Review of chromium (VI) apoptosis, cell-cycle-arrest, and carcinogenesis

Journal of Environmental Science and Health - Part C Environmental Carcinogenesis and Ecotoxicology Reviews

Volumn 28, Issue 3, 2010, Pages 188-230

  Chiu, A ^a   Shi, X L ^b   Lee, W K P ^c   Hill, R ^c   Wakeman, T P ^d   Katz, A ^e   Xu, B ^f   Dalal, N S ^g   Robertson, J D ^h   Chen, C ^a   Chiu, N ^a   Donehower, L ⁱ  

^a U S ENVIRONMENTAL PROTECTION AGENCY   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

^c DALHOUSIE UNIVERSITY   (Canada)

^d DUKE UNIVERSITY   (United States)

^e ILLINOIS STATE UNIVERSITY   (United States)

^f HOUSTON METHODIST RESEARCH INSTITUTE   (United States)

^g FLORIDA STATE UNIVERSITY   (United States)

^h UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

ⁱ BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

apoptosis; chloride intracellular channel carrier; genomic plasticity; pentavalent chromium; senescence; somatic recombination; tetravalent chromium

Indexed keywords

APOPTOSIS; GENOMIC PLASTICITY; INTRACELLULAR CHANNEL; PENTAVALENT CHROMIUM; SENESCENCE; SOMATIC RECOMBINATION; TETRAVALENT CHROMIUM;

BIOGRAPHIES; CELL DEATH; CHLORINE COMPOUNDS; DNA; GENES; MITOCHONDRIA; PLASTICITY;

CHROMIUM;

CALPASTATIN; CASPASE 2; CHROMIUM; DNA BASE; FREE RADICAL; PROTEIN BAX; PROTEIN KINASE; PROTEIN P53; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; SUGAR;

APOPTOSIS; ATAXIA TELANGIECTASIA; CARCINOGENESIS; CELL CYCLE ARREST; CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CELL CYCLE S PHASE; CELL DAMAGE; CELL ORGANELLE; DNA DAMAGE; DNA REPAIR; DNA STRAND BREAKAGE; DOUBLE STRANDED DNA BREAK; GENETICS; HEREDITY; HETEROZYGOSITY; HOMOLOGOUS RECOMBINATION; HUMAN; HYDROXYLATION; MITOCHONDRION; MITOSIS; MITOTIC RECOMBINATION; NEOPLASM; NONHUMAN; REVIEW; SENESCENCE; SPECIES;

APOPTOSIS; CELL CYCLE; CELL TRANSFORMATION, NEOPLASTIC; CHROMIUM; HUMANS;

ATAXIA TELANGIECTASIA;

EID: 77957129631     PISSN: 10590501     EISSN: 15324095     Source Type: Journal    
DOI: 10.1080/10590501.2010.504980     Document Type: Review

References (142)

