Characterization of the cell death induced by cadmium in HaCaT and C6 cell lines

References

• (IARC) Iafroc. Beryllium, cadmium, mercury, and exposures in the glass manufacturing industry. In: International Agency for Research on Cancer Monographs on the Evaluation of Carcinogenic Risks to humans. Lyon: IARC Scientific Publications; 1993;58:119–237.
   Google Scholar
• Oh SH, Lim SC. A rapid and transient ROS generation by cadmium triggers apoptosis via caspase-dependent pathway in HepG2 cells and this is inhibited through N-acetylcysteine-mediated catalase upregulation. Toxicol Appl Pharmacol 2006; 212: 212–223
   PubMed Web of Science ®Google Scholar
• Aronis A, Melendez JA, Golan O, Shilo S, Dicter N, Tirosh O. Potentiation of Fas-mediated apoptosis by attenuated production of mitochondria-derived reactive oxygen species. Cell Death Different 2003; 10: 335–344
   PubMed Web of Science ®Google Scholar
• Asmuss M, Mullenders LH, Eker A, Hartwig A. Differential effects of toxic metal compounds on the activities of Fpg and XPA, two zinc finger proteins involved in DNA repair. Carcinogenesis 2000; 21: 2097–2104
   PubMed Web of Science ®Google Scholar
• Kumar R, Agarwal AK, Seth PK. Oxidative stress-mediated neurotoxicity of cadmium. Toxicol Lett 1996; 89: 65–69
   PubMed Web of Science ®Google Scholar
• Mattie MD, Freedman JH. Protective effects of aspirin and vitamin E (alpha-tocopherol) against copper- and cadmium-induced toxicity. Biochem Biophys Res Comm 2001; 285: 921–925
   PubMed Web of Science ®Google Scholar
• Poliandri AH, Cabilla JP, Velardez MO, Bodo CC, Duvilanski BH. Cadmium induces apoptosis in anterior pituitary cells that can be reversed by treatment with antioxidants. Toxicol Appl Pharmacol 2003; 190: 17–24
   PubMed Web of Science ®Google Scholar
• Pourahmad J, O'Brien PJ. A comparison of hepatocyte cytotoxic mechanisms for Cu2+ and Cd2 + . Toxicology 2000; 143: 263–273
   PubMed Web of Science ®Google Scholar
• Szuster-Ciesielska A, Stachura A, Slotwinska M, Kaminska T, Sniezko R, Paduch R, Abramczyk D, Filar J, Kandefer-Szerszen M. The inhibitory effect of zinc on cadmium-induced cell apoptosis and reactive oxygen species (ROS) production in cell cultures. Toxicology 2000; 145: 159–171
   PubMed Web of Science ®Google Scholar
• Watjen W, Beyersmann D. Cadmium-induced apoptosis in C6 glioma cells: influence of oxidative stress. Biometals 2004; 17: 65–78
   PubMed Web of Science ®Google Scholar
• Raff MC, Barres BA, Burne JF, Coles HS, Ishizaki Y, Jacobson MD. Programmed cell death and the control of cell survival: lessons from the nervous system. Science 1993; 262: 695–700
   PubMed Web of Science ®Google Scholar
• Afford S, Randhawa S. Apoptosis. Mol Pathol 2000; 53: 55–63
   PubMedGoogle Scholar
• Neurath MF, Finotto S, Fuss I, Boirivant M, Galle PR, Strober W. Regulation of T-cell apoptosis in inflammatory bowel disease: to die or not to die, that is the mucosal question. Trends Immunol 2001; 22: 21–26
   PubMed Web of Science ®Google Scholar
• Rich T, Stephens R, Trowsdale J. MHC linked genes associated with apoptosis/programmed cell death. Biochem Soc Trans 1999; 27: 781–785
   PubMed Web of Science ®Google Scholar
• Agnantis NJ Goussia AC [Apoptosis and cancer]. Bull l'Acad Natl Med 1999;183:277–286; discussion 277–286.
