Cadmium: Toxic effects on the reproductive system and the embryo

Reproductive Toxicology

Volumn 25, Issue 3, 2008, Pages 304-315

  Thompson, Jennifer ^a   Bannigan, John ^a  

^a UNIVERSITY COLLEGE DUBLIN   (Ireland)

Author keywords

Blastocyst; Cadmium; Cell adhesion; Chick embryo; Ovary; Oxidative stress; Testis; Ventral body wall defect

Indexed keywords

CADMIUM; CELL ADHESION MOLECULE; CIGARETTE SMOKE; HEAVY METAL; TRACE ELEMENT;

APOPTOSIS; BIOACCUMULATION; BLASTOCYST; BLOOD TESTIS BARRIER; CARDIOVASCULAR MALFORMATION; CELL ADHESION; CHICK EMBRYO; CHROMATIN; CRANIOFACIAL MALFORMATION; CUMULUS OOPHORUS; DEVELOPMENTAL STAGE; EMBRYO DEVELOPMENT; EMBRYOTOXICITY; ENVIRONMENTAL EXPOSURE; FISH; GAMETE; GASTROINTESTINAL MALFORMATION; HUMAN; LIMB MALFORMATION; NECROSIS; NEUROLOGIC DISEASE; NIDATION; NONHUMAN; OOCYTE DEVELOPMENT; OVARY; OVULATION; PLACENTA; POLLUTANT; PREGNANCY TERMINATION; REPRODUCTIVE TOXICITY; REVIEW; STEROIDOGENESIS; TROPHOBLAST; UROGENITAL TRACT MALFORMATION; VERTEBRA MALFORMATION;

BLASTOCYST; CADMIUM; CELL ADHESION; DNA DAMAGE; EMBRYO IMPLANTATION; EMBRYONIC DEVELOPMENT; FEMALE; HUMANS; MALE; OOGENESIS; OXIDATIVE STRESS; PREGNANCY; REPRODUCTION; SPERMATOGENESIS;

ANIMALIA;

EID: 43849091641     PISSN: 08906238     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.reprotox.2008.02.001     Document Type: Review

References (204)

1. WHO. Cadmium (Environmental Health Criteria No. 134) (1992), WHO, Geneva
2. Muntau H., and Baudo R. Sources of cadmium, its distribution and turnover in the freshwater environment. IARC 118 (1992) 133-148
3. IARC. IARC monographs on the evaluation of carcinogenic risks to humans, vol. 58. Beryllium, Cd, mercury and exposures in the glass manufacturing industry (February 9-16, 1993), IARC, Lyons, France
4. Martelli A., Rousselet E., Dycke C., Bouron A., and Moulis J.-M. Cadmium toxicity in animal cells by interference with essential metals. Biochimie 88 (2006) 1807-1814
5. WHO. Cadmium-environmental aspects (Environmental Health Criteria 135) (1992), WHO, Geneva
6. IRPTC. IRPTC legal file 1986 vol. 1 (1987), International Register of Potentially Toxic Chemicals, United Nations Environment Programme, Geneva
7. McLellan J.S., Flanagan P.R., Chamberlain M.J., and Valberg L.S. Measurement of dietary cadmium absorption in humans. J Toxicol Environ Health 4 (1978) 131-138
8. Nasreddine L., and Parent-Massin D. Food contamination by metals and pesticides in the European Union. Should we worry?. Toxicol Lett 127 (2002) 29-41
9. Watanabe T., Koizumi A., Fujita H., Kumai M., and Ikeda M. Role of rice in dietary cadmium intake of farming population with no known man-made pollution in Japan. Tohoku J Exp Med 144 (1984) 83-90
10. Vahter M., Berglund M., Slorach S., Jorhem L., and Lind B. Integrated personal monitoring of cadmium exposure in Sweden. IARC 118 (1992) 113-120
11. Jarup L., Berglund M., Elinder C.G., Nordberg G., and Vahter M. Health effects of cadmium exposure-a review of the literature and a risk estimate. Scand J Work Environ Health 24 Suppl 1 (1998) 1-51
12. McKenzie-Parnell J.M., Kjellstrom T.E., Sharma R.P., and Robinson M.F. Unusually high intake and fecal output of cadmium, and fecal output of other trace elements in New Zealand adults consuming dredge oysters. Environ Res 46 (1988) 1-14
13. Satarug S., and Moore M.R. Adverse health effects of chronic exposure to low-level cadmium in foodstuffs and cigarette smoke. Environ Health Perspect 112 (2004) 1099-1103
14. Nandi M., Slone D., Jick H., Shapiro S., and Lewis G.P. Cadmium content of cigarettes. Lancet 2 (1969) 1329-1330
15. Lewis G.P., Coughlin L.L., Jusko W.J., and Hartz S. Contribution of cigarette smoking to cadmium accumulation in man. Lancet 1 7745 (1972) 291-292
16. Friberg L., Piscator M., Nordberg G.F., and Kjellstrom T. Cadmium in the environment. 2nd ed. (1974), Chemical Rubber Co., Cleveland, OH
17. Elinder C.G., Kjellstrom T., Lind B., Linnman L., Piscator M., and Sundstedt K. Cadmium exposure from smoking cigarettes: variations with time and country where purchased. Environ Res 32 (1983) 220-227
18. Jarup L., Rogenfelt A., Elinder C.G., Nogawa K., and Kjellstrom T. Biological half-time of cadmium in the blood of workers after cessation of exposure. Scand J Work Environ Health 9 (1983) 327-331
19. Matsuno K., Kodama Y., and Tsuchiya K. Biological half-time and body burden of cadmium in dogs after a long-term oral administration of cadmium. Biol Trace Elem Res 29 (1991) 111-123
