Mechanisms of cadmium carcinogenesis

Toxicology and Applied Pharmacology

Volumn 238, Issue 3, 2009, Pages 272-279

  Joseph, Pius ^a  

^a Health Effects Laboratory Division   (United States)

Author keywords

Apoptosis; Cadmium; Carcinogenesis; DNA damage repair; Gene expression; Oxidative stress

Indexed keywords

CADMIUM; CALCIUM ION; CASPASE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; DNA; DNA FORMAMIDOPYRIMIDINE GLYCOSYLASE; GLUTAMATE CYSTEINE LIGASE; GLUTATHIONE; GLUTATHIONE PEROXIDASE; GLUTATHIONE REDUCTASE; HEME OXYGENASE; HYPOXIA INDUCIBLE FACTOR 1; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INITIATION FACTOR 3; INITIATION FACTOR 4E; METALLOTHIONEIN; MITOGEN ACTIVATED PROTEIN KINASE; MYC PROTEIN; PROTEIN C FOS; PROTEIN C JUN; PROTEIN P53; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR NRF2; TRANSCRIPTION FACTOR SP1; UPSTREAM STIMULATORY FACTOR;

APOPTOSIS; CADMIUM POISONING; CARCINOGENICITY; CHEMICAL CARCINOGENESIS; CIGARETTE SMOKING; DNA DAMAGE; DNA METHYLATION; DNA REPAIR; DNA STRAND BREAKAGE; EARLY RESPONSE GENE; ENVIRONMENTAL EXPOSURE; ESOPHAGUS CARCINOMA; GENE EXPRESSION; GENOTOXICITY; HUMAN; IMMEDIATE EARLY GENE; LUNG CANCER; MALIGNANT TRANSFORMATION; NONHUMAN; OCCUPATIONAL EXPOSURE; OXIDATIVE STRESS; REVIEW; TOXICOGENETICS;

ANIMALS; APOPTOSIS; CADMIUM; CARCINOGENS, ENVIRONMENTAL; CELL TRANSFORMATION, NEOPLASTIC; DNA DAMAGE; DNA REPAIR; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; NEOPLASMS; OXIDATIVE STRESS; RISK ASSESSMENT;

ANIMALIA;

EID: 67649649748     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2009.01.011     Document Type: Review

References (108)

