Cellular vitamin C increases chromate toxicity via a death program requiring mismatch repair but not p53

Carcinogenesis

Volumn 28, Issue 7, 2007, Pages 1613-1620

  Reynolds, Mindy ^a   Zhitkovich, Anatoly ^a  

^a BROWN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ASCORBIC ACID; CHROMIC ACID; PROTEIN MUTL; PROTEIN MUTS; PROTEIN P53; SERINE; SHORT HAIRPIN RNA;

APOPTOSIS; ARTICLE; CELL CULTURE; CELL DEATH; CELL LEVEL; CELL PROTECTION; CELL SURVIVAL; CHEMICAL CARCINOGENESIS; CLONOGENESIS; CONTROLLED STUDY; CULTURE MEDIUM; CYTOTOXICITY; DNA ADDUCT; GENE EXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; LETHALITY; LUNG ALVEOLUS EPITHELIUM; LUNG CANCER; LUNG CARCINOGENESIS; LUNG FIBROBLAST; MISMATCH REPAIR; PHENOTYPE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REPORTER GENE; TOXICOKINETICS; WILD TYPE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; APOPTOSIS; ASCORBIC ACID; CELL SURVIVAL; CELLS, CULTURED; CHROMATES; DNA ADDUCTS; DNA MISMATCH REPAIR; HUMANS; LUNG; MUTATION; MUTS HOMOLOG 2 PROTEIN; NUCLEAR PROTEINS; PHOSPHORYLATION; POTASSIUM COMPOUNDS; TUMOR SUPPRESSOR PROTEIN P53;

EID: 34547732984     PISSN: 01433334     EISSN: 14602180     Source Type: Journal    
DOI: 10.1093/carcin/bgm031     Document Type: Article

References (50)