20. Nordberg M., Jin T., and Nordberg G.F. Cadmium, metallothionein and renal tubular toxicity. IARC 118 (1992) 293-297
21. El-Ashmawy I.M., and Youssef S.A. The antagonistic effect of chlorpromazine on cadmium toxicity. Toxicol Appl Pharmacol 161 (1999) 34-39
22. Sauer J.M., Waalkes M.P., Hooser S.B., Kuester R.K., McQueen C.A., and Sipes I.G. Suppression of Kupffer cell function prevents cadmium induced hepatocellular necrosis in the male Sprague-Dawley rat. Toxicology 121 (1997) 155-164
23. Tam P.P.L., and Liu W.K. Gonadal development and fertility of mice treated prenatally with cadmium during the early organogenesis stages. Teratology 32 3 (1985) 453-462
24. Toman R., Massanyi P., and Uhrin V. Changes in the testis and epididymis of rabbits after an intraperitoneal and peroral administration of cadmium. Trace Elem Electrolytes 19 3 (2002) 114-117
25. Kotsonis F.N., and Klaassen C.D. Toxicity and distribution of cadmium administered to rats at sublethal doses. Toxicol Appl Pharmacol 41 (1977) 667-680
26. Fende P.L., and Niewenhuis R.J. An electron microscopic study of the effects of cadmium chloride on cryptorchid testes of the rat. Biol Reprod 16 (1977) 298-305
27. Niewenhuis R.J. Effects of cadmium upon regenerated testicular vessels in the rat. Biol Reprod 23 (1980) 171-179
28. Berliner A.F., and Jones-Witters P. Early effects of a lethal cadmium dose on gerbil testis. Biol Reprod 13 (1975) 240-247
29. Laskey J.W., Rehnberg G.L., Laws S.C., and Hein J.F. Reproductive effects of low acute doses of cadmium chloride in adult male rats. Toxicol Appl Pharmacol 73 2 (1984) 250-255
30. Jin L.J., Lou Z.F., and Dong J.Y. Effects of cadmium and mercury on DNA damage of mice bone marrow cell and testicle germ cell in vitro. Carcinog Teratog Mutagen 16 2 (2004) 94-97
31. Yang H.S., Han D.K., Kim J.R., and Sim J.C. Effects of α-tocopherol on cadmium-induced toxicity in rat testis and spermatogenesis. J Korean Med Sci 21 (2006) 445-451
32. Aoyagi T., Ishikawa H., Miyaji K., Hayakawa K., and Hata M. Cadmium-induced testicular damage in a rat model of sub-chronic intoxication. Reprod Med Biol 1 (2002) 59-63
33. Bench G., Corzett M.H., Martinelli R., and Balhorn R. Cadmium concentrations in the testes, sperm, and spermatids of mice subjected to long-term cadmium chloride exposure. Cytometry 35 (1999) 30-36
34. Dixon R.L., Lee I.P., and Sherins R.J. Methods to assess reproductive effects of environmental chemicals: studies of cadmium and boron administered orally. Environ Health Perspect 13 (1976) 59-67
35. Chung N.P.Y., and Cheng C.Y. Is cadmium chloride-induced inter-sertoli tight junction permeability barrier disruption a suitable in vitro model to study the events of junction disassembly during spermatogenesis in the rat testis?. Endocrinology 142 5 (2001) 1878-1888
36. Wong C., Mruk D.D., Lui W., and Cheng C.Y. Regulation of blood-testis barrier dynamics: an in vivo study. J Cell Sci 117 (2004) 783-798
37. Yan H.H.N., and Cheng C.Y. Blood-testis barrier dynamics are regulated by an engagement/disengagement mechanism between tight and adherens junctions via peripheral adaptors. PNAS 102 33 (2006) 11722-11727
38. Akinloye O., Arowojolu A.O., Shittu O.B., and Anetor J.I. Cadmium toxicity: a possible cause of male infertility in Nigeria. Reprod Biol 6 1 (2006) 17-30
39. Saaranen M., Kantola M., Saarikoski S., and Vanha-Perttula T. Human seminal plasma cadmium: comparison with fertility and smoking habits. Andrologia 21 2 (1989) 140-145
40. Al-Bader A., Omu A.E., and Dashti H. Chronic cadmium toxicity to sperm of heavy cigarette smokers: immunomodulation by zinc. Arch Androl 43 2 (1999) 135-140
41. Leoni G., Bogliolo L., Deiana G., Berlinquer F., Rosati I., Pintus P.P., et al. Influence of cadmium exposure on in vitro ovine gamete dysfunction. Reprod Toxicol 16 4 (2002) 371-377
42. Waalkes M.P., Rehm S., Perantoni A.O., and Coogan T.P. Cadmium exposure in rats and tumours of the prostate. IARC 118 (1992) 391-400
43. West D.W., Slattery M.L., Robison L.M., French T.K., and Mahoney A.W. Adult dietary intake and prostate cancer risk in Utah: a case-control study with special emphasis on aggressive tumors. Cancer Causes Control 2 (1991) 85-94
44. Kazantzis G., Lam T.H., and Sullivan K.R. Mortality of cadmium-exposed workers. Scand J Work Environ Health 14 (1988) 220-223
