Generation of S phase-dependent DNA double-strand breaks by Cr(VI) exposure: Involvement of ATM in Cr(VI) induction of γ-H2AX

Carcinogenesis

Volumn 25, Issue 11, 2004, Pages 2265-2274

  Ha, Linan ^a   Ceryak, Susan ^a   Patierno, Steven R ^a  

^a GEORGE WASHINGTON UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; CYCLINE; DOUBLE STRANDED DNA; HISTONE H2A; HISTONE H2AX GAMMA; SODIUM CHROMATE; UNCLASSIFIED DRUG; ZINOSTATIN;

ARTICLE; CELL CYCLE G1 PHASE; CELL CYCLE PHASE; CELL CYCLE S PHASE; CELL SYNCHRONIZATION; CHEMICAL CARCINOGENESIS; COMET ASSAY; CONTROLLED STUDY; DNA STRAND BREAKAGE; ENZYME ACTIVATION; FLOW CYTOMETRY; HUMAN; HUMAN CELL; HYPOTHESIS; IMMUNOCYTOCHEMISTRY; IMMUNOFLUORESCENCE; OCCUPATIONAL CARCINOGENESIS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RESPIRATORY TRACT CANCER;

ATAXIA TELANGIECTASIA; CELL CYCLE; CELL CYCLE PROTEINS; CELL SURVIVAL; CELLS, CULTURED; CHROMIUM; DNA DAMAGE; DNA-BINDING PROTEINS; FIBROBLASTS; HISTONES; HUMANS; PROTEIN-SERINE-THREONINE KINASES; S PHASE; SKIN; TUMOR SUPPRESSOR PROTEINS;

EID: 8844259700     PISSN: 01433334     EISSN: None     Source Type: Journal    
DOI: 10.1093/carcin/bgh242     Document Type: Article

References (52)

