Endocrine Disruption by Cadmium, a Common Environmental Toxicant with Paradoxical Effects on Reproduction

Experimental Biology and Medicine

Volumn 229, Issue 5, 2004, Pages 383-392

  Henson, Michael C ^a   Chedrese, P Jorge ^b  

^a TULANE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^b UNIVERSITY OF SASKATCHEWAN   (Canada)

Author keywords

Cadmium; Placenta; Stable granulosa cells; Steroidogenesis; Toxicology

Indexed keywords

8 BROMO CYCLIC AMP; AMINOGLUTETHIMIDE; CADMIUM; CADMIUM CHLORIDE; CHOLESTEROL; CHOLESTEROL MONOOXYGENASE (SIDE CHAIN CLEAVING); ENDOCRINE DISRUPTOR; ESTROGEN; LOW DENSITY LIPOPROTEIN RECEPTOR; MESSENGER RNA; PREGNENOLONE; PROGESTERONE; UNCLASSIFIED DRUG; ZINC;

CIRCULATION; CONTROLLED STUDY; CORPUS LUTEUM FUNCTION; DNA BINDING; ENDOCRINE DISEASE; ENVIRONMENTAL EXPOSURE; ENVIRONMENTAL FACTOR; FEMALE; HUMAN; INHIBITION KINETICS; METAL METABOLISM; MORPHOLOGICAL TRAIT; OVARY; PLACENTA; PROGESTERONE METABOLISM; REGULATORY MECHANISM; REPRODUCTIVE TOXICITY; SHORT SURVEY; SMOKING; STATISTICAL SIGNIFICANCE; STEROIDOGENESIS; TISSUE SPECIFICITY; TOBACCO; TOXICITY TESTING; ZINC FINGER MOTIF;

MAMMALIA; NICOTIANA TABACUM; SUIDAE;

EID: 2142714539     PISSN: 15353702     EISSN: None     Source Type: Journal    
DOI: 10.1177/153537020422900506     Document Type: Short Survey

References (93)