45. Sorahan T., Lister A., Gilthorpe M.S., and Harrington J.M. Mortality of copper cadmium alloy workers with special reference to lung cancer and non-malignant diseases of the respiratory system, 1946-92. Occup Environ Med 52 (1995) 804-812
46. Waalkes M.P., Anver M., and Diwan B.A. Carcinogenic effects of cadmium in the Noble (NBL/Cr) rat: induction of pituitary, testicular, and injection site tumors and intraepithelial proliferative lesions of the dorsolateral prostate. Toxicol Sci 52 (1999) 154-161
47. Waalkes M.P., Anver M.R., and Diwan B.A. Chronic toxic and carcinogenic effects of oral cadmium in the Noble (NBL/Cr) rat: induction of neoplastic and proliferative lesions of the adrenal, kidney, prostate, and testes. J Toxicol Environ Health A 58 4 (1999) 199-214
48. Fort D.J., Stover E.L., Bantle J.A., Dumont J.N., and Finch R.A. Evaluation of a reproductive toxicity assay using Xenopus laevis: boric acid, cadmium and ethylene glycol monomethyl ether. J Appl Toxicol 21 (2001) 41-52
49. Fort D.J., McLaughlin D.W., Rogers R.L., and Buzzard B.O. Effect of endocrine disrupting chemicals on germinal vesicle breakdown in xenopus in vitro. Drug Chem Toxicol 25 3 (2002) 293-308
50. Lienesch L.A., Dumont J.N., and Bantle J.A. The effect of cadmium on oogenesis in Xenopus laevis. Chemosphere 41 10 (2000) 1651-1658
51. Saksena S.K., and Salmonsen R. Effects of cadmium chloride on ovulation and on induction of sterility in the female golden hamster. Biol Reprod 29 (1983) 249-256
52. Rehm S., and Waalkes M.P. Cadmium-induced ovarian toxicity in hamsters, mice and rats. Toxicol Sci 10 4 (1988) 635-647
53. Paksy K., Varga B., Horvath E., Tatrai E., and Ungvary G. Acute effects of cadmium on preovulatory serum FSH, LH, and prolactin levels and on ovulation and ovarian hormone secretion in estrous rats. Reprod Toxicol 3 4 (1989) 241-247
54. Paksy K., Varga B., and 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 10 (1996) 27-36
55. Paksy K., Varga B., Naray M., Olajos F., and Folly G. Altered ovarian progesterone secretion induced by cadmium fails to interfere with embryo transport in the oviduct of the rat. Reprod Toxicol 6 1 (1992) 77-83
56. Piasek M., and Laskey J.W. Acute cadmium exposure and ovarian steroidogenesis in cycling and pregnant rats. Reprod Toxicol 8 6 (1994) 495-507
57. Mlynarcikova A., Fickova M., and Scsukova S. Ovarian intrafollicular processes as a target for cigarette smoke components and selected environmental reproductive disruptors. Endocr Regul 39 (2005) 20-31
58. Vrsanska S., Nagyova E., Mlynarcikova A., Fickova M., and Kolena J. Components of cigarette smoke inhibit expansion of oocyte-cumulus complexes from porcine oocytes. Physiol Res 52 (2003) 383-387
59. Piasek M., Laskey J.W., Kostial K., and 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 (2002) S36-S44
60. Paksy K., Rajczy K., Forgacs Z., Lazar P., Bernard A., Gati I., et al. Effect of cadmium on morphology and steroidogenesis of cultured human ovarian granulosa cells. J Appl Toxicol 17 5 (1997) 321-327
61. Schmid B.P., Hall J.L., Goulding E., Fabro S., and Dixon R. In vitro exposure of male and female mice gametes to cadmium chloride during the fertilization process, and its effects on pregnancy outcome. Toxicol Appl Pharmacol 69 3 (1983) 326-332
62. Storeng R., and Jonsen J. Effect of nickel chloride and cadmium acetate on the development of pre-implantation mouse embryos in vitro. Toxicology 17 2 (1980) 183-187
63. De S.K., Paria B.C., Dey S.K., and Andrews G.K. Stage-specific effects of cadmium on pre-implantation embryo development and implantation in the mouse. Toxicology 80 1 (1993) 13-25
64. Yu H.S., Tam P.P.L., and Chan S.T.H. Effects of cadmium on pre-implantation mouse embryos in vitro with special reference to their implantation capacity and subsequent development. Teratology 32 3 (1985) 347-353
65. Abraham R., Charles A.K., Mankes R., LeFevre R., Renak V., and Ashok L. In vitro effects of cadmium chloride on preimplantation rat embryos. Ecotoxicol Environ Saf 12 3 (1986) 213-219
66. Jeong S.H., Habeebu S.S., and Klaassen C.D. Cadmium decreases gap junctional intercellular communication in mouse liver. Toxicol Sci 57 1 (2000) 156-166
67. Fang M.Z., Mar W.C., and Cho M.H. Cadmium-induced alterations of connexin expression in the promotion stage of in vitro two-stage transformation. Toxicology 161 1/2 (2001) 117-127