1. Abate C., Patel L., Rauscher III F.J., and Curran T. Redox regulation of fos and jun DNA-binding activity in vitro. Science (New York, N.Y.) 249 (1990) 1157-1161
2. Abshire M.K., Devor D.E., Diwan B.A., Shaughnessy Jr. J.D., and Waalkes M.P. In vitro exposure to cadmium in rat L6 myoblasts can result in both enhancement and suppression of malignant progression in vivo. Carcinogenesis 17 (1996) 1349-1356
3. Achanzar W.E., Achanzar K.B., Lewis J.G., Webber M.M., and Waalkes M.P. Cadmium induces c-myc, p53, and c-jun expression in normal human prostate epithelial cells as a prelude to apoptosis. Toxicol. Appl. Pharmacol. 164 (2000) 291-300
4. Achanzar W.E., Diwan B.A., Liu J., Quader S.T., Webber M.M., and Waalkes M.P. Cadmium-induced malignant transformation of human prostate epithelial cells. Cancer Res. 61 (2001) 455-458
5. Achanzar W.E., Webber M.M., and Waalkes M.P. Altered apoptotic gene expression and acquired apoptotic resistance in cadmium-transformed human prostate epithelial cells. Prostate 52 (2002) 236-244
6. Alam J., Wicks C., Stewart D., Gong P., Touchard C., Otterbein S., Choi A.M., Burow M.E., and Tou J. Mechanism of heme oxygenase-1 gene activation by cadmium in MCF-7 mammary epithelial cells. Role of p38 kinase and Nrf2 transcription factor. J. Biol. Chem. 275 (2000) 27694-27702
7. Alvarez S.M., Gomez N.N., Scardapane L., Zirulnik F., Martinez D., and Gimenez M.S. Morphological changes and oxidative stress in rat prostate exposed to a non-carcinogenic dose of cadmium. Toxicol. Lett. 153 (2004) 365-376
8. Angel P., and Karin M. The role of Jun, Fos and the AP-1 complex in cell-proliferation and transformation. Biochim. Biophys. Acta 1072 (1991) 129-157
9. ATSDR. Toxicological profile of cadmium. Agency for Toxic Substances and Disease Registry (1999)
10. Badisa V.L., Latinwo L.M., Odewumi C.O., Ikediobi C.O., Badisa R.B., Brooks-Walter A., Lambert A.T., and Nwoga J. Cytotoxicity and stress gene microarray analysis in cadmium-exposed CRL-1439 normal rat liver cells. Int. J. Mol. Med. 22 (2008) 213-219
11. Benbrahim-Tallaa L., Liu J., Webber M.M., and Waalkes M.P. Estrogen signaling and disruption of androgen metabolism in acquired androgen-independence during cadmium carcinogenesis in human prostate epithelial cells. Prostate 67 (2007) 135-145
12. Benbrahim-Tallaa L., Waterland R.A., Dill A.L., Webber M.M., and Waalkes M.P. Tumor suppressor gene inactivation during cadmium-induced malignant transformation of human prostate cells correlates with overexpression of de novo DNA methyltransferase. Environ. Health Perspect. 115 (2007) 1454-1459
13. Bertin G., and Averbeck D. Cadmium: cellular effects, modifications of biomolecules, modulation of DNA repair and genotoxic consequences (a review). Biochimie 88 (2006) 1549-1559
14. Blumenthal N.C., Cosma V., Skyler D., LeGeros J., and Walters M. The effect of cadmium on the formation and properties of hydroxyapatite in vitro and its relation to cadmium toxicity in the skeletal system. Calcif. Tissue Int. 56 (1995) 316-322
15. Bolduc J.S., Denizeau F., and Jumarie C. Cadmium-induced mitochondrial membrane-potential dissipation does not necessarily require cytosolic oxidative stress: studies using rhodamine-123 fluorescence unquenching. Toxicol. Sci. 77 (2004) 299-306
16. Bonda E., Wlostowski T., and Krasowska A. Testicular toxicity induced by dietary cadmium is associated with decreased testicular zinc and increased hepatic and renal metallothionein and zinc in the bank vole (Clethrionomys glareolus). BioMetals 17 (2004) 615-624
