium on serum sex hormone levels in pigs. J. Anim. Physiol. Anim. Nutr. 2006, 90, 380–384.
   PubMed Web of Science ®Google Scholar
• Piasek, M.; Schonwald, N.; Blanusa, M.; Kostial, K.; Laskey, J.W. Biomarkers of heavy metal reproductive effects and interaction with essential elements in experimental studies on female rats. Arh. Hig. Rada. Toksikol. 1996, 47, 245–259.
   PubMedGoogle Scholar
• Piasek, M.; Laskey, J.W. Effects of in vitro cadmium exposure on ovarian steroidogenesis in rats. J. Appl. Toxicol. 1999, 19, 211–217.
   PubMed Web of Science ®Google Scholar
• Stoica, A.; Katzenellenbogen, B.S.; Martin, M.B. Activation of estrogen receptor alpha by the heavy metal cadmium. Mol. Endocrinol. 2000, 14, 545–553.
   PubMed Web of Science ®Google Scholar
• Byrne, C.; Divekar, S.D.; Storchan, G.B.; Parodi, D.A.; Martin, M.B. Cadmium – a metalllohormone? Toxicol. Appl. Pharmacol. 2009, 238, 266–271.
   PubMed Web of Science ®Google Scholar
• Garcia-Morales, P.; Saceda, M.; Kenney, N.; Kim, N.; Saloman, D.S.; Gottardis, M.M.; Soloman, H.B.; Sholler, P.F.; Jordan, V.C.; Martin, M.B. Effect of cadmium on estrogen receptor levels and estrogen-induced responses in human breast cancer cells. J. Biol. Chem. 1994, 269, 16896–16901.
   PubMed Web of Science ®Google Scholar
• Martinez-Campa, C.; Alonso-Gonzalez, C.; Mediavilla, M.D.; Cos, S.; Gonzalez, A.; Ramos, S.; Sanchez-Barcelo, E.J. Melatonin inhibits both ER alpha activation and breast cancer cell proliferation induced by a metalloestrogen, cadmium. J. Pineal. Res. 2006, 40, 291–296.
   PubMed Web of Science ®Google Scholar
• Brama, M.; Gnessi, L.; Basciani, S.; Cerulli, N.; Politi, L.; Spera, G.; Mariani, S.; Cherubini, S.; d’Abusco, A.S.; Scandurra, R.; Migliaccio, S. Cadmium induces mitogenic signaling in breast cancer cell by an ERalpha dependent mechanism. Mol. Cell. Endocrinol. 2007, 264, 102–108.
   PubMed Web of Science ®Google Scholar
• Martin, M.B.; Voeller, H.J.; Gelmann, E.P.; Lu, J.; Stoica, E.G.; Hebert, E.J.; Reiter, R.; Singh, B.; Danielsen, M.; Pentecost, E.; Stoica, A. Role of cadmium in the regulation of AR gene expression and activity. Endocrinol. 2002, 143, 263–275.
   PubMed Web of Science ®Google Scholar
• Coin, P.G.; Stevens, J.B. Toxicity of cadmium chloride in vitro: indices of cytotoxicity with the pulmonary alveolar macrophages. Toxicol. Appl. Pharmacol. 1986, 82, 140–150.
   PubMed Web of Science ®Google Scholar
• Nakatsuru, S.; Oohashi, J.; Nozaki, H.; Nakada, S.; Imura, N. Effect of mercurials on lymphocyte functions in vitro. Toxicology 1985, 36, 297–305.
   PubMed Web of Science ®Google Scholar
• Borenfreund, E.; Puerner, J.A. Cytotoxicity of metals, metalmetal and metal-chelator combinations assayed in vitro. Toxicology 1986, 39, 121–134.
   PubMed Web of Science ®Google Scholar
• Kunimoto, N.; Mirua, T.; Kubota, K. An apparent acceleration of age-related changes of rat red blood cells by cadmium. Toxicol. Appl. Pharmacol. 1985, 77, 451–457.
   PubMed Web of Science ®Google Scholar
• Tan, E.L.; Williams, M.W.; Schenley, R.L.; Perdue, S.W.; Hayden, T.L.; Turner, J.E.; Hsie, A.W.A. The toxicity of sixteen metallic compounds in Chinese hamster ovary cells. Toxicol. Appl. Pharmacol. 1984, 74, 330–336.
   PubMed Web of Science ®Google Scholar
• Nishiyama, S.; Nakamura, K. Stimulation of adrenal DNA synthesis in cadmium-treated male rats. Toxicol. Appl. Pharmacol. 1984, 74, 337–344.
   PubMed Web of Science ®Google Scholar
• Nishiyama, S.; Nakamura, K.; Ogawa, M. Effects of heavy metals on corticosteroid production in cultured rat adrenocortical cells. Toxicol. Appl. Pharmacol. 1985, 81, 174–176.
   PubMed Web of Science ®Google Scholar
• Tchounwou, P.B.; Ishaque, A.B.; Schneider, J. Cytotoxicity and transcriptional activation of stress genes in human liver carcinoma cells (HepG2) exposed to cadmium chloride. Mol. Cell. Biochem. 2001, 222, 21–28.
   PubMed Web of Science ®Google Scholar
• Ng, T.B.; Liu, W.K. Toxic effect of heavy metals on cells isolated from the rat adrenal and testis. In Vitro Cell Dev. Biol. 1990, 26(1), 24–28.
   PubMed Web of Science ®Google Scholar