68. Hardy K., Warner A., Winston R.M.L., and Becker D.L. Expression of intercellular junctions during implantation development of the human embryo. Mol Human Reprod 2 8 (1996) 621-632
69. Kidder G.M., and Winterhager E. Intercellular communication in preimplantation development: the role of gap junctions. Front Biosci 6 (2001) D731-D736
70. Yu H.S., and Chan S.T. Zinc amelioration of cadmium toxicity on preimplantation mouse zygotes in vitro. Teratology 37 1 (1988) 13-19
71. Peters J.M., Duncan J.R., Wiley L.M., and Keen C.L. Influence of antioxidants on cadmium toxicity of mouse preimplantation embryos in vitro. Toxicology 99 1/2 (1995) 11-18
72. Larsen W. Human embryology. 2nd ed. (1997), WB Saunders Company
73. Talbot P., Shur B.D., and Myles D.G. Cell adhesion and fertilization: steps in oocyte transport, sperm-zona pellucida interactions, and sperm-egg fusion. Biol Reprod 68 (2003) 1-9
74. Chen L., Zhang H., Powers R.W., Russell P.T., and Larsen W.J. Covalent linkage between proteins of the inter-α-inhibitor family and hyaluronic acid is mediated by a factor produced by Granulose cells. J Biol Chem 271 (1996) 19409-19414
75. Talbot P., Geiske C., and Knoll M. Oocyte pick-up by the mammalian oviduct. Mol Biol Cell 10 (1999) 5-8
76. Chen L., Wert S.E., Hendrix E.M., Russell P.T., Cannon M., and Larsen W.J. Hyaluronic acid synthesis and gap junction endocytosis are necessary for normal expansion of the cumulus mass. Mol Reprod Dev 26 (1990) 236-247
77. Fiorini C., Tilloy-Ellul A., Chevalier S., Charuel C., and Pointis G. Sertoli cell junctional proteins as early targets for different classes of reproductive toxicants. Reprod Toxicol 18 (2004) 413-421
78. Yu H.S., and Chan S.T. Effects of cadmium on preimplantation and early postimplantation mouse embryos in vitro with special reference to their trophoblastic invasiveness. Pharmacol Toxicol 60 2 (1987) 129-134
79. Di Sant'Agnese P.A., Jensen K.D., Levin A., and Miller R.K. Placental toxicity of cadmium in the rat: an ultrastructural study. Placenta 4 2 (1983) 149-163
80. Powlin S.S., Keng P.C., and Miller R.K. Toxicity of cadmium in human trophoblast cells (Jar choriocarcinoma): role of calmodulin and the calmodulin inhibitor, zaldaride maleate. Toxicol Appl Pharmacol 144 (1997) 225-234
81. Lin F.J., Fitzpatrick J.W., Iannotti C.A., Martin D.S., Mariani B.D., and Tuan R.S. Effects of cadmium on trophoblast calcium transport. Placenta 18 (1997) 341-356
82. Goyer R.A., and Cherian M.G. Role of metallothionein in human placenta and rats exposed to cadmium. IARC Sci Publ 118 (1992) 238-247
83. Breen J.G., Eisenmann C., Horowitz S., and Miller R.K. Cell-specific increases in metallothionein expression in the human placenta perfused with cadmium. Reprod Toxicol 8 4 (1994) 297-306
84. Torreblanca A., Del Ramo J., and Sarkar B. Cadmium effect on zinc metabolism in human trophoblast cells: involvement of cadmium-induced metallothionein. Toxicology 72 2 (1992) 167-174
85. Weir P.J., Miller R.K., Maulik D., and DiSant'Agnese P.A. Toxicity of cadmium in the perfused human placenta. Toxicol Appl Pharmacol 105 1 (1990) 156-171
86. Breen J.G., Nelson E., and Miller R.K. Cellular adaptation to chronic cadmium exposure: intracellular localization of metallothionein protein in human trophoblast cells (Jar). Teratology 51 4 (1995) 266-272
87. Piasek M., Blanusa M., Kostial K., and Laskey J.W. Placental cadmium and progesterone concentrations in cigarette smokers. Reprod Toxicol 15 (2001) 673-681
88. Kawai M., Swan K.F., Green A.E., Edwards D.E., Anderson M.B., and Henson M.C. 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 (2002) 178-183
89. Menoud P.A., and Schowing J. A preliminary study of the mechanisms of cadmium teratogenicity in chick embryo after direct action. J Toxicol Clin Exp 7 2 (1987) 77-84
90. Webster W.S., and Messerle K. Changes in the mouse neuroepithelium associated with cadmium-induced neural tube defects. Teratology 21 (1980) 79-88
91. Messerle K., and Webster W.S. The classification and development of cadmium-induced limb defects in mice. Teratology 25 (1982) 61-70
92. De S.K., Dey S., and Andrews G.K. Cadmium teratogenicity and its relationship with metallothionein gene expression in midgestation mouse embryos. Toxicology 64 (1990) 89-104
93. Sunderman Jr. F.W., Plowman M.C., and Hopfer S.M. Teratogenicity of cadmium chloride in the South African frog, Xenopus laevis. IARC 118 (1992) 249-256