1. IARC Monograph on the Evaluation of Carcinogenic Risks to Humans: Chromium, Nickle and Welding. Lyon, France: IARC; 1990;49:389401.
2. NTP Technical Report on the Toxicology and Carcinogenesis Studies of Sodium Dichromate Dihydrate (CAS NO. 7789-12-0) in F344 Rats and B6C3F1 Mice (Drinking Water Studies). Research Triangle Park, NC: National Toxicology Program; July 2008.
3. Kerger BD, Paustenbach DJ, Corbett GE, Finley BL. Absorption and elimination of trivalent and hexavalent chromium in humans following ingestion of a bolus dose in drinking water. Toxicol Appl Pharmacol. 1996;41:145-158.
4. Connett PH,Wetterhahn KE. Metabolism of the carcinogenic chromate by cellular constituents. Struct Bend. 1983;54:93-124.
5. Buttner B, Beyersmann D. Modification of erythrocyte anion carrier by chromate. Xenobiotica. 1985;15:735-741.
6. Ulmasov B, Bruno J, Woost PG, Edwards JC. Tissue and subcellular distribution of CLCI1. BMC Cell Biol. 2007 Feb 27;8:8.
7. Cromer BA, Mottoa CJ, Board PG, Parker MW. From glutathione transferase to pore in a CLIC. Eur Biophys J. 2002;356-364.
8. Harrop SJ, DeMaerez MZ, Fairlie WD, Reztsova T, Valen-zuela SA, Mazzanti M, Tonini R, Qiu MR, Jankova L, Warton K, Bauskin AR, Wu WM, Pankurst S, Campell TJ, Breit SN, Curmi PMG. Crystal structure of a soluble form of the intracellular chloride ion channel CLIC (NCC27) at 1.4 Å resolution. J Biol Chem. 2001;276(48):44993-45000.
9. Gilbert HF. Adv Enzymol Relat Areas Mol Biol. 1990;63:69-172.
10. Shi X, Chiu A, Chen CT, Halliwell B, Castranova V, Vallyathan V. Reduction of chromium(VI) and its relationship to carcinogenesis. J Toxicol Environ Health B Crit Rev. 1999 Jan-Mar;2(1):87-104.
11. Dalal NS, Shi X. ESR evidence for the glutathionyl radical in die reduction of chromium-(VI) by glutathione. In: Medical, biomedical and chemical aspects of free radicals, Hayaishi O, Niki E, Konodo M, Yoshikawa T, eds. Amsterdam: Elsevier; 1989:547-550.
12. Shi X, Dalai NS. On the mechanism of the chromate reduction by glutathione: ESR evidence for the glutathionyl radical and err isolable Cr(V) intermediate. Biochem Biophys Res Common. 1988;156:137-142.
13. Bose RN, Moghaddas S, Gelerinter E. Long-lived chromium(V) and chromium(V) metabolites in the chromium(V1)-glutathione reaction: NMR, ESR, HPLC, and kinetic characterization. Inorg Chem. 1992;31:1987-1994.
14. Liu KJ, Shi X, Dalal NS. Synthesis of Cr(IV)-GSH, its identification and its free hydroxyl generation: a model compound for Cr(VI) carcinogenicity. Biochem Biophys Res Commun. 1997;235:54-58.
15. Cupo DY,Wetterhahn KE. Binding of chromium to chromatin and DNA from liver and kidney of rats treated with sodium dichromate and chromiurn (III) chloride in vivo. Cancer Res. 1985;45:1146-1151.
16. Cupo DY, Wetterhahn KE. Modification of chromium(VI)-induced DNA drainage by glutathione and cytochromes P-450 in chick embryo hepatocytes. Proc Natl Acad Sci USA. 1985;82:6755-6759.
17. Liebross RH, Wetterhahn KE. In vivo formation of chromium(V) in chick embryo red blood cells. Chem. Res, Toxicol. 1990;3:401-403.
18. Liebross RH, Wetterhahn KE. In vivo formation of chromium(V) in chick embryo liver and red blood cells. Carcinogenesis. 1992;13:2111-2120.
19. Liu KJ, Jiang J, Swartz HM, Shi X. Low-frequency EPR detection of chromium(V) formation by chromium(VI) reduction in whole live mice. Arch Biochem Biophys. 1994 Sep;313(2):248-252.
20. Rossi SC, Gorman N, Wetterhahn KE. Mitochondrial reduction of the carcinogen chromate: formation of chromium(V). Chem Res Toxicol. 1988;1(2):101-107.