   PubMed Web of Science ®Google Scholar
• Barinaga M. Is apoptosis key in Alzheimer's disease?. Science 1998; 281: 1303–1304
   PubMed Web of Science ®Google Scholar
• Coutant A, Lebeau J, Bidon-Wagner N, Levalois C, Lectard B, Chevillard S. Cadmium-induced apoptosis in lymphoblastoid cell line: involvement of caspase-dependent and -independent pathways. Biochimie 2006; 88: 1815–1822
   PubMed Web of Science ®Google Scholar
• Lag M, Refsnes M, Lilleaas EM, Holme JA, Becher R, Schwarze PE. Role of mitogen activated protein kinases and protein kinase C in cadmium-induced apoptosis of primary epithelial lung cells. Toxicology 2005; 211: 253–264
   PubMed Web of Science ®Google Scholar
• Lee WK, Bork U, Gholamrezaei F, Thevenod F. Cd(2 + )-induced cytochrome c release in apoptotic proximal tubule cells: role of mitochondrial permeability transition pore and Ca(2 + ) uniporter. Am J Physiol 2005; 288: F27–F39
   Google Scholar
• Lemarie A, Lagadic-Gossmann D, Morzadec C, Allain N, Fardel O, Vernhet L. Cadmium induces caspase-independent apoptosis in liver Hep3B cells: role for calcium in signaling oxidative stress-related impairment of mitochondria and relocation of endonuclease G and apoptosis-inducing factor. Free Radic Biol Med 2004; 36: 1517–1531
   PubMed Web of Science ®Google Scholar
• Waisberg M, Joseph P, Hale B, Beyersmann D. Molecular and cellular mechanisms of cadmium carcinogenesis. Toxicology 2003; 192: 95–117
   PubMed Web of Science ®Google Scholar
• Zhou T, Zhou G, Song W, Eguchi N, Lu W, Lundin E, Jin T, Nordberg G. Cadmium-induced apoptosis and changes in expression of p53, c-jun and MT-I genes in testes and ventral prostate of rats. Toxicology 1999; 142: 1–13
   PubMed Web of Science ®Google Scholar
• Kim DK, Baek JH, Kang CM, Yoo MA, Sung JW, Chung HY, Kim ND, Choi YH, Lee SH, Kim KW. Apoptotic activity of ursolic acid may correlate with the inhibition of initiation of DNA replication. Int J Cancer 2000; 87: 629–636
   PubMed Web of Science ®Google Scholar
• Earnshaw WC, Martins LM, Kaufmann SH. Mammalian caspases: structure, activation, substrates, and functions during apoptosis. Ann Rev Biochem 1999; 68: 383–424
   PubMed Web of Science ®Google Scholar
• Bargonetti J, Manfredi JJ. Multiple roles of the tumor suppressor p53. Curr Opin Oncol 2002; 14: 86–91
   PubMed Web of Science ®Google Scholar
• Wang Y, Rosengarth A, Luecke H. Structure of the human p53 core domain in the absence of DNA. Acta Crystallograph 2007; 63: 276–281
   Google Scholar
• Levine AJ. p53, the cellular gatekeeper for growth and division. Cell 1997; 88: 323–331
   PubMed Web of Science ®Google Scholar
• May P, May E. Twenty years of p53 research: structural and functional aspects of the p53 protein. Oncogene 1999; 18: 7621–7636
   PubMed Web of Science ®Google Scholar
• Cao F, Zhou T, Simpson D, Zhou Y, Boyer J, Chen B, Jin T, Cordeiro-Stone M, Kaufmann W. p53-Dependent but ATM-independent inhibition of DNA synthesis and G2 arrest in cadmium-treated human fibroblasts. Toxicol Appl Pharmacol 2007; 218: 174–185
   PubMed Web of Science ®Google Scholar
• Lavin MF, Gueven N. The complexity of p53 stabilization and activation. Cell Death Different 2006; 13: 941–950
   PubMed Web of Science ®Google Scholar
• Thompson CB. Apoptosis in the pathogenesis and treatment of disease. Science 1995; 267: 1456–1462