94. Layton W.M., and Layton M.W. Cadmium-induced limb defects in mice: strain associated differences in sensitivity. Teratology 19 (1979) 229-235
95. Feuston M.H., and Scott Jr. W.J. Cadmium-induced forelimb ectrodactyly: a proposed mechanism of teratogenesis. Teratology 32 (1985) 407-419
96. Holt D., and Webb M. Teratogenicity of ionic cadmium in the Wistar rat. Arch Toxicol 59 (1987) 443-447
97. Perez-Coll C.S., Herkovits J., and Salibian A. Effects of cadmium on the development of an amphibian. Arch Biol Med Exp (Santiago) 18 1 (1985) 33-39
98. Herkovits J., Cardellini P., Pavanati C., and Perez-Coll C.S. Susceptibility of early life stages of Xenopus laevis to cadmium. Environ Toxicol Chem 16 2 (1997) 312-316
99. Cheng S.H., Wai A.W.K., So C.H., and Wu R.S.S. Cellular and molecular basis of cadmium-induced deformities in zebrafish embryos. Environ Toxicol Chem 19 12 (2000) 3024-3031
100. Hen Chow E.S., and Cheng S.H. Cadmium affects muscle type development and axon growth in zebrafish embryonic somitogenesis. Toxicol Sci 73 (2003) 149-159
101. Thompson J.M., and Bannigan J.G. The effects of cadmium on formation of the ventral body wall in chick embryos and their prevention by zinc pre-treatment. Teratology 64 2 (2001) 87-97
102. Thompson J.M., Hipwell E., Loo H.V., and Bannigan J.G. Effects of cadmium on cell death and cell proliferation in chick embryos. Reprod Toxicol 20 4 (2005) 539-548
103. Thompson J.M., and Bannigan J.G. Omphalocele induction in the chick embryo by administration of cadmium. J Pediatr Surg 42 10 (2007) 1703-1709
104. Thompson J., Wong L., Lau P.S., and Bannigan J. Adherens junction breakdown in the periderm following cadmium administration in the chick embryo: distribution of cadherins and associated molecules. Reprod Toxicol 25 1 (2008) 39-46
105. Schmid B.P., Kao J., and Goulding E. Evidence for reopening of the cranial neural tube in mouse embryos treated with cadmium chloride. Experientia 41 (1985) 271-272
106. Padmanabhan R. Light microscopic studies on the pathogenesis of exencephaly and cranioschisis induced in the rat after neural tube closure. Teratology 37 (1988) 29-36
107. Gale T.F., and Layton W.M. The susceptibility of inbred strains of hamsters to cadmium-induced embryotoxicity. Teratology 21 2 (1980) 181-186
108. Wlodarczyk B., Biernacki B., Minta M., and Zmudzki J. Postimplantation whole embryo culture assay for hamsters: an alternative to rat and mouse. Sci World J 1 (2001) 227-234
109. Ferm V.H. Developmental malformations induced by cadmium. A study of timed injections during embryogenesis. Biol Neonate 19 1 (1971) 101-107
110. Samarawickrama G.P., and Webb M. The acute toxicity and teratogenicity of cadmium in the pregnant rat. J Appl Toxicol 1 5 (1981) 270-277
111. Galicia-Garcia V., Rojas-Lopez M., Rojas R., Olaiz G., and Rios C. Cadmium levels in maternal, cord and newborn blood in Mexico City. Toxicol Lett 91 (1997) 57-61
112. Ronco A.M., Arguello G., Munoz L., Gras N., and Llanos M. Metals content in placentas from moderate cigarette consumers: correlation with newborn weight. Biometals 18 (2005) 233-241
113. Nishijo M., and Tawara K. Relationship between newborn size and mother's blood cadmium levels, Toyama, Japan. Arch Environ Health 59 1 (2004) 22-25
114. Nishijo M., Nakagawa H., Honda R., Tanebe K., Saito S., Teranishi H., et al. Effects of maternal exposure to cadmium on pregnancy outcome and breast milk. Occup Environ Med 59 (2002) 394-397
115. Huel G., Boudene C., and Ibrahim M.A. Cadmium and lead content of maternal and newborn hair: relationship to parity, birth weight, and hypertension. Arch Environ Health 36 (1981) 221-227
116. Frery N., Nessmann C., Girard F., Lafond J., Moreau T., Blot P., et al. Environmental exposure to cadmium and human birthweight. Toxicology 79 (1993) 109-118
117. Lagerkvist B.J., Nordberg G.F., Soderberg H.A., Ekesrydh S., Englyst V., Gustavsson M., et al. Placental transfer of cadmium. IARC 118 (1992) 287-291
118. Boadi W.Y., Yannai S., Urbach J., Brandes J.M., and Summer K.H. Transfer and accumulation of cadmium, and the level of metallothionein in perfused human placentae. Arch Toxicol 65 (1991) 318-323
119. Konecki J., Blazejowski J., Slowinski J., and Helewski K. Influence of chronic cadmium exposure during pregnancy on DNA synthesis in different organs of rat offspring. Med Sci Monit 6 6 (2000) 1077-1081
120. Schoeters G., Den Hond E., Zuurbier M., Naginiene R., Van Den Hazel P., Stilianakis N., et al. Cadmium and children: exposure and health effects. Acta Paediatr 95 Suppl 453 (2006) 50-54