21. Liu K, Shi X, Jiang JJ, Goda F, Dalal NS, Swath HM. Chromate-induced chromium(V) formation in live mice and its control by cellular antioxidants: An L-band EPR study. Arch Biochem Biophys. 1995;323:33-39.
22. Liu KJ, Shi X, Jiang JI. Docia F, Dalal NS, Swartz HM. Low frequency electron paramagnetic resonance investigation on metabolism of chromium(V1) by whole mice. Annu Clin Lab Sci. 1996;26:176-184.
23. Meister A, Anderson ME. Glutathione. Ann Rev Biochem. 1983;52:711-760.
24. Berry JP, Hourdry J, Galle P, Lagrue G. Chromium concentration by proximal renal tubule cells: and intrastructural, microanalytical and cytochemical study. J Histochemistry Cytochemistry. 1978;26(8):651-657.
25. Chiu A, Katz AJ, Beaubier J, Chiu N, Shi X. Genetic and cellular mechanisms in chromium and nickel carcinogenesis considering epidemiologic findings. Mol Cell Biochem. 2004;255:181-194.
26. Tsapakos MJ, Wetterhahn KE. The interaction of chromium with nucleic acids. Chem Biol Interact. 1983;46(2):265-277.
27. Jennette KE. Microsomal reduction of the carcinogen chromate produce chromium(V). J Am Chem Soc. 1982;104:874-875.
28. Shi X, Dalal Z, Gannett P. Chromate-mediated free radical generation from cysteine, penicillamine, hydrogen peroxide, and lipid hydroperoxides. Biochem Biophys Acta. 1994;1226:65-72.
29. Liu KJ., Shi X, Jiang JJ, Goda F, Dalal N, Swartz HM. Chromate-induced chromium(V) formation in live mice and its control by cellular antioxidants: An L0band electron paramagnetic resonance study. Arch Biochem Biophys. 1995;323:33-39.
30. Shi XG, Dalal NS. On the hydroxyl radical formation in the reaction between hydrogen peroxide and biologically generated chromium(V) species. Arch Biochem Biophys. 1990 Mar;277(2):342-350.
31. Shi X, Dalal NS. ESR spin trapping detection of hydroxyl radicals in the reaction of Cr(V) complexes with hydrogen peroxide. Free Radical Res Commun. 1990;10:17-26.
32. Shi X, Dalal NS. Evidence for a Fenton-type mechanism for the generation of OH radicals in the reduction of Cr(VI) in cellular media. Archim Biochem Biophys. 1990;277:342-350.
33. Shi X, Dalal NS. The role of Cr(V), the role of superoxide radical in chromium(VI) generated hydroxyl radical: The Cr(VI) Haber-Weiss cycle. Arch Biochem Biophy. 1992;292:323-327.
34. Sugden KD, Wetterhahn KE. Direct and hydrogen peroxide-induced chromium(V) oxidation of deoxyribose in single-stranded and double-stranded calf thymus DNA. Chem Res Toxicol. 1997;10(12):1397-1406.
35. Shi X,Mao Y, Knapton AD, Ding M, Rojanasakut Y, Gannett PM, Dalal NS, Liu K. Reaction of Cr(VI) with ascorbate and hydrogen peroxide generates hydroxyl radicals and cause DNA damage: Role of Cr(IV)-mediated Fenton-like reaction. Carcinogenesis. 1994;15:2475-2478.
36. Liu KJ, Shi X, Dalal NS. Synthesis of Cr(IV)-GSH, its identification and its free hydroxyl generation: A model compound for Cr(VI) carcinogenicity. Biochem Biophys Res Commun. 1997;235:54-58.
37. Luo H, Lu YD, Mao Y, Shi X, Dalal N. Role of chromium(IV) in the chromium(VI)- related free radical formation, dG hydroxylation and DNA damage. J Inorg Biochem. 1996;64:25-35.
38. Luo H, Lu Y, Shi X, Dalal NS. Chromium(IV)/H2O2 Fenton-like reaction cause DNA damage: implication to chromates genotoxicity. Ann Clin Lab Sci. 1996;26:185-191.
39. Ramsey CM, Dalal NS. Crystalline and water soluble Cr(4+) and Cr(5+) model compounds for chromium toxicity studies. Molecular and Cellular Biochemistry. 2004;255:113-118.