17. Boudreau J., Vincent R., Nadeau D., Trottier B., Fournier M., Krzystyniak K., and Chevalier G. Toxicity of inhaled cadmium chloride: early responses of the antioxidant and surfactant systems in rat lungs. J. Toxicol. Environ. health 23 (1988) 241-256
18. Casalino E., Sblano C., Calzaretti G., and Landriscina C. Acute cadmium intoxication induces alpha-class glutathione S-transferase protein synthesis and enzyme activity in rat liver. Toxicology 217 (2006) 240-245
19. Coutant A., Lebeau J., Bidon-Wagner N., Levalois C., Lectard B., and Chevillard S. Cadmium-induced apoptosis in lymphoblastoid cell line: involvement of caspase-dependent and -independent pathways. Biochimie 88 (2006) 1815-1822
20. Ding W., and Templeton D.M. Activation of parallel mitogen-activated protein kinase cascades and induction of c-fos by cadmium. Toxicol. Appl. Pharmacol. 162 (2000) 93-99
21. Eneman J.D., Potts R.J., Osier M., Shukla G.S., Lee C.H., Chiu J.F., and Hart B.A. Suppressed oxidant-induced apoptosis in cadmium adapted alveolar epithelial cells and its potential involvement in cadmium carcinogenesis. Toxicology 147 (2000) 215-228
22. Fatur T., Tusek M., Falnoga I., Scancar J., Lah T.T., and Filipic M. DNA damage and metallothionein synthesis in human hepatoma cells (HepG2) exposed to cadmium. Food Chem. Toxicol. 40 (2002) 1069-1076
23. Filipic M., and Hei T.K. Mutagenicity of cadmium in mammalian cells: implication of oxidative DNA damage. Mutat. Res. 546 (2004) 81-91
24. Galan A., Garcia-Bermejo L., Troyano A., Vilaboa N.E., Fernandez C., de Blas E., and Aller P. The role of intracellular oxidation in death induction (apoptosis and necrosis) in human promonocytic cells treated with stress inducers (cadmium, heat, X-rays). Eur. J. Cell Biol. 80 (2001) 312-320
25. Giaginis C., Gatzidou E., and Theocharis S. DNA repair systems as targets of cadmium toxicity. Toxicol. Appl. Pharmacol. 213 (2006) 282-290
26. Hamer D.H. Metallothionein. Annu. Rev. Biochem. 55 (1986) 913-951
27. Hardingham G.E., Chawla S., Johnson C.M., and Bading H. Distinct functions of nuclear and cytoplasmic calcium in the control of gene expression. Nature 385 (1997) 260-265
28. Hirano T., Yamaguchi Y., and Kasai H. Inhibition of 8-hydroxyguanine repair in testes after administration of cadmium chloride to GSH-depleted rats. Toxicol. Appl. Pharmacol. 147 (1997) 9-14
29. Huang D., Zhang Y., Qi Y., Chen C., and Ji W. Global DNA hypomethylation, rather than reactive oxygen species (ROS), a potential facilitator of cadmium-stimulated K562 cell proliferation. Toxicol. Lett. 179 (2008) 43-47
30. Huff J., Lunn R.M., Waalkes M.P., Tomatis L., and Infante P.F. Cadmium-induced cancers in animals and in humans. Int. J. Occup. Environ. Health 13 (2007) 202-212
31. IARC. Cadmium and cadmium compounds. Beryllium, Cadmium, Mercury, and Exposures in the Glass Manufacturing Industry. Working Group Views and Expert Opinions, Lyon, France, 9-16, February 1993. IARC Monograph on Evaluation of Carcinogenis Risks in Human (1993) 41-117
32. Jamall I.S., Naik M., Sprowls J.J., and Trombetta L.D. A comparison of the effects of dietary cadmium on heart and kidney antioxidant enzymes: evidence for the greater vulnerability of the heart to cadmium toxicity. J. Appl. Toxicol. 9 (1989) 339-345
33. Jin T., Lu J., and Nordberg M. Toxicokinetics and biochemistry of cadmium with special emphasis on the role of metallothionein. Neurotoxicology 19 (1998) 529-535