121. Gumbiner B.M. Cell adhesion: the molecular basis of tissue architecture and morphogenesis. Cell 84 (1996) 345-357
122. Lee N.P.Y., Mruk D., Lee W.M., and Cheng C.Y. Is the cadherin/catenin complex a functional unit of cell-cell actin-based adherens junctions in the rat testis?. Biol Reprod 68 (2003) 489-508
123. Lui W.Y., Mruk D., Lee W.M., and Cheng C.Y. Sertoli cell tight junction dynamics: their regulation during spermatogenesis. Biol Reprod 68 (2003) 1087-1097
124. Goossenns S., and Van Roy F. Cadherin-mediated cell-cell adhesion in the testis. Front Biosci 10 (2005) 398-419
125. Cyr D.G., Gregory M., Dube E., Dufresne J., Chan P.T.K., and Hermo L. Orchestration of occludins, claudins, catenins and cadherins as players involved in maintenance of the blood-epididymal barrier in animals and humans. Asian J Androl 9 4 (2007) 463-475
126. Bloor D.J., Wilson Y., Kibschull M., Traub O., Leese H.J., Winterhager E., et al. Expression of connexins in human preimplantation embryos in vitro. Reprod Biol Endocrinol 2 2 (2004) 25
127. Laird D.W. Life cycle of connexins in health and disease. Biochem J 394 (2006) 527-543
128. Li J., Zhang J.V., Cao Y.-J., Zhou J.-X., Liu W.-M., Fan X.-J., et al. Inhibition of the β-catenin signalling pathway in blastocyst and uterus during the window of implantation in mice. Biol Reprod 72 (2005) 700-706
129. + isoform. Development 124 (1997) 2027-2037
130. Kim J., Gye M.C., and Kim M.K. Role of occludin, a tight junction protein, in blastocoel formation, and in the paracellular permeability and differentiation of trophectoderm in preimplantation mouse embryos. Mol Cells 17 2 (2004) 248-254
131. Bloor D.J., Metcalfe A.D., Rutherford A., Brison D.R., and Kimber S.J. Expression of cell adhesion molecules during human preimplantation embryo development. Mol Human Reprod 8 3 (2002) 237-245
132. Pummi K., Malminen M., Aho H., Karvonen S.L., Peltonen J., and Peltonen S. Epidermal tight junctions: ZO-1 and occludin are expressed in mature, developing, and affected skin and in vitro differentiating keratinocytes. J Invest Dermatol 117 5 (2001) 1050-1058
133. Hentula M., Peltonen J., and Peltonen S. Expression profiles of cell-cell and cell-matrix junction proteins in developing human epidermis. Arch Dermatol Res 293 (2001) 259-267
134. Arita K., Akiyama M., Tsuji Y., McMillan J.R., Eady R.A.J., and Shimizu H. Changes in gap junction distribution and connexin expression pattern during human fetal skin development. J Histochem Cytochem 50 11 (2002) 1493-1500
135. Risek B., Klier G., and Gilula N.B. Developmental regulation and structural organization of connexins in epidermal gap junctions. Dev Biol 164 (1994) 183-196
136. Oteiza P.I., Adonaylo V.N., and Keen C.L. Cadmium-induced testes oxidative damage in rats can be influenced by dietary zinc intake. Toxicology 137 (1999) 13-22
137. Amara S, Abdelmelek H, Garrel C, Guiraud P, Douki T, Ravanat J-L, Favier A, Sakly M, Ben Rhouma K. Preventive effect of zinc against cadmium-induced oxidative stress in the rat testis. J Reprod Dev; in press.
138. Gupta R.S., Gupta E.S., Dhakal B.K., Thakur A.R., and Ahnn J. Vitamin C and vitamin E protect the rat testes from cadmium-induced reactive oxygen species. Mol Cells 17 1 (2004) 132-139
139. Shaikh Z.A., Vu T.T., and Zaman K. Oxidative stress as a mechanism of chronic cadmium-induced hepatotoxicity and renal toxicity and protection by antioxidants. Toxicol Appl Pharmacol 154 (1999) 256-263
140. Santos F.W., Zeni G., Rocha J.B.T., Weis S.N., Fachinetto J.M., Favero A.M., et al. Diphenyl diselenide reverses cadmium-induced oxidative damage on mice tissues. Chem-Biol Interact 151 (2005) 159-165
141. Ognjanovic B., Zikic R.V., Stajn A., Saicic Z.S., Kostic M.M., and Petrovic V.M. The effects of selenium on the antioxidant defense system in the liver of rats exposed to cadmium. Physiol Res 44 5 (1995) 293-300
142. El-Sharaky A.S., Newairy A.A., Badreldeen M.M., Eweda S.M., and Sheweita S.A. Protective role of selenium against renal toxicity induced by cadmium in rats. Toxicology 235 (2007) 185-193
143. Shaikh Z.A., and Tang W. Protection against chronic cadmium toxicity by glycine. Toxicology 132 2/3 (1999) 139-146
144. Ardais AP, Santos FW, Nogueira CW. Ebselen attenuates cadmium-induced speed testicular damage in mice. J Appl Toxicol; in press.