40. Dalal NS, Milar JM, JagadeeshMS, Seehra MS. Paramagnetic resonance and susceptibility of K3CrO8. J Chem Phys. 1981;74:1916-1923.
41. Cage B, Dalal NS. Unhydrated Cr(V) peroxychromates M3CrO8 (M = Na,K, Rb): Low-dimensional antiferromagnets exhibiting large specific heats at mK to 5 K temperatures. Chem Mat. 2001;13:880-890.
42. Cage B, Geyer W, Abboud KA, Dalal NS. Hydrated Cr(V) peroxychromates M3Cr O8. X H2O (M = Li, Na, Cs): Model 3d1 systems exhibiting linear chain behavior and antiferromagnetic interactions. Chem Mat. 2001;13:871-879.
43. Hamilton JW, Wetterhahn KF. Chromium(VI)-induced DNA-damage in check embryo liver and blood cells in vivo. Carcinogenesis. 1986;7:2085-2088.
44. Snyder RU. Role of active species in metal-induced DNA strand breakage in human diploid fibroblasts. Mutat Res. 1988;193:237-246.
45. Wakeman TP, Kim WJ, Callens S, Chiu A, Brown KD, Xu B. The ATM-SMC1 pathway is essential for activation of the chromium[VI] -induced S-phase checkpoint. Mutation Research. 2004;554:241-251.
46. Ha L, Ceryak S, Patierno SR. Generation of S phase-dependent DNA doublestrand break by Cr(VI) exposure: Involvement of ATM in Cr(VI) induction of gamma- H2AX. Carcinogenesis. 2004;25:2265-2274.
47. Kortenkamp A, Ozolins Z, Beyersmann D, OBrien P. Generation of PM2 DNA breaks in the course of reduction of chromium(VI) by glutathione. Muni Res. 1989;216(1):19-26.
48. Sugiyama M. Effects of vitamin E and vitamin 82 on chromate-induced DNA lesions. Biol Trace Elem Res. 1989;21:399-404.
49. Sugiyama M, Tsuzuki K, Ogura R. Effects of ascorbic acid on DNA damage, cytotoxicity, glutathione reductase, and formation of paramagnetic chromate in Chinese hamster V-79 cells treated with sodium(VI). I Biol Chem. 1991;266:3383-3386.
50. Shi X, Ding M, Ye J, Wang S, Leonard SS, Zang L, Castranova V, Vallyathan V, Chiu A, Dalal N, Liu K. Cr(IV) causes activation of nuclear transcription factor-kappa B, DNA strand breaks and dG hydroxylation via free radical reactions. J Inorg Biochim. 1999;75(1):37-44.
51. Dizadaroglu M. Chemical determination of free radical-induced damage to DNA. Free Radical Biol Med. 1991;10:225-242.
52. Sugden KD, Martin BD. Guanine and 7,8-dihydro-8-oxo-guanine-specific oxidation in DNA by chromium(V). Environ Health Perspect. 2002;110(Suppl 5):725-728.
53. Slade PG, HailerMK, Martin D, Sugden KD. Guanine-specific oxidation of doublestranded DNA by Cr(VI) and ascorbic acid forms spiroiminodihydantoin and 8-oxo-2- deoxyguanosine. Chem Res Toxicol. 2005;18(7):1140-1149.
54. Slade PG, Priestley ND, Sugden KD. Spiroiminodihydantoin as an oxo-atom transfer product of 8-oxo-2-deoxyguanosine oxidation by chromium(V). Org Lett. 2007;9:4411-4414.
55. Achanta G, Pelicano H, Feng L, Plunkett W, Huang P. Interaction of p53 and DNA-PK in response to nucleoside analogues: potential role as a sensor complex for DNA damage. Cancer Res. 2001;61:8723-8729.
56. Rinaldo C, Prodosmo A, Mancini F, Iacovelli S, Sacchi A, Moretti F, Soddu S. MDM2-regulated degradation of HIPK2 prevents p53Ser46 phosphorylation and DNA damage-induced apoptosis. Mol Cell. 2007;25:739-750.
57. Woo RA, McLure KG, Lees-Miller SP, Rancourt DE, Lee PW. DNA-dependent protein kinase acts upstream of p53 in response to DNA damage. Nature. 1998;394:700-704.
58. Bartek J, Bartkova J, Lukas J. DNA damage signaling guards against activated oncogenes and tumour progression. Oncogene. 2007;26(56):7773-7779.