34. Joseph P., Muchnok T.K., Klishis M.L., Roberts J.R., Antonini J.M., Whong W.Z., and Ong T. Cadmium-induced cell transformation and tumorigenesis are associated with transcriptional activation of c-fos, c-jun, and c-myc proto-oncogenes: role of cellular calcium and reactive oxygen species. Toxicol. Sci. 61 (2001) 295-303
35. Joseph P., Lei Y.X., Whong W.Z., and Ong T.M. Molecular cloning and functional analysis of a novel cadmium-responsive proto-oncogene. Cancer Res. 62 (2002) 703-707
36. Joseph P., Lei Y.X., Whong W.Z., and Ong T.M. Oncogenic potential of mouse translation elongation factor-1 delta, a novel cadmium-responsive proto-oncogene. J. Biol. Chem. 277 (2002) 6131-6136
37. Joseph P., Lei Y.X., and Ong T.M. Up-regulation of expression of translation factors-a novel molecular mechanism for cadmium carcinogenesis. Mol. Cell. Biochem. 255 (2004) 93-101
38. Joseph P., O'Kernick C.M., Othumpangat S., Lei Y.X., Yuan B.Z., and Ong T.M. Expression profile of eukaryotic translation factors in human cancer tissues and cell lines. Mol. Carcinog. 40 (2004) 171-179
39. Jurczuk M., Brzoska M.M., Moniuszko-Jakoniuk J., Galazyn-Sidorczuk M., and Kulikowska-Karpinska E. Antioxidant enzymes activity and lipid peroxidation in liver and kidney of rats exposed to cadmium and ethanol. Food Chem. Toxicol. 42 (2004) 429-438
40. Kamata H., and Hirata H. Redox regulation of cellular signalling. Cell. Signal. 11 (1999) 1-14
41. Keshava N., Zhou G., Hubbs A.F., Ensell M.X., and Ong T. Transforming and carcinogenic potential of cadmium chloride in BALB/c-3T3 cells. Mutat. Res. 448 (2000) 23-28
42. Kim J., and Sharma R.P. Cadmium-induced apoptosis in murine macrophages is antagonized by antioxidants and caspase inhibitors. J. Toxicol. Environ. Health 69 (2006) 1181-1201
43. Klaassen C.D., and Liu J. Metallothionein transgenic and knock-out mouse models in the study of cadmium toxicity. J. Toxicol. Scie. 23 Suppl. 2 (1998) 97-102
44. Kondoh M., Araragi S., Sato K., Higashimoto M., Takiguchi M., and Sato M. Cadmium induces apoptosis partly via caspase-9 activation in HL-60 cells. Toxicology 170 (2002) 111-117
45. Koyuturk M., Yanardag R., Bolkent S., and Tunali S. The potential role of combined anti-oxidants against cadmium toxicity on liver of rats. Toxicol. Ind. Health 23 (2007) 393-401
46. Lag M., Westly S., Lerstad T., Bjornsrud C., Refsnes M., and Schwarze P.E. Cadmium-induced apoptosis of primary epithelial lung cells: involvement of Bax and p53, but not of oxidative stress. Cell Biol. Toxicol. 18 (2002) 29-42
47. Lee M.J., Nishio H., Ayaki H., Yamamoto M., and Sumino K. Upregulation of stress response mRNAs in COS-7 cells exposed to cadmium. Toxicology 174 (2002) 109-117
48. Lee D.H., Lim J.S., Song K., Boo Y., and Jacobs Jr. D.R. Graded associations of blood lead and urinary cadmium concentrations with oxidative-stress-related markers in the U.S. population: results from the third National Health and Nutrition Examination Survey. Environ. Health Perspect. 114 (2006) 350-354
49. Lewinska D., Arkusz J., Stanczyk M., Palus J., Dziubaltowska E., and Stepnik M. Comparison of the effects of arsenic and cadmium on benzo(a)pyrene-induced micronuclei in mouse bone-marrow. Mutat. Res. 632 (2007) 37-43
50. Li Q., Hu N., Daggett M.A., Chu W.A., Bittel D., Johnson J.A., and Andrews G.K. Participation of upstream stimulator factor (USF) in cadmium-induction of the mouse metallothionein-I gene. Nucleic Acids Res. 26 (1998) 5182-5189
51. Li G.Y., Kim M., Kim J.H., Lee M.O., Chung J.H., and Lee B.H. Gene expression profiling in human lung fibroblast following cadmium exposure. Food Chem. Toxicol. 46 (2008) 1131-1137