   PubMed Web of Science ®Google Scholar
• Oberhammer F, Wilson JW, Dive C, Morris ID, Hickman JA, Wakeling AE, Walker PR, Sikorska M. Apoptotic death in epithelial cells: cleavage of DNA to 300 and/or 50 kb fragments prior to or in the absence of internucleosomal fragmentation. EMBO J 1993; 12: 3679–3684
   PubMed Web of Science ®Google Scholar
• Kaufmann SH, Mesner PW, Jr, Samejima K, Tone S, Earnshaw WC. Detection of DNA cleavage in apoptotic cells. Meth Enzymol 2000; 322: 3–15
   PubMed Web of Science ®Google Scholar
• Wyllie AH. Glucocorticoid-induced thymocyte apoptosis is associated with endogenous endonuclease activation. Nature 1980; 284: 555–556
   PubMed Web of Science ®Google Scholar
• Friedline JA, Garrett SH, Somji S, Todd JH, Sens DA. Differential expression of the MT-1E gene in estrogen-receptor-positive and -negative human breast cancer cell lines. Am J Pathol 1998; 152: 23–27
   PubMed Web of Science ®Google Scholar
• Hamada T, Tanimoto A, Sasaguri Y. Apoptosis induced by cadmium. Apoptosis 1997; 2: 359–367
   PubMed Web of Science ®Google Scholar
• Jin R, Bay BH, Chow VT, Tan PH, Lin VC. Metallothionein 1E mRNA is highly expressed in oestrogen receptor-negative human invasive ductal breast cancer. Br J Cancer 2000; 83: 319–323
   PubMed Web of Science ®Google Scholar
• Coyole P, Philcox JC, Carey JC, Rofe AM. Metallothionein: the multipurpose protein. Cell Mol Life Sci 2002; 59: 627–647
   PubMed Web of Science ®Google Scholar
• Fusenig NE, Boukamp P. Multiple stages and genetic alterations in immortalization, malignant transformation, and tumor progression of human skin keratinocytes. Mol Carcinogen 1998; 23: 144–158
   PubMed Web of Science ®Google Scholar
• Benda P, Lightbody J, Sato G, Levine L, Sweet W. Differentiated rat glial cell strain in tissue culture. Science 1968; 161: 370–371
   PubMed Web of Science ®Google Scholar
• Lightbody J. Establishment of differentiated clonal strains of glial brain cells in culture. Fed Proc 1968;27.
   Google Scholar
• Mouret S, Favier A, Beani JC, Leccia MT. Differential p53-mediated responses to solar-simulated radiation in human papillomavirus type 16-infected keratinocytes. Exp Dermatol 2007; 16: 476–484
   PubMed Web of Science ®Google Scholar
• Selivanova G, Iotsova V, Kiseleva E, Strom M, Bakalkin G, Grafstrom RC, Wiman KG. The single-stranded DNA end binding site of p53 coincides with the C-terminal regulatory region. Nucl Acids Res 1996; 24: 3560–3567
   PubMed Web of Science ®Google Scholar
• Selivanova G, Iotsova V, Okan I, Fritsche M, Strom M, Groner B, Grafstrom RC, Wiman KG. Restoration of the growth suppression function of mutant p53 by a synthetic peptide derived from the p53 C-terminal domain. Nat Med 1997; 3: 632–638
   PubMed Web of Science ®Google Scholar
• Selivanova G, Ryabchenko L, Jansson E, Iotsova V, Wiman KG. Reactivation of mutant p53 through interaction of a C-terminal peptide with the core domain. Mol Cell Biol 1999; 19: 3395–3402
   PubMed Web of Science ®Google Scholar
• Komarov PG, Komarova EA, Kondratov RV, Christov-Tselkov K, Coon JS, Chernov MV, Gudkov AV. A chemical inhibitor of p53 that protects mice from the side effects of cancer therapy. Science 1999; 285: 1733–1737
   PubMed Web of Science ®Google Scholar
• Towbin H, Staehelin T, Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA 1979; 76: 4350–4354
