Cadmium a metalloestrogen: Are we convinced?

Journal of Applied Toxicology

Volumn 32, Issue 5, 2012, Pages 318-332

  Silva, Nalinda ^a   Peiris John, Roshini ^b   Wickremasinghe, Rajitha ^c   Senanayake, Hemantha ^d   Sathiakumar, Nalini ^e  

^a UNIVERSITY OF SRI JAYEWARDENEPURA   (Sri Lanka)

^b UNIVERSITY OF AUCKLAND   (New Zealand)

^c UNIVERSITY OF KELANIYA   (Sri Lanka)

^d UNIVERSITY OF COLOMBO   (Sri Lanka)

^e UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

Cadmium; Metalloestrogens; Oestrogen

Indexed keywords

ASPARTIC ACID; CADMIUM; CYSTEINE; ESTRADIOL; ESTROGEN DERIVATIVE; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; FOLLITROPIN; G PROTEIN COUPLED RECEPTOR 30; GLUTAMIC ACID; HISTIDINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; METALLOESTROGEN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MYC PROTEIN; PROGESTERONE RECEPTOR; PROTEIN C FOS; PROTEIN C JUN; PROTEIN KINASE B; TELOMERASE REVERSE TRANSCRIPTASE; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR GAL4; TREFOIL FACTOR 1; TREFOIL PEPTIDE; UNCLASSIFIED DRUG;

ADENOHYPOPHYSIS; BLOOD LEVEL; BREAST CANCER; BREAST DEVELOPMENT; CANCER GROWTH; CANCER PROGNOSIS; CANCER RISK; CELL MEMBRANE; CELL MIGRATION; CELL PROLIFERATION; CELLULAR DISTRIBUTION; DISEASE ASSOCIATION; DNA SYNTHESIS; DOWN REGULATION; ENDOMETRIOSIS; ENDOMETRIUM; ENZYME PHOSPHORYLATION; ESTRADIOL BLOOD LEVEL; ESTROGEN ACTIVITY; ESTROGEN RESPONSIVE ELEMENT; GENE EXPRESSION REGULATION; HUMAN; HYPOTHALAMUS HYPOPHYSIS GONAD SYSTEM; INTRACELLULAR SIGNALING; LIGAND BINDING DOMAIN; MAMMARY GLAND; NONHUMAN; ORGAN WEIGHT; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; REVIEW; TISSUE LEVEL; TRANSCRIPTION REGULATION; UPREGULATION; URINE LEVEL; UTERUS MYOMA;

ANIMALS; BREAST; BREAST NEOPLASMS; CADMIUM; CHICK EMBRYO; ESTROGENS; FEMALE; HUMANS; METALS, HEAVY; MICE; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, ESTROGEN; TUMOR CELLS, CULTURED;

EID: 84858865247     PISSN: 0260437X     EISSN: 10991263     Source Type: Journal    
DOI: 10.1002/jat.1771     Document Type: Review

References (72)