1. Bhattacharyya MH, Wilson AK, Rajan SS, Jonah M. Biochemical pathways in cadmium toxicity. In: Zalup RK, Koropatnick J, Eds. Molecular Biology and Toxicology of Metals. London: Taylor and Francis, pp1-74, 2000.
2. Jarup L, Berglund M, Elinder CG, Nordberg G, Vahter M. Health effects of cadmium exposure - a review of the literature and risk estimate. Scand J Work Environ Health 24(Suppl 1):1-52, 1998.
3. Zadorozhnaja TD, Little RE, Miller RK, Mendel NA, Taylor RJ, Presley BJ, Gladen BC. Concentrations of arsenic, cadmium, copper, lead, mercury, and zinc in human placentas from two cities in Ukraine. J Toxicol Environ Health 61:255-263, 2000.
4. Zenzes MT, Krishnan S, Krishnan B, Zhang H, Casper RF. Cadmium accumulation in follicular fluid of women in vitro fertilization-embryo transfer is higher in smokers. Fertil Steril 64:599-603, 1995.
5. Henson MC, Anderson MB. The effects of cadmium on placental endocrine function. Recent Res Dev Endocrinol 1:37-47, 2000.
6. Massanyi P, Uhrin V, Sirolkin AV, Paksy K, Forgács ZS, Toman R, Kovačik J. Effects of cadmium on ultrastructure and steroidogenesis in cultured porcine ovarian granulosa cells. Acta Vet Brno 69:101-106, 2000.
7. Varga B, Zsolnai B, Paksy K, Náray M, Ungváry GY. Age dependent accumulation of cadmium in the human ovary. Reprod Toxicol 7:225-228, 1993.
8. Piasek M, Blanusa M, Kostial K, Laskey JW. Placental cadmium and progesterone concentrations in cigarette smokers. Reprod Toxicol 15:673-681, 2001.
9. Fiala J, Hrubá D, Crha I, Rézl P, Totušek J. Is environmental cadmium a serious hazard to Czech population? Int J Occup Med Environ Health 14:185-188, 2001.
10. Paksy K, Rajczy K, Forgács Z, Lázár P, Bernard A, Gáti I, Kaáli GS. Effect of cadmium on morphology and steroidogenesis of cultured human ovarian granulosa cells. J Appl Toxicol 17:321-327, 1997.
11. Satoh M, Koyama H, Kaji T, Kito H, Tohyama C. Perspectives on cadmium research. Tohoku J Exp Med 196:23-32, 2002.
12. Moon C-S, Paik J-M, Choi C-S, Kim D-H, Ikeda M. Lead and cadmium levels in daily foods, blood and urine in children and their mothers in Korea. Int Arch Occup Environ Health 76:282-288, 2003.
13. Nishijo M, Nakagawa H, Honda R, Tanebe K, Saito S, Teranishi H, Tawara K. Effects of maternal exposure to cadmium on pregnancy outcome and breast milk. Occup Environ Med 59:394-397, 2002.
14. Sisman AR, Bulbul M, Coker C, Onvural B. Cadmium exposure in tobacco workers: possible renal effects. J Trace Elem Med Biol 17: 51-55, 2003.
15. Satarug S, Baker JR, Reilly PE, Moore MR, Williams DJ. Changes in zinc and copper homeostasis in human livers and kidneys associated with exposure to environmental cadmium. Hum Exp Toxicol 20:205-213, 2001.
16. Piasek M, Kostial K, Laskey JW. Experimental studies on reproductive and perinatal effects of lead and cadmium. Environ Mgmt Health 7:29-32, 1996.
17. Bush PG, Mayhew TM, Abramovich DR, Aggett PJ, Burke MD, Page KR. A quantitative study on the effects of maternal smoking on placental morphology and cadmium concentration. Placenta 21:247-256, 2000.
18. Mielke HW, Gonzales CR, Smith MK, Mielke PW. The urban environment and children's health: soils as an integrator of lead, zinc, and cadmium in New Orleans, Louisiana, USA. Environ Res Sec A 81:117-129, 1999.
19. Galicia-Garcia V, Rojas-Lopez M, Rojas R, Olaiz G, Rios C. Cadmium levels in maternal, cord and newborn blood in Mexico City. Toxicol Lett 91:57-61, 1997.
20. Lafuente A, Cano P, Esquilino AI. Are cadmium effects on plasma gonadotropins, prolactin, ACTH, GH and TSH levels, dose-dependent? Biometals 16:243-250, 2003.
21. Piasek M, Laskey JW. Acute cadmium exposure and ovarian steroidogenesis in cycling and pregnant rats. Reprod Toxicol 8:495-507, 1994.
22. Piasek M, Laskey JW. Effects of in vitro exposure on ovarian steroidogenesis in rats. J Appl Toxicol 19:211-217, 1999.
23. Magers T, Talbot P, DiCarlantonio G, Knoll M, Demers D, Tsai I, Hoodbhoy T. Cigarette smoke inhalation affects the reproductive system of female hamsters. Reprod Toxicol 9:513-525, 1995.
24. Jolibois LS Jr., Shi W, George WJ, Henson MC, Anderson MB. Cadmium accumulation and effects on progesterone release by cultured human trophoblast cells. Reprod Toxicol 13:215-221, 1999.