59. Vaziri C, Saxena S, Jeon Y, Lee C, Murata K, Machida Y, Wagle N, Hwang DS, Dutta A. A p53-dependent checkpoint pathway prevents rereplication. Mol Cell. 2003;11:997-1008.
60. Taylor WR, Stark GR. Regulation of the G2/M transition by p53. Oncogene. 2001;20:1803-1815.
61. Vogelstein B, Lane D, Levine AJ. Surfing the p53 network. Nature. 2000;408:307-310.
62. Bartek J, Lukas J. Chk1 and Chk2 kinases in checkpoint control and cancer. Cancer Cell. 2003;3:421-429.
63. Lees-Miller SP, Chen YR, Anderson CW. Human cells contain a DNA-activated protein kinase that phosphorylates simian virus 40 T antigen, mouse p53, and the human Ku autoantigen. Mol Cell Biol.1990;10:6472-6481.
64. Shiloh Y. ATM and ATR: Networking cellular responses to DNA damage. Curr Opin Genet Dev. 2001;11:71-77.
65. Bakkenist CJ, Kastan MB. DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature. 2003;421:499-506.
66. Shiloh Y. ATM: From phenotype to functional genomics-and back. Ernst Schering Res Found Workshop. 2002;5:1-70.
67. Iijima K, Ohara M, Seki R, Tauchi H. Dancing on damaged chromatin: Functions of ATM and the RAD50/MRE11/NBS1 complex in cellular responses to DNA damage. J Radiat Res (Tokyo). 2008;49(5):451-464.
68. Satyanarayana A, Kaldis P. Mammalian cell-cycle regulation: Several Cdks, numerous cyclins and diverse compensatory mechanisms. Oncogene. 2009;28:2925-2939.
69. Zhao S, Weng YC, Yuan SS, Lin YT, Hsu HC, Lin SC, Gerbino E, Song MH, Zdzienicka MZ, Gatti RA, Shay JW, Ziv Y, Shiloh Y, Lee EY. Functional link between ataxia-telangiectasia and Nijmegen breakage syndrome gene products. Nature. 2000;405:473-477.
70. Willis N, Rhind N. Regulation of DNA replication by the S-phase damage checkpoint. Cell Division. 2009;4:13.
71. Falck J, Mailand N, Syljuasen RG, Bartek J, Likasm J. The ATM-Chk2- Cc1c25A checkpoint pathway guards against radioresistant DNA synthesis. Nature. 2001;410:842-847.
72. Bartek J, Falck J, Lukas J. CHK2 kinase-a busy messenger. Nat Rev Mol Cell Biol. 2001;2(12):877-886.
73. Kim ST, Xu B, Kastan MB. Involvement of the cohesion protein, Smcl, in Atmdependent and independent responses to DNA damage. Genes Dev. 2002;16:560-570.
74. Yazdi PT, Wang Y, Zhao S, Patel N, Lee EY, Qin J. SMC1 is a downstream effector in the ATM/NBS1 branch of the human S-phase checkpoint. Genes Dev. 2002;16:571-582.
75. Cimprich KA, Cortez D. ATR: An essential regulator of genomic integrity. Nat Rev Mol Cell Biol. 2008;9:616-627.
76. Kastan MB, Lim DS. The many substrates and functions of ATM. Mol Cell Biol Review. 2000;1(3):179-186.
77. Lal M, Bae D, Camilli TC, Patierno SR, Ceryak S. AKT1 mediates bypass of the G1/S checkpoint after genotoxic stress in normal human cells. Cell Cycle. 2009;8(10):1589-1602.
78. Adams KE, Medhurst AL, Dart DA, Lakin ND. Recruitment of ATR to sites of ionising radiation-induced DNA damage requires ATM and components ofMRN protein complex. Oncogene. 2006;25:3894-3904.
79. Myers JS, Cortez D. Rapid activation of ATR by ionizing radiation requires ATM and Mre11. J Biol Chem. 2006;281:9346-9350.
80. Wakeman TP, Xu B. ATR regulates hexavalent chromium-induced S-phase checkpoint through phosphorylation of SMC1. Mutat Res. 2006;610:14-20.
81. Kastan MB, Bartek J. Cell cycle checkpoints and cancer. Nature. 2004;432(7015):316-323.
82. Zhang Z, Leonard SS, Wang S, Vallyathan V, Castranova V, Shi X. Cr (VI) induces cell growth arrest through hydrogen peroxide-mediated reactions. Mol Cellular Biochem. 2001;222:77-83.