   PubMed Web of Science ®Google Scholar
• McKeon TA, Lyman ML. Calcium ion improves electrophoretic transfer of calmodulin and other small proteins. Anal Biochem 1991; 193: 125–130
   PubMed Web of Science ®Google Scholar
• Mizzen CA, Cartel NJ, Yu WH, Fraser PE, McLachlan DR. Sensitive detection of metallothioneins-1, -2 and -3 in tissue homogenates by immunoblotting: a method for enhanced membrane transfer and retention. J Biochem Biophys Meth 1996; 32: 77–83
   PubMedGoogle Scholar
• Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970; 227: 680–685
   PubMed Web of Science ®Google Scholar
• LeGendre NM. Purification of proteins and peptides by SDS-PAGE. A practical guide to protein and peptide purification for microsequencing, PT Matsudaira. Academic Press, San Diego 1989; 49–69
   Google Scholar
• Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Meth 1983; 65: 55–63
   PubMed Web of Science ®Google Scholar
• Halliwell B. Oxidative stress and cancer: have we moved forward?. Biochem J 2007; 401: 1–11
   PubMed Web of Science ®Google Scholar
• Hashemi M, Ghavami S, Eshraghi M, Booy EP, Los M. Cytotoxic effects of intra and extracellular zinc chelation on human breast cancer cells. Eur J Pharmacol 2007; 557: 9–19
   PubMed Web of Science ®Google Scholar
• Barczyk K, Kreuter M, Pryjma J, Booy EP, Maddika S, Ghavami S, Berdel WE, Roth J, Los M. Serum cytochrome c indicates in vivo apoptosis and can serve as a prognostic marker during cancer therapy. Int J Cancer 2005; 116: 167–173
   PubMed Web of Science ®Google Scholar
• Hengartner MO. The biochemistry of apoptosis. Nature 2000; 407: 770–776
   PubMed Web of Science ®Google Scholar
• Maddika S, Booy EP, Johar D, Gibson SB, Ghavami S, Los M. Cancer-specific toxicity of apoptin is independent of death receptors but involves the loss of mitochondrial membrane potential and the release of mitochondrial cell-death mediators by a Nur77-dependent pathway. J Cell Sci 2005; 118: 4485–4493
   PubMed Web of Science ®Google Scholar
• Mignotte B, Vayssiere JL. Mitochondria and apoptosis. Eur J Biochem/FEBS 1998; 252: 1–15
   PubMedGoogle Scholar
• Vayssiere JL, Petit PX, Risler Y, Mignotte B. Commitment to apoptosis is associated with changes in mitochondrial biogenesis and activity in cell lines conditionally immortalized with simian virus 40. Proc Natl Acad Sci USA 1994; 91: 11752–11756
   PubMed Web of Science ®Google Scholar
• Watjen W, Haase H, Biagioli M, Beyersmann D. Induction of apoptosis in mammalian cells by cadmium and zinc. Environ Health Persp 2002; 110(Suppl 5)865–867
   PubMedGoogle Scholar
• Zamzami N, Susin SA, Marchetti P, Hirsch T, Gomez-Monterrey I, Castedo M, Kroemer G. Mitochondrial control of nuclear apoptosis. J Exp Med 1996; 183: 1533–1544
   PubMed Web of Science ®Google Scholar
• Joseph P, Muchnok TK, Klishis ML, Roberts JR, Antonini JM, Whong WZ, 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 2001; 61: 295–303
   PubMed Web of Science ®Google Scholar
• 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 2002; 14: 327–340
   PubMed Web of Science ®Google Scholar
• Boehning D, Patterson RL, Sedaghat L, Glebova NO, Kurosaki T, Snyder SH. Cytochrome c binds to inositol (1,4,5) trisphosphate receptors, amplifying calcium-dependent apoptosis. Nat Cell Biol 2003; 5: 1051–1061