25. Jolibois LS Jr., Burow ME, Swan KF, George WJ, Anderson MB, Henson MC. Effects of cadmium on cell viability, trophoblastic development, and expression of low density lipoprotein receptor transcripts in cultured human placental cells. Reprod Toxicol 13:473-480, 1999.
26. Kawai M, Swan KF, Green AE, Edwards DE, Anderson MB, Henson MC. Placental endocrine disruption induced by cadmium: effects on P450 cholesterol side-chain cleavage and 3β-hydroxysteroid dehydrogenase enzymes in cultured human trophoblasts. Biol Reprod 67:178-183, 2002.
27. Paksy K, Varga B, Lázár P. Zinc protection against cadmium-induced infertility in female rats. Effect of zinc and cadmium on the progesterone production of cultured granulosa cells. Biometals 10:27-35, 1996.
28. Powlin SS, Keng PC, Miller RK. Toxicity of cadmium in human trophoblast cells (JAr choriocarcinoma): role of calmodulin and the calmodulin inhibitor, zaldaride maleate. Toxicol Appl Pharmacol 144:225-234, 1997.
29. Chedrese PJ, Rodway MR, Swan CL, Gillio-Meina C. Establishment of a stable steroidogenic porcine granulosa cell line. J Molec Endocrinol 20:287-292, 1998.
30. Urban RJ, Shupnik MA, Bodenburg YH. Insulin-like growth factor-1 increases expression of the porcine P-450 cholesterol side chain cleavage gene through a GC-rich domain. J Biol Chem 269:25761-25769, 1994.
31. scc. J Biol Chem 264:21934-21942, 1989.
32. Smida AD, Valderrama XP, Agostini MC, Furlan MA, Chedrese PJ. Cadmium stimulates transcription of the cytochrome P450 side chain cleavage gene in genetically modified stable porcine granulosa cells. Biol Reprod 70:25-31, 2004.
33. Rodway MR, Swan CL, Crellin NK, Gillio-Meina C, Chedrese PJ. Steroid regulation of progesterone synthesis in a stable porcine granulosa cell line: a role for progestins. J Steroid Biochem Molec Biol 68:173-180, 1999.
34. Kuhnert BR, Kuhnert PM, Zarlingo TJ. Associations between placental cadmium and zinc and age and parity in pregnancy women who smoke. Obstet Gynecol 71:67-70, 1988.
35. Frery N, Nessmann C, Girard F, Lafond J, Moreau T, Blot P, Lellouch J, Huel G. Environmental exposure to cadmium and human birthweight. Toxicology 79:109-118, 1993.
36. Shiverick KT, Salafia C. Cigarette smoking and pregnancy 1: ovarian, uterine and placental effects. Placenta 20:265-272, 1999.
37. Wier PJ, Miller RK. The pharmacokinetics of cadmium in the dually perfused human placenta. Trophoblast Res 2:357-366, 1987.
38. Boadi WY, Yannai S, Urbach J, Brandes JM, Summer KH. Transfer and accumulation of cadium, and the level of metallothionein in perfused human placentae. Arch Toxicol 65:318-323, 1991.
39. Piasek M, Laskey JW, Kostial K, Blanusa M. Assessment of steroid disruption using cultures of whole ovary and/or placenta in rat and in human placental tissue. Int Arch Occup Environ Health 75(Suppl):S36-S44, 2002.
40. Wier PJ, Miller RK, Maulik D, di Sant' Agnese PA. Toxicity of cadmium in the perfused human placenta. Toxicol Appl Pharmacol 105:156-171, 1990.
41. di Sant' Agnese PA, Jensen KD, Levin A, Miller RK. Placental toxicity of cadmium in the rat: an ultrastructural study. Placenta 4:149-163, 1983.
42. Falcone T, Little AB. Placental synthesis of steroid hormones. In: Tulchinsky D, Ryan KJ, Eds. Maternal-Fetal Endocrinology. Philadelphia: W. B. Saunders Company, pp3-16, 1980.
43. Huszar G. Biology of the myometrium and cervix. In: Warsham J. Ed. The Biological Basis of Reproductive and Developmental Medicine. New York: Elsevier Biomedical. pp85-104, 1983.
44. Trottier B, Athot J, Ricard AC, Lafond J. Maternal-fetal distribution of cadmium in the guinea pig following a low dose inhalation exposure. Toxicol Lett 129:189-197, 2002.
45. Egawa M, Yasuda K, Nakajima T, Okada H, Yoshimura T, Yuri T, Yasuhara M, Nakamoto T, Nagata F, Kanzaki H. Smoking enhances oxytocin-induced rhythmic myometrial contraction. Biol Reprod 68:2274-2280, 2003.
46. Cnattingius S, Granath F, Petersson G, Harlow BL. The influence of gestational age and smoking habits on the risk of subsequent preterm deliveries. N Engl J Med 341:943-948, 1999