1. IARC (1990) Monographs on the evaluation of carcinogenic risks to humans, Chromium, Nickel and Welding, Vol. 49, World Health Organization, Lyon. pp. 49-256.
2. Sorahan,T. et al. (1998) Lung cancer mortality in nickel/chromium platers, 1946-95. Occup. Environ. Med., 55, 236-242.
3. Gibb,H.J. et al. (2000) Lung cancer among workers in chromium chemical production. Am. J. Ind. Med., 38, 115-126.
4. Zhitkovich,A. (2002) Chromium: Exposure, toxicity and biomonitoring approaches. In Wilson,S.H. and Suk,W.A. (eds.) Biomarkers of Environmentally Associated Disease: Technologies, Concepts, and Perspectives pp. 269-287.
5. Barchowsky,A. et al. (2003) Metal-induced cell signaling and gene activation in lung diseases. Free Radic. Biol. Med., 34, 1130-4135.
6. De Flora,S. (2000) Threshold mechanisms and site specificity in chromium(VI) carcinogenesis. Carcinogenesis, 21, 533-541.
7. Stern,A.H. (1998) The association of chromium in household dust with urinary chromium in residences adjacent to chromate production waste sites. Environ. Health Perspect., 106, 833-939.
8. O'Brien,T.J. et al. (2003) Complexities of chromium carcinogenesis: Role of cellular response, repair and recovery mechanisms. Mutat. Res., 533, 3-36.
9. Zhitkovich,A. (2005) Importance of chromium-DNA adducts in mutagenicity and toxicity of cbromium(VI). Chem. Res. Toxicol., 18, 3-11.
10. Standeven,A.M. et al. (1992) Ascorbate is the principal reductant of chromium(VI) in rat lung ultrafiltrates and cytosols, and mediates chromium-DNA binding in vitro. Carcinogenesis, 13, 1319-1324.
11. Standeven,A.M. et al. (1991) Ascorbate is the principal reductant of chromium(VI) in rat liver and kidney ultrafiltrates. Carcinogenesis, 12, 1733-1737.
12. Quievryn,G. et al. (2003) Genotoxicity and mutagenicity of chroniium(VI)/ascorbate-generated DNA adducts in human and bacterial cells. Biochemistry, 42, 1062-1070.
13. Quievryn,G. et al. (2002) Carcinogenic chromium(VI) induces cross-linking of vitamin C to DNA in vitro and in human lung A549 cells. Biochemistry, 41, 3156-3167.
14. O'Brien,T. et al. (2002) Critical role of chromium (Cr)-DNA interactions in the formation of Cr-induced polymerase arresting lesions. Biochemistry, 41, 12529-12537.
15. Quievryn,G. et al. (2006) Lower mutagenicity but higher stability of Cr-DNA adducts formed during gradual chromate activation with ascorbate. Carcinogenesis, 27, 2316-2321.
16. Reynolds,M. et al. (2007) Ascorbate acts as a highly potent inducer of chromate mutagenesis and clastogenesis: Linkage to DNA breaks in G2 phase by mismatch repair. Nucleic Acids Res., 35, 465-476.
17. Peterson-Roth,E. et al. (2005) Mismatch repair proteins are activators of toxic responses tp chromium-DNA damage. Mol. Cell Biol. 25, 3596-3607.
18. Zhitkovich,A. et al. (2005) Killing of chromium-damaged cells by migmatch repair and its relevance to carcinogenesis. Cell Cycle, 4, 1050-1052.
19. Wang,S. et al. (2001) Mechanisms of Cr(VI)-induced p53 activation: the role of phosphorylation, mdm2 and ERK. Carcinogenesis, 22 757-762.
20. Russo,P. et al. (2005) Molecular mechanisms of hexavalent chromium-induced apoptosis in human bronchoalveolar cells. Am. J. Respir. Cell Mol. Biol., 33, 589-600.
21. Kondo,K. et al. (1997) Mutations of the p53 gene in human lung cancer from chromate-exposed workers. Biochem. Biophys. Res. Commun. 239, 95-100.
22. Hirose,T. et al. (2002) Frequent microsatellite, instability in lung cancer from chromate-exposed workers. Mol. Carcinog., 33 172-180.
23. Takahashi,Y. et al. (2005) Microsatellite instability and protein expression of the DNA mismatch repair gene, hMLH1, of lung cancer in chromate-exposed workers. Mol. Carcinog., 42, 150-158.
24. Luo,Y. et al. (2004) ATM-mediated stabilization of hMutL DNA mismatch repair proteins augments p53 activation during DNA damage. Mol. Cell Biol., 24, 6430-16344.
25. Brummelkamp,T.R. et al. (2002) A system for stable expression of short interfering RNAs in mammalian cells. Science, 296, 550-553.
26. Reynolds,M. et al. (2004) Human nucleotide excision repair efficiently removes chromium-DNA phosphate adducts and protects cells against chromate toxicity. J. Biol. Chem., 279, 30419-30424.
27. Messer,J. et al. (2006) Causes of DNA single-strand breaks during reduction of chromate by glutathione in vitro and in cells. Free Radic. Biol. Med., 40, 1981-1992.
28. Slade,R. et al. (1985) Comparison of lung antioxidant levels in humans and laboratory animals. Am. Rev. Respir. Dis., 131, 742-746.
29. Karaczyn,A. et al. (2006) Ascorbate depletion mediates up-regulation of hypoxia-associated proteins by cell density and nickel. J. Cell Biochem, 97, 1025-1035.
30. Koh,W.S. et al. (1998) Differential effects and transport kinetics of ascorbate derivatives in leukemic cell lines. Anticancer Res., 18, 2487-2493.
31. Vera,J.C. et al. (1995) Resolution of the facilitated transport of dehydroascorbic acid from its intracellular accumulation as ascorbic acid. J. Biol. Chem., 270, 23706-23712.
32. Roos,W.P. et al. (2006) DNA damage-induced cell death by apoptosis. Trends Mol. Med., 12, 440-450.
33. Jiricny,J. (2006) The multifaceted mismatch-repair system. Nat. Rev. Mol. Cell. Biol., 7, 335-346.
34. Salnikow,K. et al. (2004) Depletion of intracellular ascorbate by the carcinogenic metals nickel and cobalt results in the induction of hypoxic stress. J. Biol. Chem., 279, 40337-40344.
35. Rumsey,S.C. et al. (1997) Glucose transporter isoforms GLUT1 and GLUT3 transport dehydroascorbic acid. J. Biol. Chem., 272, 18982-18989.
36. Carlisle,D.L. et al. (2000) Apoptosis and P53 induction in human lung fibroblasts exposed to chromium(VI): Effect of ascorbate and tocopherol. Toxicol. Sci., 55, 60-68.
37. Martin,B.D. et al. (2006) Ascorbate is a pro-oxidant in chromium-treated human lung cells. Mutat. Res., 610, 74-84.
38. Stearns,D.M. et al. (1994) Reaction of Cr(VI) with ascorbate produces chromium(V), chromium(IV), and carbon-based radicals. Chem. Res. Toxicol., 7, 219-230.
39. Lay,P.A. et al. (1998) Activation of molecular oxygen during the reactions of chromium(VI/V/IV) with biological reductants: Implications for chromium-induced genotoxicities. J. Am. Chem. Soc., 120, 6704-6714.
40. Papouli,E. et al. (2004) Dependence of the cytotoxicity of DNA-damaging agents on the mismatch repair status of human cells. Cancer Res., 64, 3391-3394.
41. Zhitkovich,A. et al. (1995) Glutathione and free amino acids form stable adducts with DNA following exposure of intact mammalian cells to chromate. Carcinogenesis, 16, 907-913.
42. Zhitkovich,A. et al. (1996) Formation of the amino acid-DNA complexes by hexavalent and trivalent chromium in vitro: importance of trivaterit chromium and the phosphate group. Biochemistry, 35, 7275-7282.
43. Lowe,S.W. et al. (1993) p53 is required for radiation-induced apoptosis in mouse thymocytes. Nature, 362, 847-849.
44. Zhang,D. et al. (2006) A role for the deubiquitinating enzyme USP28 in control of the DNA-damage response. Cell, 126, 529-542.
45. Flores,E.R. et al. (2002) p63 and p73 are required for p53-dependent apoptosis in response to DNA damage. Nature, 416 560-564.
46. Feng,L. et al. (2005) Functional analysis of the roles of posttranslational modifications at the p53 C terminus in regulating p53 stability and activity. Mol. Cell Biol., 25, 5389-5395.
47. Knights,C.D. et al. (2006) Distinct p53 acetylation, cassettes differentially influence gene-expression patterns and cell fate. J. Cell Biol., 173, 533-544.
48. Cadisle,D.L. et al. (2000) Chromium(VI) induces p53-dependent apoptosis in diploid human lung and mouse dermal fibroblasts. Mol. Carcinog., 28, 111-118.
49. Park,J.S. et al. (2001) Functional inactivation of p73, a homolog of p53, tumor suppressor protein, by human papillomavirus E6 proteins. Int. J. Cancer, 91, 822-827.
50. Shimodaira,H. et al. (2003) Interaction of mismatch repair protein PMS2 and the p53-related transcription factor p73 in apoptosis response to cisplatin. Proc. Natl. Acad. Sci. USA, 100, 2420-2425.