145. Vousden K.H. Outcomes of p53 activation-spoilt for choice. J Cell Sci 119 (2006) 5015-5020
146. Xu G., Zhou G., Jin T., Zhou T., Hammarstrom S., Bergh A., et al. Apoptosis and p53 gene expression in male reproductive tissues of cadmium exposed rats. Biometals 12 (1998) 131-139
147. Zhou T., Zhou G., Song W., Eguchi N., Lu W., Lundin E., et al. Cadmium-induced apoptosis and changes in expression of p53, c-jun and MT-1 genes in testes and ventral prostate of rats. Toxicology 142 (1999) 1-13
148. Pulido M.D., and Parrish A.R. Metal-induced apoptosis: mechanisms. Mutat Res 533 (2003) 227-241
149. Wätjen W., Haase H., Biagioli M., and Beyersmann D. Induction of apoptosis in mammalian cells by cadmium and zinc. Environ Health Perspect 110 Suppl 5 (2002) 865-867
150. Cullinane J., Thompson J., and Bannigan J. Protection from cadmium teratogenicity in the chick embryo by divalent metallic cations. Reprod Toxicol 24 (2007) 78-79 [abstracts]
151. Santos F.W., Oro T., Zeni G., Rocha J.B.T., do Nascimento P.C., and Nogueira C.W. Cadmium induced testicular damage and its response to administration of succimer and diphenyl diselenide in mice. Toxicol Lett 152 (2004) 255-263
152. Luo S.Q., Plowman M.C., Hopfer S.M., and Sunderman Jr. F.W. Mg(2+)-deprivation enhances and Mg(2+)-supplementation diminishes the embryotoxic and teratogenic effects of Ni2+, Co2+, Zn2+, and Cd2+ for frog embryos in the FETAX assay. Ann Clin Lab Sci 23 2 (1993) 121-129
153. Bridges C.C., and Zalups R.K. Molecular and ionic mimicry and the transport of toxic metals. Toxicol Appl Pharmacol 204 (2005) 274-308
154. Chmielnicka J., and Sowa B. Cadmium interaction with essential metals (Zn, Cu, Fe), metabolism metallothionein, and ceruloplasmin in pregnant rats and fetuses. Ecotoxicol Environ Saf 35 (1996) 277-281
155. Jacobs R.M., Jones A.O., Fox M.R., and Fry Jr. B.E. Retention of dietary cadmium and the ameliorative effect of zinc, copper, and manganese in Japanese quail. J Nutr 108 1 (1978) 22-32
156. He L., Girijashanker K., Dalton T.P., Reed J., Li H., Soleimani M., et al. ZIP-8, member of the Solute-Carrier-39 (SLC39) metal-transporter family: characterization of transporter properties. Mol Pharmacol 70 1 (2006) 171-180
157. Shannon R.D. Revised effective ionic radii and systematic studies of interatomic distances in halides and chalcogenides. Acta Cryst A32 (1976) 751-767
158. Braeckman B., Smagghe G., Brutsaert N., Cornelis R., and Raes H. Cadmium uptake and defence mechanism in insect cells. Environ Res A 80 (1999) 231-243
159. Souza V., Bucio L., and Gutierrez-Ruiz M.C. Cadmium uptake by a human hepatic cell line (WRL-68 cells). Toxicology 120 (1997) 215-220
160. Prasad A.S., Oberleas D., Wolf P., and Horwitz J.P. Studies on zinc deficiency: changes in trace elements and enzyme activities in tissues of zinc-deficient rats. J Clin Invest 46 4 (1967) 549-557
161. Matthews K.W., Mueller-Ortiz S.L., and Wetsel R.A. Carboxypeptidase N: a pleiotropic regulator of inflammation. Mol Immunol 40 (2004) 785-793
162. 1 cells. Toxicol Appl Pharmacol 107 (1991) 81-97
163. Yin T., and Green K.J. Regulation of desmosome assembly and adhesion. Semin Cell Dev Biol 15 (2004) 665-677
164. 2+ in mouse epidermal cells is controlled by E-cadherin. J Cell Biol 114 3 (1991) 545-555
165. Saez J.C., Berthoud V.M., Branes M.C., Martinez A.D., and Beyer E.C. Plasma membrane channels formed by connexins: their regulation and functions. Physiol Rev 83 (2003) 1359-1400
166. 2+. Biochim Biophys Acta 1498 (2000) 91-98
167. King L.M., Banks W.A., and George W.J. Differences in cadmium transport to the testis, epididymis, and brain in cadmium-sensitive and -resistant murine strains 129/J and A/J. J Pharmacol Exp Therap 289 2 (1999) 825-830
168. King L.M., Banks W.A., and George W.J. Differential zinc transport into the testis and brain of cadmium-sensitive and -resistant murine strains. J Androl 21 5 (2000) 656-663
169. Dalton T.P., He L., Wang B., Miller M.L., Jin L., Stringer K.F., et al. Identification of mouse SLC39A8 as the transporter responsible for cadmium-induced toxicity in the testis. PNAS 102 9 (2005) 3401-3406
170. Waalkes M.P., and Poirier L.A. Interactions of cadmium with interstitial tissue of the rat testes. Uptake of cadmium by isolated interstitial cells. Biochem Pharmacol 34 14 (1985) 2513-2518
171. Page K.R., Abramovich D.R., Aggett P.J., Bain M., Chipperfield A.R., Durdy H., et al. Uptake of zinc by human placental microvillus border membranes and characterization of the effects of cadmium on this process. Placenta 13 2 (1992) 151-161
172. Sunderman Jr. F.W. Cadmium substitution for zinc in finger-loop domains of gene-regulating proteins as a possible mechanism for the genotoxicity and carcinogenicity of cadmium compounds. Toxicol Environ Chem 27 (1990) 131-141
173. Predki P.F., and Sarkar B. The effect of replacement of "zinc finger" zinc on estrogen receptor DNA interactions. J Biol Chem 267 9 (1992) 5842-5846