1. Xu,J., Bubley,G.J., Dettick,B., Blankenship,L.J. and Patierno,S.R. (1996) Chromium(VI) treatment of normal human lung cells results in guanine-specific DNA polymerase arrest, DNA-DNA cross-links and S-phase blockade of cell cycle. Carcinogenesis, 17, 1511-1517.
2. Singh,J., Bridgewater,L.C. and Patierno,S.R. (1998) Differential sensitivity of chromium-mediated DNA interstrand crosslinks and DNA-protein crosslinks to disruption by alkali and EDTA. Toxicol. Sci., 45, 72-76.
3. Bridgewater,L.C., Manning,F.C. and Patierno,S.R. (1994) Base-specific arrest of in vitro DNA replication by carcinogenic chromium: relationship to DNA interstrand crosslinking. Carcinogenesis 15, 2421-2427.
4. Singh,J., McLean,J.A., Pritchard,D.E., Montaser,A. and Patierno,S.R. (1998) Sensitive quantitation of chromium-DNA adducts by inductively coupled plasma mass spectrometry with a direct injection high-efficiency nebulizer. Toxicol. Sci., 46, 260-265.
5. Xu,J., Manning,F.C. and Patierno,S.R. (1994) Preferential formation and repair of chromium-induced DNA adducts and DNA-protein crosslinks in nuclear matrix DNA. Carcinogenesis, 15, 1443-1450.
6. Ueno,S., Kashimoto,T., Susa,N. et al. (2001) Detection of dichromate(VI)-induced DNA strand breaks and formation of paramagnetic chromium in multiple mouse organs. Toxicol. Appl. Pharmacol., 170, 56-62.
7. Werfel,U., Langen,V., Eickhoff,I., Schoonbrood,J., Vahrenholz,C., Brauksiepe,A., Popp,W. and Norpoth,K. (1998) Elevated DNA single-strand breakage frequencies in lymphocytes of welders exposed to chromium and nickel. Carcinogenesis, 19, 413-418.
8. Xu,J., Manning,F.C. and Patierno,S.R. (1994) Preferential formation and repair of chromium-induced DNA adducts and DNA-protein crosslinks in nuclear matrix DNA. Carcinogenesis, 15, 1443-1450.
9. Cox,M.M., Goodman,M.F., Kreuzer,K.N., Sherratt,D.J., Sandler,S.J. and Marians,K.J. (2000) The importance of repairing stalled replication forks. Nature, 404, 37-41.
10. Seigneur,M., Bidnenko,V., Ehrlich,S.D. and Michel,B. (1998) RuvAB acts at arrested replication forks. Cell, 95, 419-430.
11. Seigneur,M., Ehrlich,S.D. and Michel,B. (2000) RuvABC-dependent double-strand breaks in dnaBts mutants require recA. Mol. Microbiol., 38, 565-574.
12. Costanzo,V., Robertson,K., Bibikova,M., Kim,E., Grieco,D., Gottesman,M., Carroll,D. and Gautier,J. (2001) Mre11 protein complex prevents double-strand break accumulation during chromosomal DNA replication. Mol. Cell, 8, 137-147.
13. Michel,B., Ehrlich,S.D. and Uzest,M. (1997) DNA double-strand breaks caused by replication arrest. EMBO J., 16, 430-438.
14. Weitao,T., Budd,M., Hoopes,L.L. and Campbell,J.L. (2003) Dna2 helicase/nuclease causes replicative fork stalling and double-strand breaks in the ribosomal DNA of Saccharomyces cerevisiae. J. Biol. Chem., 278, 22513-22522.
15. O'Brien,T., Mandel,H.G., Pritchard,D.E. and Patierno,S.R. (2002) Critical role of chromium (Cr)-DNA interactions in the formation of Cr-induced polymerase arresting lesions. Biochemistry, 41, 12529-12537.
16. Bridgewater,L.C., Manning,F.C. and Patierno,S.R. (1998) Arrest of replication by mammalian DNA polymerases alpha and beta caused by chromium-DNA lesions. Mol. Carcinog., 23, 201-206.
17. Bridgewater,L.C., Manning,F.C., Woo,E.S. and Patierno,S.R. (1994) DNA polymerase arrest by adducted trivalent chromium. Mol. Carcinog., 9, 122-133.
18. Okada,S., Ohba,H. and Taniyama,M. (1981) Alterations in ribonucleic acid synthesis by chromium (III). J. Inorg. Biochem., 15, 223-231.
19. Ha,L., Ceryak,S. and Patierno,S.R. (2003) Chromium (VI) activates ataxia telangiectasia mutated (ATM) protein. Requirement of ATM for both apoptosis and recovery from terminal growth arrest. J. Biol. Chem., 278, 17885-17894.
20. Beamish,H., Williams,R., Chen,P., Khanna,K.K., Hobson,K., Watters,D., Shiloh,Y. and Lavin,M. (1996) Rapamycin resistance in ataxia-telangiectasia. Oncogene, 13, 963-970.
21. Kastan,M.B. and Lim,D.S. (2000) The many substrates and functions of ATM. Nature Rev. Mol. Cell. Biol., 1, 179-186.
22. Lee,S.A., Dritschilo,A. and Jung,M. (2001) Role of ATM in oxidative stress-mediated c-Jun phosphorylation in response to ionizing radiation and CdC12. J. Biol. Chem., 276, 11783-11790.
23. Zhang,Y., Ma,W.Y., Kaji,A., Bode,A.M. and Dong,Z. (2002) Requirement of ATM in UVA-induced signaling and apoptosis. J. Biol. Chem., 277, 3124-3131.
24. Thatcher,T.H. and Gorovsky,M.A. (1994) Phylogenetic analysis of the core histones H2A, H2B, H3 and H4. Nucleic Acids Res., 22 174-179.
25. West,M.H. and Bonner,W.M. (1980) Histone 2A, a heteromorphous family of eight protein species. Biochemistry, 19, 3238-3245.
26. Celeste,A., Petersen,S., Romanienko,P.J. et al. (2002) Genomic instability in mice lacking histone H2AX. Science, 296 922-927.
27. Rogakou,E.P., Pilch,D.R., Orr,A.H., Ivanova,V.S. and Bonner,W.M. (1998) DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J. Biol. Chem., 273, 5858-5868.