   PubMed Web of Science ®Google Scholar
• Zhou T, Jia X, Chapin RE, Maronpot RR, Harris MW, Liu J, Waalkes MP, Eddy EM. Cadmium at a non-toxic dose alters gene expression in mouse testes. Toxicol Lett 2004; 154: 191–200
   PubMed Web of Science ®Google Scholar
• Green D, Kroemer G. The central executioners of apoptosis: caspases or mitochondria?. Trends Cell Biol 1998; 8: 267–271
   PubMed Web of Science ®Google Scholar
• Shih CM, Wu JS, Ko WC, Wang LF, Wei YH, Liang HF, Chen YC, Chen CT. Mitochondria-mediated caspase-independent apoptosis induced by cadmium in normal human lung cells. J Cell Biochem 2003; 89: 335–347
   PubMed Web of Science ®Google Scholar
• Yuan C, Kadiiska M, Achanzar WE, Mason RP, Waalkes MP. Possible role of caspase-3 inhibition in cadmium-induced blockage of apoptosis. Toxicol Appl Pharmacol 2000; 164: 321–329
   PubMed Web of Science ®Google Scholar
• Abarzua P, LoSardo JE, Gubler ML, Spathis R, Lu YA, Felix A, Neri A. Restoration of the transcription activation function to mutant p53 in human cancer cells. Oncogene 1996; 13: 2477–2482
   PubMed Web of Science ®Google Scholar
• Selivanova G. Mutant p53: the loaded gun. Curr Opin Invest Drugs. 2001; 2: 1136–1141
   PubMedGoogle Scholar
• Magal SS, Jackman A, Pei XF, Schlegel R, Sherman L. Induction of apoptosis in human keratinocytes containing mutated p53 alleles and its inhibition by both the E6 and E7 oncoproteins. Int J Cancer 1998; 75: 96–104
   PubMed Web of Science ®Google Scholar
• Kim AL, Raffo AJ, Brandt-Rauf PW, Pincus MR, Monaco R, Abarzua P, Fine RL. Conformational and molecular basis for induction of apoptosis by a p53 C-terminal peptide in human cancer cells. J Biol Chem 1999; 274: 34924–34931
   PubMed Web of Science ®Google Scholar
• Li Y, Mao Y, Rosal RV, Dinnen RD, Williams AC, Brandt-Rauf PW, Fine RL. Selective induction of apoptosis through the FADD/caspase-8 pathway by a p53 c-terminal peptide in human pre-malignant and malignant cells. Int J Cancer 2005; 115: 55–64
   PubMed Web of Science ®Google Scholar
• Li Y, Raffo AJ, Drew L, Mao Y, Tran A, Petrylak DP, Fine RL. Fas-mediated apoptosis is dependent on wild-type p53 status in human cancer cells expressing a temperature-sensitive p53 mutant alanine-143. Cancer Res 2003; 63: 1527–1533
   PubMed Web of Science ®Google Scholar
• Li Y, Rosal RV, Brandt-Rauf PW, Fine RL. Correlation between hydrophobic properties and efficiency of carrier-mediated membrane transduction and apoptosis of a p53 C-terminal peptide. Biochem Biophys Res Comm 2002; 298: 439–449
   PubMed Web of Science ®Google Scholar
• Rosal R, Brandt-Rauf P, Pincus MR, Wang H, Mao Y, Li Y, Fine RL. The role of alpha-helical structure in p53 peptides as a determinant for their mechanism of cell death: necrosis versus apoptosis. Adv Drug Deliv Rev 2005; 57: 653–660
   PubMed Web of Science ®Google Scholar
• Senatus PB, Li Y, Mandigo C, Nichols G, Moise G, Mao Y, Brown MD, Anderson RC, Parsa AT, Brandt-Rauf PW, Bruce JN, Fine RL. Restoration of p53 function for selective Fas-mediated apoptosis in human and rat glioma cells in vitro and in vivo by a p53 COOH-terminal peptide. Molec Cancer Ther 2006; 5: 20–28
   PubMed Web of Science ®Google Scholar
