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

Free Radical Research

Volumn 42, Issue 2, 2008, Pages 142-153

  Nzengue, Yves ^a   Steiman, Regine ^a   Guiraud, Pascale ^a  

^a UNIV GRENOBLE ALPES   (France)

Author keywords

Apoptosis; C6 cells; Cadmium; HaCaT cells; Metallothioneins; p53

Indexed keywords

CADMIUM; CASPASE 3; CASPASE 9; DNA FRAGMENT; METALLOTHIONEIN; PROTEIN P53;

ANIMAL CELL; ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; CELL DEATH; CONTROLLED STUDY; ENZYME ACTIVATION; GENE MUTATION; GLIA CELL; HUMAN; HUMAN CELL; KERATINOCYTE; NONHUMAN; OXIDATIVE STRESS; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; WILD TYPE;

ANIMALS; APOPTOSIS; CADMIUM; CASPASE 3; CASPASE 9; CELL DEATH; CELL LINE, TRANSFORMED; CELL LINE, TUMOR; CELL SURVIVAL; CYCLIN-DEPENDENT KINASE INHIBITOR P21; DNA FRAGMENTATION; HUMANS; METALLOTHIONEIN; RATS; TUMOR SUPPRESSOR PROTEIN P53;

RATTUS;

EID: 39749162754     PISSN: 10715762     EISSN: 10292470     Source Type: Journal    
DOI: 10.1080/10715760701837100     Document Type: Article

References (95)

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