47. Hanke W, Kalinka J, Florek E, Sobala W. Passive smoking and pregnancy outcome in central Poland. Hum Exp Toxicol 18:265-271, 1999.
48. Ahern J, Pickett KE, Selvin S, Abrams B. Preterm birth among African American and white women: a multilevel analysis of socioeconomic characteristics and cigarette smoking. J Epidemiol Community Health 57:606-611, 2003.
49. Phung H, Bauman A, Nguyen TV, Young L, Tran M, Hillman K. Risk factors for low birth weight in a socio-economically disadvantaged population: parity, marital status, ethnicity and cigarette smoking. Eur J Epidemiol 18:235-243, 2003.
50. Ventura SJ, Hamilton BE, Mathews TJ, Chandra A. Trends and variations in smoking during pregnancy and low birth weight: evidence from the birth certificate, 1990-2000. Pediatrics 111:1176-1180, 2003.
51. Dejmek J, Solansky I, Podrazilova K, Sram RJ. The exposure of nonsmoking and smoking mothers to environmental tobacco smoke during different gestational phases and fetal growth. Environ Health Perspect 110:601-606, 2002.
52. Miller WL. Molecular biology of steroid hormone synthesis. Endocr Rev 9:295-318, 1988.
53. Ringler G, Strauss JF III. In vitro systems for the study of human placental endocrine function. Endocr Rev 11: 105-123, 1990.
54. Henson MC, Shi W, Greene SJ, Reggio BC. Effects of pregnant human, nonpregnant human, and fetal bovine sera on human chorionic gonadotropin, estradiol, and progesterone release by cultured human trophoblast cells. Endocrinology 137:2067-2074, 1996.
55. Richards RG, Hartman SM, Handwerger S. Human cytotrophoblast cells cultured in maternal serum progress to a differentiated syncytial phenotype expressing both human chorionic gonadotropin and human placental lactogen. Endocrinology 135:321-329, 1994.
56. Hinkle PM, Osbourne ME. Cadmium toxicity in rat pheochromocytoma cells: studies on the mechanism of uptake. Toxicol App Pharmacol 124:91-98, 1994.
57. Blazka ME, Shaikh ZA. Differences in cadmium and mercury uptakes by hepatocytes: role of calcium channels. Toxicol Appl Pharmacol 110:355-363, 1991.
58. 2+-induced c-myc mRNA accumulation in NRK-49F cells is blocked by protein kinase inhibitor H7 but not by HA1004, indicating that protein kinase C is a mediator of the response. Toxicology 81:155-164, 1993.
59. Nishizuka Y. Studies and prospectives of protein kinase C. Science 233:305-312, 1986.
60. Long GJ. The effect of cadmium on cytosolic free calcium, protein kinase C, and collagen synthesis in rat osteosarcoma (ROS 17/2.8) cells. Toxicol Appl Pharmacol 143:189-195, 1997.
61. 2+-ATPase activity by cadmium, lead and mercury. Enzyme 45:109-115, 1991.
62. Misra UK, Gawdi G, Akabani G, Pizzo SV. Cadmium-induced DNA synthesis and cell proliferation in macrophages: the role of intracellular calcium and signal transduction mechanisms. Cell Signal 14:327-340, 2002.
63. Smith JB, Dwyer SD, Smith L. Cadmium evokes inositol polyphosphate formation and calcium mobilization: evidence for a cell surface receptor that cadmium stimulates and zinc antagonizes. J Biol Chem 264:7115-7118, 1989.
64. Jayes FCL, Day RN, Garmey JC, Urban RJ, Zhang G, Veldhuis JD. Calcium ions positively modulate follicle-stimulating hormone- and exogenous cyclic 3′, 5′-adenosine monophosphate-driven transcription of the P450scc gene in porcine granulosa cells. Endocrinology 141:2377-2384, 2000.
65. t cells. Kidney Int 48:383-389, 1995.
66. Hoeffler JP, Meyer TE, Yun Y, Jameson JL, Habener JF. Cyclic AMP-responsive DNA-binding protein: structure based on a cloned placental cDNA. Science 242:1430-1433, 1988.
67. Albright SR, Tjian R. TAFs revisited: more data reveal new twists and confirm old ideas. Gene 242:1-13, 2000.
68. Goyer R. Toxic effects of metals. In: Amdur M, Doull J, Klassen C, Eds. Toxicology: The basic science of poisons. New York: Macmillan, pp623-680, 1991.
69. Mellon SH, Vaisse C. cAMP regulates P450scc gene expression by a cycloheximide-insensitive mechanism in cultured mouse Leydig MA-10 cells. Proc Natl Acad Sci U S A 86:7775-7779, 1989.
70. Brentano ST, Miller WL. Regulation of human cytochrome P450scc and adrenodoxin mRNAs in JEG-3 cytotrophoblast cells. Endocrinology 131:3010-3018, 1992.