• Choi BM, Park R, Pae HO, Yoo JC, Kim YC, Jun CD, Jung BH, Oh GS, So HS, Kim YM, Chung HT. Cyclic adenosine monophosphate inhibits ursolic acid-induced apoptosis via activation of protein kinase A in human leukaemic HL-60 cells. Pharmacol Toxicol 2000; 86: 53–58
   PubMedGoogle Scholar
• el-Deiry WS, Tokino T, Velculescu VE, Levy DB, Parsons R, Trent JM, Lin D, Mercer WE, Kinzler KW, Vogelstein B. WAF1, a potential mediator of p53 tumor suppression. Cell 1993; 75: 817–825
   PubMed Web of Science ®Google Scholar
• Kim TK. In vitro transcriptional activation of p21 promoter by p53. Biochem Biophys Res Comm 1997; 234: 300–302
   PubMed Web of Science ®Google Scholar
• Waldman T, Kinzler KW, Vogelstein B. p21 is necessary for the p53-mediated G1 arrest in human cancer cells. Cancer Res 1995; 55: 5187–5190
   PubMed Web of Science ®Google Scholar
• Ko LJ, Prives C. p53: puzzle and paradigm. Genes Dev 1996; 10: 1054–1072
   PubMed Web of Science ®Google Scholar
• Caelles C, Helmberg A, Karin M. p53-dependent apoptosis in the absence of transcriptional activation of p53-target genes. Nature 1994; 370: 220–223
   PubMed Web of Science ®Google Scholar
• Gao C, Tsuchida N. Activation of caspases in p53-induced transactivation-independent apoptosis. Jpn J Cancer Res 1999; 90: 180–187
   PubMedGoogle Scholar
• Sansome C, Zaika A, Marchenko ND, Moll UM. Hypoxia death stimulus induces translocation of p53 protein to mitochondria. Detection by immunofluorescence on whole cells. FEBS Lett 2001; 488: 110–115
   PubMed Web of Science ®Google Scholar
• Polyak K, Xia Y, Zweier JL, Kinzler KW, Vogelstein B. A model for p53-induced apoptosis. Nature 1997; 389: 300–305
   PubMed Web of Science ®Google Scholar
• Marchenko ND, Zaika A, Moll UM. Death signal-induced localization of p53 protein to mitochondria. A potential role in apoptotic signaling. J Biol Chem 2000; 275: 16202–16212
   PubMed Web of Science ®Google Scholar
• Urani C, Melchioretto P, Canevali C, Crosta GF. Cytotoxicity and induction of protective mechanisms in HepG2 cells exposed to cadmium. Toxicol In Vitro 2005; 19: 887–892
   PubMed Web of Science ®Google Scholar
• Urani CM, Canevali PC, Morazzoni C, Gribaldo FL. Metallothionein and hsp70 expression in HepG2 cells after prolonged cadmium exposure. Toxicol In Vitro 2007; 21: 314–319
   PubMed Web of Science ®Google Scholar
• Andrews GK. Regulation of metallothionein gene expression by oxidative stress and metal ions. Biochem Pharmacol 2000; 59: 95–104
   PubMed Web of Science ®Google Scholar
• Fatur T, Tusek M, Falnoga I, Scancar J, Lah TT, Filipic M. DNA damage and metallothionein synthesis in human hepatoma cells (HepG2) exposed to cadmium. Food Chem Toxicol 2002; 40: 1069–1076
   PubMed Web of Science ®Google Scholar
• Hidalgo J, Aschner M, Zatta P, Vasak M. Roles of the metallothionein family of proteins in the central nervous system. Brain Res Bull 2001; 55: 133–145
   PubMed Web of Science ®Google Scholar
• Nordberg M. Metallothioneins: historical rewiew qnd state of knowledge. Talanta 1998; 46: 243–254
   PubMed Web of Science ®Google Scholar
• Penkowa M. Metallothioneins are multipurpose neuroprotectants during brain pathology. FEBS J 2006; 273: 1857–1870
   PubMed Web of Science ®Google Scholar
• West AK, Chuah MI, Vickers JC, Chung RS. Protective role of metallothioneins in the injured mammalian brain. Rev Neurosci 2004; 15: 157–166
   PubMed Web of Science ®Google Scholar