1. Agency for Toxic Substances and Disease Registry. 2008. Draft Toxicological Profile for Cadmium. ATSDR: Atlanta, GA; Chapter 6.
2. Åkesson A, Julin B, Wolk A. 2008. Long-term dietary cadmium intake and postmenopausal endometrial cancer incidence: a population-based prospective cohort study. Cancer Res. 68(15): 6435-6441.
3. Ali I, Penttinen-Damdimopoulou PE, Mäkelä SI, Berglund M, Stenius U, Åkesson A, Håkansson H, Halldin K. 2010. Estrogen-like effects of cadmium in vivo do not appear to be mediated via the classical estrogen receptor transcriptional pathway. Environ. Health Perspect. 118(10): 1389-1394.
4. Alonso-González C, González A, Mazarrasa O, Güezmes A, Sánchez-Mateos S, Martínez-Campa C, Cos S, Sánchez-Barceló EJ, Mediavilla MD. 2007. Melatonin prevents the estrogenic effects of sub-chronic administration of cadmium on mice mammary glands and uterus. J. Pineal Res. 42: 403-410.
5. Antila E, Mussalo-Rauhamaa H, Kantola M, Atroshi F, Westermarck T. 1996. Association of cadmium with human breast cancer. Sci. Total Environ. 186: 251-256.
6. Ariazi EA, Brailoiu E, Yerrum S, Shupp HA, Slifker MJ, Cunliffe HE, Black MA, Donato AL, Arterburn JB, Oprea TI, Prossnitz ER, Dun NJ, Jordan VC. 2010. The G protein-coupled receptor GPR30 inhibits proliferation of estrogen receptor-positive breast cancer cells. Cancer Res. 70(3): 1184-1194.
7. Barrett KE, Barman SM, Boitano S, Brooks HL. 2003. The gonads: development & function of the reproductive system. In Ganong's Review of Medical Physiology. Lange: USA; Chapter 25.
8. Benbrahim-Tallaa L, Tokar EJ, Diwan BA, Dill AL, Coppin J-F, Waalkes MP. 2009. Cadmium malignantly transforms normal human breast epithelial cells into a basal-like phenotype. Environ. Health Perspect. 117(12): 1847-1852.
9. Beyersmann D, Hartwig A. 2008. Carcinogenic metal compounds: recent insight into molecular and cellular mechanisms. Arch. Toxicol. 82: 493-512.
10. Bjornstrom L, Sjoberg M. 2005. Mechanisms of estrogen receptor signaling: convergence of genomic and nongenomic actions on target genes. Mol. Endocrinol. 19(4): 833-842.
11. Brama M, Gnessi L, Basciani S, Cerulli N, Politi L, Spera G, Mariani S, Cherubini S, d'Abusco AS, Scandurra R, Migliaccio S. 2007. Cadmium induces mitogenic signaling in breast cancer cell by an ER alpha-dependent mechanism. Mol. Cell. Endocrinol. 264: 102-108.
12. Bridges CC, Zalups RK. 2005. Molecular and ionic mimicry and the transport of toxic metals. Toxicol. Appl. Pharmacol. 204: 274-308.
13. Brzozowski AM, Pike ACW, Dauter Z, Hubbard RE, Bonn T, Engstro O, Hman LO, Greene GL, Gustafsson JAK, Carlquist M. 1997. Molecular basis of agonism and antagonismin the oestrogen receptor. Nature 389(16): 753-758.
14. Buffet NC, Djakoure C, Maitre SC, Bouchard P. 1998. Regulation of the human menstrual cycle. Front. Neuroendocrinol. 19(3): 151-186.
15. Cantor KP, Stewart PA, Brinton LA, Dosemeci M. 1994. Occupational exposures and female breast cancer mortality in the United States. J. Occup. Med. 37: 336-348.
16. Choea S-Y, Kima S-J, Kima H-G, Leeb JH, Choib Y, Leeb H, Kimb Y. 2003. Evaluation of estrogenicity of major heavy metals. Sci. Total Environ. 312: 15-21.