71. Ringler GE, Kao L-C, Miller WL, Strauss JF III. Effects of 8-bromo-cAMP on expression of endocrine functions by cultured human trophoblast cells: regulation of specific mRNAs. Mol Cell Endocrinol 61:13-21, 1989.
72. Little B, Billiar RB, Halla M, Heinsons A, Jassani M, Kline IT, Purdy RH. Pregnenolone production in pregnancy. Am J Obstet Gynecol 111:505-514, 1971.
73. Beaudoin C, Blomquist CH, Bonenfant M, Tremblay Y. Expression of the genes for 3β-hydroxysteroid dehydrogenase type 1 and cytochrome P450scc during syncytium formation by human placental cytotrophoblast cells in culture and the regulation by progesterone and estradiol. J Endocrinol 154:379-387, 1997.
74. Orly J, Rei Z, Greenberg NM, Richards JS. Tyrosine kinase inhibitor AG18 arrests FSH-induced granulosa cell differentiation: use of RT-PCR assay for multiple mRNA. Endocrinology 134:2336-2346, 1994.
75. Chung BC, Matteson KJ, Voutilainen R, Mohandas TK, Miller WL. Human cholesterol side-chain cleavage enzyme, P450scc: cDNA cloning, assignment of the gene to chromosome 15, and expression in the placenta. Proc Natl Acad Sci U S A 83:8962-8966, 1986.
76. Inoue H, Higashi Y, Morohashi K, Fujii-Kuriyama Y. The 5′-flanking region of the human P450(SCC) gene shows responsiveness to cAMP-dependent regulation in a transient gene-expression system of Y-1 adrenal tumor cells. Eur J Biochem 171:435-440, 1988.
77. Moore CC, Hum DW, Miller WL. Identification of positive and negative placenta-specific basal elements and a cAMP response element in the human gene for P450scc. Mol Endocrinol 6:2045-2058, 1992.
78. Kostrzewska A, Sobieszek A. Diverse actions of cadmium on the smooth muscle myosin phosphorylation system. FEBS Lett 263:381-384, 1990.
79. Sunderman FW Jr., Barber AM, Finger-loops, oncogenes and metals. Ann Clin Lab Sci 18:267-288, 1988.
80. Vallee BL, Ulmer DD. Biochemical effects of mercury, cadmium and lead. Ann Rev Biochem 41:91-128, 1972.
81. Jacobson KB, Turner JE. The interaction of cadmium and certain other metal ions with proteins and nucleic acids. Toxicology 16:1-37, 1980.
82. Borgeest C, Greenfield C, Tomic D, Flaws JA. The effects of endocrine disrupting chemicals on the ovary. Front Biosci 7:d1941-d1948, 2002.
83. Guillette LJ, Crain DA, Gunderson MP, Kools SAE, Milnes MR, Orlando EF, Rooney AA, Woodward AR. Alligators and endocrine disrupting contaminants: a current perspective. Am Zool 40:438-452, 2002.
84. Garcia-Morales P, Saceda M, Kenney N, Salomon DS, Kim N, Salomon DS, Gottardis MM, Solomon HB, Sholler PF, Jordan VC, Martin MB. Effect of cadmium on estrogen receptor levels and estrogen-induced responses in human breast cancer cells. J Biol Chem 269:16896-16901, 1994.
85. Martin BM, Reiter R, Pham T, Avellanet YR, Camara J, Lahm M, Pentecost E, Pratap K, Gilmore BA, Diverakar S, Dagata RS, Bull JL, Stoica A. Estrogen-like activity of metals in MCF-7 breast cancer cells. Endocrinology 144:2425-2436, 2003.
86. Johnson MD, Kenney N, Stoica A, Hillakivi-Clarke L, Singh B, Chepko G, Clarke R, Sholler PF, Lirio AA, Foss C, Reiter R, Trock B, Paik S, Martin MB. Cadmium mimics the in vivo effects of estrogen in the uterus and mammary gland. Nat Med 9:1081-1084, 2003.
87. Stoica A, Katzenellenbogen BS, Martin MB. Activation of estrogen receptor-alpha by the heavy metal cadmium. Mol Endocrinol 14:545-553, 2000.
88. Ng TB, Liu WK. Toxic effect of heavy metals on cells isolated from the rat adrenal and testis. In Vitro Cell Dev Biol 26:24-28, 1990.
89. Mgbonyebi OP, Smothers CT, Mrotek JJ. Modulation of adrenal cell functions by cadmium salts: 1. Cadmium chloride effects on basal and ACTH-stimulated steroidogenesis. Cell Bio Toxicol 9:223-234, 1993.
90. Terracio L, Nachtigal M. Oncogenicity of rat prostate cells transformed in vitro with cadmium chloride. Arch Toxicol 61:450-456, 1988.
91. Beyersmann D, Hechtenburg S. Cadmium, gene regulation, and cellular signaling in mammalian cells. Toxicol Appl Pharmacol 144:247-261, 1997.
92. Waalkes MP, Misra RR. In: Chang LW, Ed. Toxicology of Metals. Boca Raton: CRC Press. p 231, 1996.
93. Kondoh M, Araragi S, Sato K, Higashimoto M, Takiguchi M, Sato M. Cadmium induces apoptosis partly via caspase-9 activation in HL-60 cells. Toxicology 170:111-117, 2002.