28. Rogakou,E.P., Boon,C., Redon,C. and Bonner,W.M. (1999) Megabase chromatin domains involved in DNA double-strand breaks in vivo. J. Cell Biol., 146, 905-916.
29. Celeste,A., Fernandez-Capetillo,O., Kruhlak,M.J., Pilch,D.R., Staudt,D.W., Lee,A., Bonner,R.F., Bonner,W.M. and Nussenzweig,A. (2003) Histone H2AX phosphorylation is dispensable for the initial recognition of DNA breaks. Nature Cell Biol., 5, 675-679.
30. Furuta,T., Takemura,H., Liao,Z.Y. et al. (2003) Phosphorylation of histone H2AX and activation of Mre11, Rad50 and Nbs1 in response to replication-dependent DNA double-strand breaks induced by mammalian DNA topoisomerase I cleavage complexes. J. Biol. Chem., 278, 20303-20312.
31. Paull,T.T., Rogakou,E.P., Yamazaki,V., Kirchgessner,C.U., Gellert,M. and Bonner,W.M. (2000) A critical role for histone H2AX in recruitment of repair factors to nuclear foci after DNA damage. Curr. Biol., 10, 886-895.
32. Burma,S., Chen,B.P., Murphy,M., Kurimasa,A. and Chen,D.J. (2001) ATM phosphorylates histone H2AX in response to DNA double-strand breaks. J. Biol. Chem., 276, 42462-42467.
33. Ward,I.M. and Chen,J. (2001) Histone H2AX is phosphorylated in an ATR-dependent manner in response to replicational stress. J. Biol. Chem., 276, 47759-47762.
34. Marko,N.F., Dieffenbach,P.B., Yan,G., Ceryak,S., Howell,R.W., McCaffrey,T.A. and Hu,V.W. (2003) Does metabolic radiolabeling stimulate the stress response? Gene expression profiling reveals differential cellular responses to internal beta vs. external gamma radiation. FASEB J., 17, 1470-1486.
35. Bravo,R., Frank,R., Blundell,P.A. and Macdonald-Bravo,H. (1987) Cyclin/PCNA is the auxiliary protein of DNA polymerase-delta. Nature, 326, 515-517.
36. Celisi.J.E., Madsen,P., Nielsen,S. and Celis,A. (1986) Nuclear patterns of cyclin (PCNA) antigen distribution subdivide S-phase in cultured cells - some applications of PCNA antibodies. Leuk. Res. 10, 237-249.
37. Cartman,C.E., Lim,D.S., Cimprich,K.A., Taya,Y., Tamai,K., Sakaguchi,K., Appella,E., Kastan,M.B. and Siliciano,J.D. (1998) Activation of the ATM kinase by ionizing radiation and phosphorylation of p53. Science, 281, 1677-1679.
38. Adamson,A.W., Kim,W.J., Shangary,S., Baskaran,R. and Brown,K.D. (2002) ATM is activated in response to N-methyl-N′-nitro-N-nitrosoguanidine-induced DNA alkylation. J. Biol. Chem., 277, 38222-38229.
39. Qian,Y., Jiang,B.H., Flynn,D.C., Leonard,S.S., Wang,S., Zhang,Z., Ye,J., Chen,F., Wang,L. and Shi,X. (2001) Cr(VI) increases tyrosine phosphorylation through reactive oxygen species-mediated reactions. Mol. Cell. Biochem., 222, 199-204.
40. Krepkiy,D., Antholine,W.E., Myers,C. and Petering,D.H. (2001) Model reactions of Cr(VI) with DNA mediated by thiol species. Mol. Cell. Biochem., 222, 213-219.
41. Liu,K., Husler,J., Ye,J. et al. (2001) On the mechanism of Cr(VI)-induced carcinogenesis: dose dependence of uptake and cellular responses. Mol. Cell. Biochem., 222, 221-229.
42. Bagchi,D., Bagchi,M. and Stohs,S.J. (2001) Chromium(VI)-induced oxidative stress, apoptotic cell death and modulation of p53 tumor suppressor gene. Mol. Cell. Biochem., 222, 149-158.
43. Zhang,Z., Leonard,S.S., Wang,S., Vallyathan,V., Castranova,V. and Shi,X. (2001) Cr(VI) induces cell growth arrest through hydrogen peroxide-mediated reactions. Mol. Cell. Biochem., 222, 77-83.
44. McGowan,C.H. (2003) Running into problems: how cells cope with replicating damaged DNA. Mutat. Res., 532, 75-84.
45. De Silva,I.U., McHugh,P.J., Clingen,P.H. and Hartley,J.A. (2000) Defining the roles of nucleotide excision repair and recombination in the repair of DNA interstrand cross-links in mammalian cells. Mol. Cell. Biol., 20, 7980-7990.
46. Bessho,T. (2003) Induction of DNA replication-mediated double strand breaks by psoralen DNA interstrand cross-links. J. Biol. Chem. 278, 5250-5254.
47. O'Brien,T.J., Ceryak,S. and Patierno,S.R. (2003) Complexities of chromium carcinogenesis: role of cellular response, repair and recovery mechanisms. Mutat. Res., 533, 3-36.
48. Das,K.C., Lewis-Molock,Y. and White,C.W. (1995) Activation of NF-kappa B and elevation of MnSOD gene expression by thiol reducing agents in lung adenocarcinoma (A549) cells. Am. J. Physiol., 269 L588-L602.
49. Ogrunc,M. and Sancar,A. (2003) Identification and characterization of human MUS81-MMS4 structure-specific endonuclease. J. Biol. Chem., 278, 21715-21720.
50. Kuzminov,A. (2001) Single-strand interruptions in replicating chromosomes cause double-strand breaks. Proc. Natl Acad. Sci. USA, 98, 8241-8246.
51. Merrill,B.J. and Holm,C. (1999) A requirement for recombinational repair in Saccharomyces cerevisiae is caused by DNA replication defects of mec1 mutants. Genetics, 153, 595-605.
52. Park,E.J., Chan,D.W., Park,J.H., Oettinger,M.A. and Kwon,J. (2003) DNA-PK is activated by nucleosomes and phosphorylates H2AX within the nucleosomes in an acetylation-dependent manner. Nucleic Acids Res. 31, 6819-6827.