17. Couse JF, Yates MM, Walker VR, Korach KS. 2003. Characterization of the hypothalamic-pituitary-gonadal axis in estrogen receptor (ER) null mice reveals hypergonadism and endocrine sex reversal in females lacking ER alpha but not ERbeta. Mol. Endocrinol. 17(6): 1039-1053.
18. Darbre PD. 2005. Aluminium, antiperspirants and breast cancer. J. Inorg. Biochem. 99: 1912-1919.
19. Darbre PD. 2006a. Environmental oestrogens, cosmetics and breast cancer. Baillieres Best Pract. Res. Clin. Endocrinol. Metab. 20(1): 121-143.
20. Darbre PD. 2006b. Metalloestrogens: an emerging class of inorganic xenoestrogens with potential to add to the oestrogenic burden of the human breast. J. Appl. Toxicol. 26(191): 197.
21. Davis DL, Bradlow HL, Wolff M, Woodruff T, Hoel DG, Anton-Culver H. 1993. Medical hypothesis: xenoestrogens as preventable causes of breast cancer. Environ. Health Perspect. 101(5): 372-377.
22. DelaIglesia HO, Schwartz WJ. 2006. Timely ovulation: circadian regulation of the female hypothalamo-pituitary-gonadal axis. Endocrinology 147(3): 1148-1153.
23. Eilers M, Eisenman RN. 2008. Myc's broad reach. Genes Dev. 22(20): 2755-2766.
24. Fifield FW, Haines PJ 1995. Environmental Analytical Chemistry. Blackie: London.
25. Filon FL, D'Agostin F, Crosera M, Adami G, Bovenzi M, Maina G. 2009. In vitro absorption of metal powders through intact and damaged human skin. Toxicol. in Vitro 23: 574-579.
26. Flarend R, Bin T, Elmore D, Hemb SL. 2001. A preliminary study of the dermal absorption of aluminium from antiperspirants using Aluminium-26. Food Chem. Toxicol. 39: 163-168.
27. Florea AM, Büsselberg D. 2006. Occurrence, use and potential toxic effects of metals and metal compounds. Bio Metals 19: 419-427.
28. Gallagher CM, Chen JJ, Kovach JS. 2010. Environmental cadmium and breast cancer risk. Aging 2(11): 804-814.
29. Garcia-Morales P, Aceda M, Kenney N, Kims N, Salomon DS, Gottardisn MM, Solomonn HB, Shollern PF, Jordan C, Martin MB. 1994. Effect of cadmium on estrogen receptor levels and estrogen-induced responses in human breast cancer cells. J. Biol. Chem. 269(24): 16896-16901.
30. Giudice LC. 2010. Endometriosis. New Engl. J. Med. 362: 2389-2398.
31. Han XY, Xu ZR, Wang Y, Du WL. 2006. Effects of cadmium on serum sex hormone levels in pigs. J. Animal Physiol. Animal Nutr. 90: 380-384.
32. Heilier JF, Donnez J, Verougstraete V, Donnez O, Grandjean F, Haufroid V, Nackers F, Lison D. 2006. Cadmium, lead and endometriosis. Int. Arch. Occup. Environ. Health 80: 149-153.
33. Heldring N, Pike A, Andersson S, Matthews J, Cheng G, Hartman J, Tujague M, Ström A, Treuter E, Warner M, Gustafsson JA. 2007. Estrogen receptors: how do they signal and what are their targets. Physiol. Rev. 87(3): 905-931.
34. Hewitt SC, Korach KS. 2003. Oestrogen receptor knockout mice: roles for oestrogen receptors alpha and beta in reproductive tissues. Reproduction 125: 143-149.
35. Höfer N, Diel P, Wittsiepe J, Wilhelm M, Degen GH. 2009. Dose- and route-dependent hormonal activity of the metalloestrogen cadmium in the rat uterus. Toxicol. Lett. 191: 123-131.
36. Höfer N, Diel P, Wittsiepe J, Wilhelm M, Kluxen FM, Degen GH. 2010. Investigations on the estrogenic activity of the metallohormone cadmium in the rat intestine. Arch. Toxicol. 84: 541-552.
37. Horst GJ. 2010. Estrogen in the limbic system. Vitam. Horm. 82: 319-338.