52. Liao V.H., and Freedman J.H. Cadmium-regulated genes from the nematode Caenorhabditis elegans. Identification and cloning of new cadmium-responsive genes by differential display. J. Biol. Chem. 273 (1998) 31962-31970
53. Liu F., and Jan K.Y. DNA damage in arsenite- and cadmium-treated bovine aortic endothelial cells. Free Radic. Biol. Med. 28 (2000) 55-63
54. Liu J., Corton C., Dix D.J., Liu Y., Waalkes M.P., and Klaassen C.D. Genetic background but not metallothionein phenotype dictates sensitivity to cadmium-induced testicular injury in mice. Toxicol. Appl. Pharmacol. 176 (2001) 1-9
55. Livneh E., and Fishman D.D. Linking protein kinase C to cell-cycle control. Eur. J. Biochem./FEBS 248 (1997) 1-9
56. Maki A., Berezesky I.K., Fargnoli J., Holbrook N.J., and Trump B.F. Role of [Ca2+]i in induction of c-fos, c-jun, and c-myc mRNA in rat PTE after oxidative stress. Faseb J. 6 (1992) 919-924
57. Mannino D.M., Holguin F., Greves H.M., Savage-Brown A., Stock A.L., and Jones R.L. Urinary cadmium levels predict lower lung function in current and former smokers: data from the Third National Health and Nutrition Examination Survey. Thorax 59 (2004) 194-198
58. Mikhailova M.V., Littlefield N.A., Hass B.S., Poirier L.A., and Chou M.W. Cadmium-induced 8-hydroxydeoxyguanosine formation, DNA strand breaks and antioxidant enzyme activities in lymphoblastoid cells. Cancer Lett. 115 (1997) 141-148
59. Minami A., Takeda A., Nishibaba D., Takefuta S., and Oku N. Cadmium toxicity in synaptic neurotransmission in the brain. Brain Res. 894 (2001) 336-339
60. Misra R.R., Crance K.A., Bare R.M., and Waalkes M.P. Lack of correlation between the inducibility of metallothionein mRNA and metallothionein protein in cadmium-exposed rodents. Toxicology 117 (1997) 99-109
61. Misra R.R., Smith G.T., and Waalkes M.P. Evaluation of the direct genotoxic potential of cadmium in four different rodent cell lines. Toxicology 126 (1998) 103-114
62. 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
63. Momose Y., and Iwahashi H. Bioassay of cadmium using a DNA microarray: genome-wide expression patterns of Saccharomyces cerevisiae response to cadmium. Environ. Toxicol. Chem. 20 (2001) 2353-2360
64. Morimoto R.I., Tissieres A., and Georgopoulos C. The Biology of Heat Shock Proteins and Molecular Chaperons (1994), CSHL Press, New York, NY
65. Mukherjee J.J., Gupta S.K., and Kumar S. Inhibition of benzopyrene diol epoxide-induced apoptosis by cadmium(II) is AP-1-independent: role of extracelluler signal related kinase. Chem.-Biol. Interact. 172 (2008) 72-80
66. Muller R.M., Taguchi H., and Shibahara S. Nucleotide sequence and organization of the rat heme oxygenase gene. J. Biol. Chem. 262 (1987) 6795-6802
67. Nigam D., Shukla G.S., and Agarwal A.K. Glutathione depletion and oxidative damage in mitochondria following exposure to cadmium in rat liver and kidney. Toxicol. Lett. 106 (1999) 151-157
68. O'Connor T.R., Graves R.J., de Murcia G., Castaing B., and Laval J. Fpg protein of Escherichia coli is a zinc finger protein whose cysteine residues have a structural and/or functional role. J. Biol. Chem. 268 (1993) 9063-9070
69. Obara N., Imagawa S., Nakano Y., Suzuki N., Yamamoto M., and Nagasawa T. Suppression of erythropoietin gene expression by cadmium depends on inhibition of HIF-1, not stimulation of GATA-2. Arch. Toxicol. 77 (2003) 267-273