174. Faurskov B., and Bjerregaard H.F. Evidence for cadmium mobilization of intracellular calcium through a divalent cation receptor in renal distal epithelial A6 cells. Pflugers Arch-Eur J Physiol 445 (2002) 40-50
175. Misra U.K., Gawdi G., Akabani G., and Pizzo S.V. Cadmium-induced DNA synthesis and cell proliferation in macrophages: the role of intracellular calcium and signal transduction mechanisms. Cell Signal 14 (2002) 327-340
176. Cooper G.M., and Hausman R.E. The cell: a molecular approach. 4th ed. (2007), ASM Press, Sinauer Associates
177. Suzuki Y., Chao S.H., Zysk J.R., and Cheung W.Y. Stimulation of calmodulin by cadmium ion. Arch Toxicol 57 3 (1985) 205-211
178. Radisky D., and Kaplan J. Regulation of transition metal transport across the yeast plasma membrane. J Biol Chem 274 8 (1999) 4481-4484
179. Piersma A.H., Roelen B., Roest P., Haakmat-Hoesenie A.S., Van Achterberg T.A.E., and Mummery C.L. Cadmium-induced inhibition of proliferation and differentiation of embryonal carcinoma cells and mechanistic aspects of protection by zinc. Teratology 48 (1993) 335-341
180. King L.A., MacDonald P.C., and Casey M.L. Regulation of metallothionein expression in human amnion epithelial and mesenchymal cells. Am J Obstet Gynecol 177 6 (1997) 1496-1501
181. Kang Y.J. Metallothionein redox cycle and function. Exp Biol Med 231 (2006) 1459-1467
182. Manuel Y., Thomas Y., and Pellegrini O. Metallothionein and tissue damage. IARC 118 (1992) 231-237
183. Hamada T., Sasaguri T., Tanimoto A., Arima N., Shimajiri S., Abe T., et al. Apoptosis of human kidney 293 cells is promoted by polymerized cadmium-metallothionein. Biochem Biophys Res Commun 219 (1996) 829-834
184. Ishido M., Tohyama C., and Suzuki T. Cadmium-bound metallothionein induces apoptosis in rat kidneys, but not in cultured kidney LLC-PK1 cells. Life Sci 64 (1999) 797-804
185. Aughey E., Fell G.S., Svott R., and Black M. Histopathology of early effects of oral cadmium in the rat kidney. Environ Health Perspect 54 (1984) 153-161
186. Sabolic I., Ljubojevic M., Herak-Kramberger C.M., and Brown D. Cd-MT causes endocytosis of brush border transporters in rat renal proximal tubules. Am J Physiol Renal Physiol 283 (2002) F1389-F1402
187. Lin R.H., Lee C.H., Chen W.K., and Lin-Shiau S.Y. Studies on cytotoxic and genotoxic effects of cadmium nitrate and lead nitrate in Chinese hamster ovary cells. Environ Mol Mutagen 23 2 (1994) 143-149
188. Hansmann I., and Probeck H.D. Detection of nondisjunction in mammals. Environ Health Perspect 31 (1979) 161-165
189. Fatur T., Lah T.T., and Filipic M. Cadmium inhibits repair of UV-, methyl methanesulfonate- and N-methyl-N-nitrosourea-induced DNA damage in Chinese hamster ovary cells. Mutat Res 529 (2003) 109-116
190. Gick G.G., and McCarthy K.S. Amplification of the metallothionein-I gene in cadmium- and zinc-resistant Chinese hamster ovary cells. J Biol Chem 257 15 (1982) 9049-9053
191. Yang J.-L., Chao J.-I., and Lin J.-G. Reactive oxygen species may participate in the mutagenicity and mutational spectrum of cadmium in Chinese hamster ovary-K1 cells. Chem Res Toxicol 9 (1996) 1360-1367
192. Yang P.-M., Chiu S.-J., Lin K.-A., and Lin L.-Y. Effect of cadmium on cell cycle progression in Chinese hamster ovary cells. Chem-Biol Interact 149 (2004) 125-136
193. Shiverick K.T., and Salafia C. Cigarette smoking and pregnancy. I. Ovarian, uterine and placental effects. Placenta 20 (1999) 265-272
194. Gray R.H., and Wu L.Y. Subfertility and risk of spontaneous abortion. Am J Pub Health 90 9 (2000) 1452-1454
195. Wilks D.J., and Hay A.W.M. Smoking and female fecundity: the effect and importance of study design. Reprod Biol 112 (2004) 127-135
196. Neal M.S., Hughes E.G., Holloway A.C., and Foster W.G. Sidestream smoking is equally as damaging as mainstream smoking on IVF outcomes. Human Reprod 20 9 (2005) 2531-2535
197. Mortada W.I., Sobh M.A., and El-Defrawy M.M. The exposure to cadmium, lead and mercury from smoking and its impact on renal integrity. Med Sci Monit 10 3 (2004) CR112-CR116
198. Zenzes M.T., Krishnan S., Krishnan B., Zhang H., and Casper R.F. Cadmium accumulation in follicular fluid of women in IVF is higher in smokers. Fertil Steril 64 (1995) 599-603
199. Varga B., Zsolnai B., Paksy K., Naray M., and Ungvary G. Age dependent accumulation of cadmium in the human ovary. Reprod Toxicol 7 3 (1993) 225-228
200. Stillman R.J., Rosenberg M.J., and Sachs B.P. Smoking and reproduction. Fertil Steril 46 4 (1986) 545-566
201. Karaer A., Avsar F.A., and Batioglu S. Risk factors for ectopic pregnancy: a case-control study. Aust NZ J Obstet Gynaecol 46 (2006) 521-527
202. Gerhard I., Monga B., Waldbrenner A., and Runnebaum B. Heavy metals and fertility. J Toxicol Environ Health A (1998)
203. Cogswell M.E., Weisberg P., and Spong C. Cigarette smoking, alcohol use and adverse pregnancy outcomes: implications for micronutrient supplementation. J Nutr 133 5 Suppl 2 (2003) 1722S-1731S
204. Semczuk M., and Semczuk-Sikora A. New data on toxic metal intoxication (Cd, Pb, and Hg in particular) and Mg status during pregnancy. Med Sci Monit 7 2 (2001) 332-340