38. Itoh H, Iwasaki M, Nakajima Y, Endo Y, Hanaoka T, Sasaki H, Tanaka T, Yang B, Tsugane S. 2008. A case-control study of the association between urinary cadmium concentration and endometriosis in infertile Japanese women. Sci. Total Environ. 402: 171-175.
39. Jackson LW, Zullo MD, Goldberg JM. 2008. The association between heavy metals, endometriosis and uterine myomas among premenopausal women: National Health and Nutrition Examination Survey 1999-2002. Hum. Reprod. 23(3): 679-687.
40. Johnson MD, Kenny N, Stoica A, Hilakivi-Clarke L, Singh B, Chepko G, Clarke R, Sholler PF, Lirio AA, Foss C, Reiter R, Trock B, Paik S, Martin MB. 2003. Cadmium mimics the in vivo effects of estrogen in the uterus and mammary glands. Nat. Med. 9(8): 1081-1084.
41. Johnston SR. 2010. New strategies in estrogen receptor-positive breast cancer. Clin. Cancer Res. 16(7): 1979-1987.
42. Kitawaki J, Kado N, Ishihara H, Koshiba H, Kitaoka Y, Honjo H. 2003. Endometriosis: the pathophysiology as an estrogen-dependent disease. J. Steroid Biochem. Mol. Biol. 83: 149-155.
43. Koninckx PR. 1999. The physiopathology of endometriosis: pollution and dioxin. Gynecol. Obstet. Invest. 47(suppl. 1): 47-50.
44. Kuo J, Hamid N, Bondar G, Prossnitz ER, Micevych P. 2010. Membrane estrogen receptors stimulate intracellular calcium release and progesterone synthesis in hypothalamic astrocytes. J. Neurosci. 30(39): 12950-12957.
45. Le Guével R, Petit FG, Goff PL, Métivier R, Valotaire Y, Pakdel F. 2000. Inhibition of rainbow trout (Oncorhynchus mykiss) estrogen receptor activity by cadmium. Biol. Reprod. 63: 259-266.
46. Levin ER. 2010. Plasma membrane estrogen receptors. Trends Endocrinol. Metab. 20(10): 477-482.
47. Li Y, Wang JP, Santen RJ, Kim TH, Park H, Fan P, Yue W. 2010. Estrogen stimulation of cell migration involves multiple signaling pathway interactions. Endocrinology 151(11): 5146-5156.
48. Liu J, Huang H, Zhang W, Li H. 2010. Cadmium induced increase uterine wet weight and its mechanism. Birth Defects Res. (PtB) 89: 43-49.
49. Madak-Erdogan Z, Kieser KJ, Kim SH, Komm B, Katzenellenbogen JA, Katzenellenbogen BS. 2008. Nuclear and extranuclear pathway inputs in the regulation of global gene expression by estrogen receptors. Mol. Endocrinol. 22: 2116-2127.
50. Martínez-Campa CM, Alonso-González C, Mediavilla MD, González SCA, Sanchez-Barcelo EJ. 2008. Melatonin down-regulates hTERT expression induced by either natural estrogens (17b-estradiol) or metalloestrogens (cadmium) in MCF-7 human breast cancer cells. Cancer Lett. 268: 272-277.
51. Matthews J, Gustafson JA. 2003. Estrogen signaling: a subtle balance between ER-alpha and ER-beta. Mol. Intervent. 3(5): 281-292.
52. McElroy JA, Shafer MM, Trentham-Dietz A, Hampton JM, Newcomb PA. 2006. Cadmium exposure and breast cancer risk. J. Natl. Cancer Inst. 98(12): 869-873.
53. Nasiadek M, Krawczyk T, Sapotal A. 2005. Tissue levels of cadmium and trace elements in patients with myoma and uterine cancer. Hum. Exp. Toxicol. 24: 623-630.
54. Nasiadek M, Swiatkowska E, Nowinska A, Krawczyk T, Wilczynski JR, Sapota A. 2011. The effect of cadmium on steroid hormones and their receptors in women with uterine myomas. Arch. Environ. Contam. Toxicol. 60(4):734-741.