83. Hayashi Y, Kondo T, Zhao QL, Ogawa R, Cui ZG, Feril LB Jr, Teranishi H, Kasuya M. Signal transduction of p53-independent apoptotic pathway induced by hexavalent chromium in U937 cells. Toxicol Applied Pharmacol. 2004;197:96-106.
84. Wise SS, Holmes AL, Wise JP Sr. Hexavalent chromium-induced DNA damage and repair mechanisms. Rev Environ Health. 2008;23:39-57.
85. Weterings E, Chen DJ. DNA-dependent protein kinase in non-homologous end joining: A lock with multiple keys? Mini-review. J Cell Biology. 2007;179:183-186.
86. Shrivastav M, De Haro LP, Nickloff JA. Regulation of DNA double-strand break repair pathway choice. Review. Cell Research. 2008;18:134-147.
87. Graf U, Frei H, Kagi A, Katz AJ, Würgler FE. Thirty compounds tested in the Drosophila wing spot test. Mutat Res. 1989;22:359-373.
88. Graf U, Würgler FE. The somatic white-ivory eye spot test does not detect the same spectrum of genotoxic events as the wing somatic mutation and recombination test in Drosophila melanogaster. Environ Mol Mutagen. 1996;27:219-226.
89. Katz AJ, Chiu A, Beaubier J, Shi X. Combining Drosophila melanogaster somatic-mutation-recombination and electron-spin-resonance-spectroscopy data to interpret epidemiologic observations on chromium carcinogenicity. Mol Cell Biochem. 2001;222:61-68.
90. Spańo MA, Frei H, Würgler FE, Graf U. Recombinagenic activity of four compounds in the standard and high bioactivation crosses of Drosophila melanogaster in the wing spot test. Mutagenesis. 2001;16(5):385-394.
91. Sengstag C. The role of mitotic recombination in carcinogenesis. Crit Rev Toxicol. 1994;24:323-353.
92. Shammas MA, Reis RJS. Recombination and its role in DNA repair, cellular immortalization and cancer. Age. 1999;22:71-88.
93. Cavenee WK, White RL. The genetic basis of cancer. Sci Am. 1995;272:72-79.
94. Tischfield JA. Loss of heterozygosity or: How I learned to stop worrying and love mitotic recombination. Am J Hum Genet. 1997;61:995-999.
95. Shao C, Deng L, Henegariu O, Liang L, Stambrook PJ, Tischfield JA. Chromosomal instability contributes to loss of heterozygosity in mice lacking p53. Proc Natl Acad Sci USA. 2000;97:7405-7474
96. Kroemer G. The proto-oncogene Bcl-2 and its role in regulating apoptosis. Nature Med. 1997;36:614-620.
97. Kroemer G, Galluzzi L, Brenner C. Mitochondrial membrane permeabilization in cell death. Physiol Rev. 2007;87:99-163.
98. Green DR, Kroemer G. The pathophysiology of mitochondrial cell death. Sci. 2004;305:626-629.
99. Jimi S, Uchiyama M, Takaki A, Suzumiya J, Syuji H. Mechanism of cell death induced by cadmium and arsenic. Ann NY Acad Sci USA. 2004;1011:325-331.
100. Yoon YS, Cho HS, Lee H, Yoon G. Mitochondrial dysfunction via disruption of complex-II activity during iron chelation-induced senescence-like growth arrest of Chang cell. Ann NY Acad Sci. 2004;1011:123-132.
101. Baptiste-Okoh N, Barsotti AM, Prives C. Caspase 2 is both required for p53- mediated apoptosis and downregulated by p53 in a p21-dependent manner. Cell Cycle. 2008;7(9):1133-1138.
102. Vousden KH. p53 and PUMA: A deadly duo. Sci. 2005;309:1685-1686.
103. Tomita Y, Marchenko N, Nemajerova A, Dehner A, Klein C, Pan HG, Kessler H, Pancoska P, Moll UM. WTp53, but not tumor derived mutants, bind to Bcl2 via the DNA binding domain and induce mitochondrial permeabilization. J Biol Chem. 2006;281(13):8600-8606.
104. Mihara M, Erster S, Zaika A, Petrenko O, Chittenden T, Pancoska P, Moll UM. p53 has a direct apoptogenic role at the mitochondria. Mol Cell. 2003;11:577-590.
105. Mioll UM, Wolff S, Spiedel D, Deppert W. Transcription independent proapoptotic functions of p53. Curr Opinion Cell Bio. 2005;117:631-636.