70. Ochi T., and Ohsawa M. Participation of active oxygen species in the induction of chromosomal aberrations by cadmium chloride in cultured Chinese hamster cells. Mutat. Res. 143 (1985) 137-142
71. Ogawa K., Utsunomiya T., Mimori K., Tanaka Y., Tanaka F., Inoue H., Murayama S., and Mori M. Clinical significance of elongation factor-1 delta mRNA expression in oesophageal carcinoma. Br. J. Cancer 91 (2004) 282-286
72. Othumpangat S., Kashon M., and Joseph P. Eukaryotic translation initiation factor 4E is a cellular target for toxicity and death due to exposure to cadmium chloride. J. Biol. Chem. 280 (2005) 25162-25169
73. Palus J., Rydzynski K., Dziubaltowska E., Wyszynska K., Natarajan A.T., and Nilsson R. Genotoxic effects of occupational exposure to lead and cadmium. Mutat. Res. 540 (2003) 19-28
74. Pesch B., Haerting J., Ranft U., Klimpel A., Oelschlagel B., and Schill W. Occupational risk factors for renal cell carcinoma: agent-specific results from a case-control study in Germany. MURC Study Group. Multicenter urothelial and renal cancer study. Int. J. Epidemiol. 29 (2000) 1014-1024
75. Potts R.J., Bespalov I.A., Wallace S.S., Melamede R.J., and Hart B.A. Inhibition of oxidative DNA repair in cadmium-adapted alveolar epithelial cells and the potential involvement of metallothionein. Toxicology 161 (2001) 25-38
76. Qu W., Diwan B.A., Reece J.M., Bortner C.D., Pi J., Liu J., and Waalkes M.P. Cadmium-induced malignant transformation in rat liver cells: role of aberrant oncogene expression and minimal role of oxidative stress. Int. J. Cancer 114 (2005) 346-355
77. Ren X.Y., Zhou Y., Zhang J.P., Feng W.H., and Jiao B.H. Metallothionein gene expression under different time in testicular Sertoli and spermatogenic cells of rats treated with cadmium. Reprod. Toxicol. (Elmsford, N.Y.) 17 (2003) 219-227
78. Rivedal E., and Sanner T. Metal salts as promoters of in vitro morphological transformation of hamster embryo cells initiated by benzo(a)pyrene. Cancer Res. 41 (1981) 2950-2953
79. Rossman T.G., and Roy N.K. Is cadmium genotoxic?. In: Norgberg G.F., Alessio L., and Herber R.F.M. (Eds). Cadmium in Human Environment: Toxicity and Carcinogenicity (1992), International Agency for Research on Cancer, Lyon 367-375
80. Sahmoun A.E., Case L.D., Jackson S.A., and Schwartz G.G. Cadmium and prostate cancer: a critical epidemiologic analysis. Cancer Investig. 23 (2005) 256-263
81. Schwartz G.G., and Reis I.M. Is cadmium a cause of human pancreatic cancer?. Cancer Epidemiol., Biomarkers Prev. 9 (2000) 139-145
82. Shih C.M., Wu J.S., Ko W.C., Wang L.F., Wei Y.H., Liang H.F., Chen Y.C., and Chen C.T. Mitochondria-mediated caspase-independent apoptosis induced by cadmium in normal human lung cells. J. Cell. Biochem. 89 (2003) 335-347
83. Shih C.M., Ko W.C., Wu J.S., Wei Y.H., Wang L.F., Chang E.E., Lo T.Y., Cheng H.H., and Chen C.T. Mediating of caspase-independent apoptosis by cadmium through the mitochondria-ROS pathway in MRC-5 fibroblasts. J. Cell. Biochem. 91 (2004) 384-397
84. Shih Y.L., Lin C.J., Hsu S.W., Wang S.H., Chen W.L., Lee M.T., Wei Y.H., and Shih C.M. Cadmium toxicity toward caspase-independent apoptosis through the mitochondria-calcium pathway in mtDNA-depleted cells. Ann. N. Y. Acad. Sci. 1042 (2005) 497-505
85. Shimada H., Shiao Y.H., Shibata M., and Waalkes M.P. Cadmium suppresses apoptosis induced by chromium. J. Toxicol. Environ. Health 54 (1998) 159-168
86. Shippee R.L., Burgess D.H., Ciavarra R.P., DiCapua R.A., and Stake P.E. Cadmium-induced suppression of the primary immune response and acute toxicity in mice: differential interaction of zinc. Toxicol. Appl. Pharmacol. 71 (1983) 303-306