55. Otto C, Rohde-Schulz B, Schwarz G, Fuchs I, Klewer M, Brittain D, Langer G, Bader B, Prelle K, Nubbemeyer R, Fritzemeier K-H. 2008. G protein-coupled receptor 30 localizes to the endoplasmic reticulum and is not activated by estradiol. Endocrinology 149(10): 4846-4856.
56. Piasek M, Laskey JW. 1994. Acute cadmium exposure and ovarian steroidogenesis in cycling and pregnant rats. Reprod. Toxicol. 8(6): 495-507.
57. Pike ACW, Brzozowski AM, Walton J, Hubbard RE, Bonn T, Gustafsson JA, Carlquist< M. 2000. Structural aspects of agonism and antagonism in the oestrogen receptor. Biochem. Soc. Trans. 28(4): 396-400.
58. Sadler AJ, Pugazhendhi D, Darbre PD. 2009. Use of global gene expression patterns in mechanistic studies of oestrogen action in MCF7 human breast cancer cells. J. Steroid Biochem. Mol. Biol. 114(1-2): 21-32.
59. Safe S. 2003. Cadmium disguise dupes the estrogen receptor. Nat. Med. 9(8): 1000-1001.
60. Saleh F, Behbehani A, Asfar S, Khan I, Ibrahim G. 2011. Abnormal blood levels of trace elements and metals, DNA damage, and breast cancer in the state of Kuwait. Biol. Trace Elem. Res. 141(1-3): 96-109.
61. Siewit LC, Gengler B, Vegas E, Puckett R, Louie MC. 2010. Cadmium promotes breast cancer cell proliferation by potentiating the interaction between ER alpha and c-Jun. Mol. Endocrinol. 24(5): 981-992.
62. Silva E, Lopez-Espinosa MJ, Molina-Molina J-M, Fernández M, Olea N, Kortenkamp A. 2006. Lack of activity of cadmium in in vitro estrogenicity assays. Toxicol. Appl. Pharmacol. 216: 20-28.
63. Stoica A, Katzenellenbogen BS, Martin MB. 2000. Activation of estrogen receptor-alpha by the heavy metal cadmium. Mol. Endocrinol. 14(4): 545-553.
64. Vahter M, Berglund M, Akesson A, Liden C. 2002. Metals and women's health. Environ. Res. 88: 145-155.
65. Vahter M, Åkesson A, Lidén C, Ceccatellia S, Berglunda M. 2007. Gender differences in the disposition and toxicity of metals. Environ. Res. 104: 85-95.
66. Vivacqua A, Bonofiglio D, Recchia AG, Musti AM, Picard D, Andò S, Maggiolini M. 2006. The G protein-coupled receptor GPR30 mediates the proliferative effects induced by 17β-estradiol and hydroxytamoxifen in endometrial cancer cells. Mol. Endocrinol. 20(3): 631-646.
67. Watanabe H, Suzuki A, Mizutani T, Khono S, Lubahn DB, Handa H, Iguchi T. 2002. Genome-wide analysis of changes in early gene expression induced by oestrogen. Genes Cells 7(5): 497-507.
68. Wilson VS, Bobseine K, Gray LE. 2004. Development and characterization of a cell line that stably expresses an estrogen-responsive luciferase reporter for the detection of estrogen receptor agonist and antagonists. Toxicol. Sci. 81: 69-77.
69. World Health Organization. 1992. Cadmium. Environmental Health Criteria. International Program on Chemical Safety no. 134. WHO: Geneva.
70. Yaghjyan L, Colditz GA. 2011. Estrogens in the breast tissue: a systematic review. Cancer Causes Control 22(4): 529-540.
71. Yu X, Filardo EJ, Shaikh ZA. 2010. The membrane estrogen receptor GPR30 mediates cadmium-induced proliferation of breast cancer cells. Toxicol. Appl. Pharmacol. 245: 83-90.
72. Zang Y, Odwin-DaCosta S, Yager JD. 2009. Effects of cadmium on estrogen receptor mediated signaling and estrogen induced DNA synthesis in T47D human breast cancer cells. Toxicol. Lett. 184(2): 134-138.