106. Tomita Y, Marchenko N, Nemajerova A, Dehner A, Klein C, Pan HG, Kessler H, Pancoska P, Moll UM. WTp53, but not tumor derived mutants, bind to Bcl2 via the DNA binding domain and induce mitochondrial permeabilization. J Biol Chem. 2006;281(13):8600-8606.
107. Chen L,Willis SN,Wei A, Smith BJ, Fletcher JI, HindsMG, Colman PM, Day CL, Adams JM, Huang DCS. Differential targeting of prosurvival Bcl-2 proteins by their BH3-only ligands allows complementary apoptotic function. Mol Cell. 2005;17:393-403.
108. Kuwana T, Bouchier-Hayes L, Chipuk JE, Bonzon C, Sullivan BA, green DR, Newmeuyer DD. BH3 domains of BH3-only proteins differentially regulate Baxmediated mitochondrial membrane permeabilization both directly and indirectly. Mol Cell. 2005;17:525-535.
109. Susin SA, Zamzami N, Castedo M, Hirsch T, Marchetti P, Macho A, Daugas E, Geuskens M. Kroemer Bcl-2 inhibits the mitochondrial release of an apoptogenic process. J ExpMed. 1996;184:1331-1341.
110. Eskes R, Desagher S, Antonsson B, Martinou JC. Bid induces the oligomerization and insertion of Bax into the outer mitochondrial membrane. Mol Cell Biol. 2000;20(3):929-935.
111. Baptiste N, Prives C. p53 in the cytoplasm: A question of overkill. Cell. 2004;116(4):487-489.
112. Chipuk JE, Kuwana T, Bouchier-Hayes L, Droin NM, Newmeyer DD, Schuler M, Green DR. Direct activation of Bax by p53 mediates mitochondrial membrane permeabilization and apoptosis. Sci. 2003;303:1010-1014.
113. Chipuki JE, Bouchier-Hayes L, Kuwana T, Newmeyer DD, Green DR. PUMA couples the nuclear and cytoplasmic proapoptotic function of p53. Sci. 2005;309:1732-1735.
114. Guo Y, Srinivasula SM, Druilhe A, Fernandes-Alnemri T, Alnemri ES. Caspase-2 induces apoptosis by releasing proapoptotic proteins from mitochondria. J Biol Chem. 2002;277:13430-13437.
115. Gao Z, Shao Y, Jiang X. Essential roles of the Bcl-2 family of proteins in caspase- 2-induced apoptosis. J Biol Chem. 2005;280:38271-38275.
116. Wagner KW, Engels IH, Deveraux QL. Caspase-2 can function upstream of bid cleavage in the TRAIL apoptosis pathway. J Biol Chem. 2004;279:35047-35052.
117. Ye J, Wang S, Leonard SS, Sun Y, Butterworth L, Antonini J, Ding M, Rojanasakul Y, Vallyathan V, Castranova V, Shi X. Role of Reactive Oxygen Species and p53 in Chromium(VI)-induced Apoptosis. J Biol Chem. 1999;274(49):34974-34980.
118. Hayashi Y, Kondo T, Zhao QL, Ogawa R, Cui ZG, Feril LB Jr, Teranishi H, Kasuya M. Signal transduction of p53-independent apoptotic pathway induced by hexavalent chromium in U937 cells. Toxicol Applied Pharmacol. 2004;197:96-106.
119. Hill R, Leidal AM, Madureira PA, Gillis LD, Cochrane HK, Waisman DM, Chiu A, Lee PW. Hypersensitivity to chromium-induced DNA damage correlates with constitutive deregulation of upstream p53 kinases in p21-/- HCT116 colon cancer cells. DNA Repair. 2008;7(2):239-252.
120. Hill R, Leidal AM, Madureira PA, Gillis LD, Waisman DM, Chiu A, Lee PW. Chromium-mediated apoptosis: Involvement of DNA-dependent protein kinase (DNAPK) and differential induction of p53 target genes. DNA Repair. 2008;7(9):1484-1499.
121. Zhivotovsky B, Orrenius S. Caspase-2 function in response to DNA damage. Biochem Biophys Res Commun. 2005;331:859-867.
122. Robertson JD, Enoksson M, Suomela M, Zhivotovsky B, Orrenius, S. Caspase- 2 acts upstream of mitochondria to promote cytochrome c release during etoposideinduced apoptosis. J Biol Chem. 2002;277:29803-29809.