87. Smirnova I.V., Bittel D.C., Ravindra R., Jiang H., and Andrews G.K. Zinc and cadmium can promote rapid nuclear translocation of metal response element-binding transcription factor-1. J. Biol. Chem. 275 (2000) 9377-9384
88. Tang N., and Enger M.D. Cd(2+)-induced c-myc mRNA accumulation in NRK-49F cells is blocked by the protein kinase inhibitor H7 but not by HA1004, indicating that protein kinase C is a mediator of the response. Toxicology 81 (1993) 155-164
89. Waalkes M.P. Cadmium carcinogenesis in review. J. Inorg. Biochem. 79 (2000) 241-244
90. Waalkes M.P. Cadmium carcinogenesis. Mutat. Res. 533 (2003) 107-120
91. Waalkes M.P., and Klaassen C.D. Concentration of metallothionein in major organs of rats after administration of various metals. Fundam. Appl. Toxicol. 5 (1985) 473-477
92. Waalkes M.P., and Rehm S. Cadmium and prostate cancer. J. Toxicol. Environ. Health 43 (1994) 251-269
93. Waalkes M.P., Perantoni A., and Rehm S. Tissue susceptibility factors in cadmium carcinogenesis. Correlation between cadmium-induction of prostatic tumors in rats and an apparent deficiency of metallothionein. Biol. Trace Elem. Res. 21 (1989) 483-490
94. Waalkes M.P., Rehm S., Riggs C.W., Bare R.M., Devor D.E., Poirier L.A., Wenk M.L., and Henneman J.R. Cadmium carcinogenesis in male Wistar [Crl:(WI)BR] rats: dose-response analysis of effects of zinc on tumor induction in the prostate, in the testes, and at the injection site. Cancer Res. 49 (1989) 4282-4288
95. Waalkes M.P., Coogan T.P., and Barter R.A. Toxicological principles of metal carcinogenesis with special emphasis on cadmium. Crit. Rev. Toxicol. 22 (1992) 175-201
96. Waalkes M.P., Rehm S., Perantoni A.O., and Coogan T.P. Cadmium exposure in rats and tumours of the prostate. IARC Sci. Publ. (1992) 391-400
97. 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
98. 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 58 (1999) 199-214
99. Waalkes M.P., Rehm S., and Cherian M.G. Repeated cadmium exposures enhance the malignant progression of ensuing tumors in rats. Toxicol. Sci. 54 (2000) 110-120
100. Waisberg M., Joseph P., Hale B., and Beyersmann D. Molecular and cellular mechanisms of cadmium carcinogenesis. Toxicology 192 (2003) 95-117
101. Wang Z., and Templeton D.M. Induction of c-fos proto-oncogene in mesangial cells by cadmium. J. Biol. Chem. 273 (1998) 73-79
102. Watjen W., and Beyersmann D. Cadmium-induced apoptosis in C6 glioma cells: influence of oxidative stress. BioMetals 17 (2004) 65-78
103. Watkin R.D., Nawrot T., Potts R.J., and Hart B.A. Mechanisms regulating the cadmium-mediated suppression of Sp1 transcription factor activity in alveolar epithelial cells. Toxicology 184 (2003) 157-178
104. Xie J., and Shaikh Z.A. Cadmium-induced apoptosis in rat kidney epithelial cells involves decrease in nuclear factor-kappa B activity. Toxicol. Sci. 91 (2006) 299-308
105. Xu G., Zhou G., Jin T., Zhou T., Hammarstrom S., Bergh A., and Nordberg G. Apoptosis and p53 gene expression in male reproductive tissues of cadmium exposed rats. BioMetals 12 (1999) 131-139
106. Yamada H., and Koizumi S. DNA microarray analysis of human gene expression induced by a non-lethal dose of cadmium. Ind. Health 40 (2002) 159-166
107. 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
108. Yuan C., Kadiiska M., Achanzar W.E., Mason R.P., and Waalkes M.P. Possible role of caspase-3 inhibition in cadmium-induced blockage of apoptosis. Toxicol. Appl. Pharmacol. 164 (2000) 321-329