123. Ha L, Ceryak S, Patierno SR. Chromium (VI) activates ataxia telangiectasia mutated (ATM) protein. Request of ATM for both apoptosis & recovery from terminal growth arrest. J Biol Chem. 2003;278:17885-17894.
124. Shi M, Vivian CJ, Lee KJ, Ge C, Morotomi-Yano K, Manzl C, Bock F, Sato S, Tomomori-Sato C, Zhu R, Haug JS, Swanson SK, Washburn MP, Chen DJ, Chen BP, Villunger A, Florens L, Du C. DNA-PKcs-PIDDosome: a nuclear caspase-2-activating complex with role in G2/M checkpoint maintenance. Cell. 2009;136(3):508-520.
125. Tanaka T, Ohkubo S, Tatsuno I, Prives C. hCAS/CSE1L associates with chromatin and regulates expression of select p53 target genes. Cell. 2007;130:638-650.
126. Mattia M, Gottifredi V, McKinney K, Prives C. p53-dependent p21 mRNA elongation is impaired when DNA replication is stalled. Mol Cell Biol. 2006;1309-1320.
127. Espinosa JM, Emerson BM. Transcriptional regulation by p53 through intrinsic DNA/chromatin binding and site-directed cofactor recruitment. Mol Cell. 2001;8:57-69.
128. Espinosa JM, Verdun RE, Emerson BM. p53 functions through stress- and promoter-specific recruitment of transcription initiation components before and after DNA damage. Mol Cell. 2003;12:1015-1027.
129. Nowell PC. The clonal evolution of tumor cell populations. Sci. 1976;194:23-28.
130. Hanahan D, Weinberg RA. The hallmarks of cancer. Cell. 2000;100:57-70.
131. Loeb LA, Loeb KR, Anderson JP. Multiple mutations and cancer. Proc Acad Sci USA. 2003;110:776-781.
132. Stephens PJ, McBride DJ, Lin ML, Varela I, Pleasance ED, Simpson JT, Stebbings LA, Leroy C, Edkins S, Mudie LJ, Greenman CD, Jia M, Latimer C, Teague JW, Lau KW, Burton J, Quail MA, Swerdlow H, Churcher C, Natrajan R, Sieuwerts AM, Martens JW, Silver DP, Langerød A, Russnes HE, Foekens JA, Reis-Filho JS, van t Veer L, Richardson AL, Børresen-Dale AL, Campbell PJ, Futreal PA, Stratton MR. Complex landscape of somatic rearrangement in human breast cancer genome. Nature. 2009;462:1005-1010.
133. Harris AW, Pinkert CA, Crawford M, Langdon WY, Brinster RL, Adams JM. The Eμ-myc transgenic mouse. A model for high incidence spontaneous lymphoma and leukemia of early. B cells J Exp Med. 1988;167:353-371.
134. Dang CV, ODonnell KA, Zeller KI, Nguyen T, Osthus RC, Li F. The c-myc target gene network. Seminars in Cancer Biology. 2006;16:253-264.
135. Nair SK, Burley SK. X-ray structure of myc-max and mad-max recognizing DNA: Molecular basis of regulation by proto-oncogene transcription factors. Cell. 2003;112:193-205.
136. Evan GI, Vousden KH. Proliferation, cell cycle and apoptosis in cancer. Nature. 2001;411:342-348.
137. Herbst A, Hemann MT, Tworkowski KA, Salghetti SE, Lowe SW, Tansey WP. A conserved element in myc that negatively regulates its proapoptotic activity. EMBO Report. 2005;6(2):177-183.
138. Strasser A, Harris AW, Beth ML, Cory S. Novel primitive lymphoid tumors induced transgenic mice by cooperation between myc and bcl-2. Nature. 1990;348:331-333.
139. Vaux DL, Cory S, Adams JM. Bcl-2 gene promotes hematopoetic cell survival and cooperates with c-myc to immortalize pre-B cells. Nature. 1988;355:440-442.
140. Felsher DW, Bishop JM. Reversible tumorigenesis by myc in hematopoetic linkages. Mol Cell. 1999;4:199-207.
141. Ji L, Arcinas M, Boxer LM. NF-kappa B sites function as positive regulators of expression of the translocated c-myc allele in Burkitts lymphoma. Mol Cell Biol. 1994;14(12):7967-7974.
142. Flouds L. The histological analysis of tumors. A critical review. Am J Cancer. 1940;39:1-24.