Histone H2AX is a critical factor for cellular protection against DNA alkylating agents

Oncogene

Volumn 27, Issue 43, 2008, Pages 5662-5671

  Meador, J A ^a   Zhao, M ^a   Su, Y ^a   Narayan, G ^a   Geard, C R ^a   Balajee, A S ^a  

^a Columbia University Medical Center ^*  (United States)

Author keywords

Alkylation DNA damage; Base excision repair; Chromosomal instability; Histone H2AX; Mitogen activated protein kinase; Poly(ADP) ribose polymerasel

Indexed keywords

ALKYLATING AGENT; HISTONE H2AX; METHYLMETHANE SULFONATE; METHYLNITRONITROSOGUANIDINE; MITOGEN ACTIVATED PROTEIN KINASE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; POLY(ADENOSINE DIPHOSPHATE RIBOSE); UNCLASSIFIED DRUG;

ANAPHASE; ANIMAL CELL; APOPTOSIS; ARTICLE; CELL CYCLE ARREST; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL PROTECTION; CHROMOSOMAL INSTABILITY; CONTROLLED STUDY; DNA DAMAGE; HETEROZYGOSITY; MOUSE; NONHUMAN; NULL ALLELE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN SYNTHESIS; WILD TYPE;

ALKYLATING AGENTS; ANIMALS; APOPTOSIS; CELL DIVISION; CELL LINE; CYTOPROTECTION; DNA DAMAGE; DNA REPAIR; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; G2 PHASE; HISTONES; HUMANS; MAP KINASE SIGNALING SYSTEM; METHYLNITRONITROSOGUANIDINE; MICE; POLY ADENOSINE DIPHOSPHATE RIBOSE; POLY(ADP-RIBOSE) POLYMERASES;

EID: 52949109178     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2008.187     Document Type: Article

References (42)

1. Aebi S, Fink D, Gordon R, Kim HK, Zheng H, Fink JL et al. (1997). Resistance to cytotoxic drugs in DNA mismatch repair-deficient cells. Clin Cancer Res 3: 1763-1767.
2. Balajee AS, Geard CR. (2001). Chromatin-bound PCNA complex formation triggered by DNA damage occurs independent of the ATM gene product in human cells. Nucleic Acids Res 29: 1341-1351.
3. Balajee AS, Geard CR. (2004). Replication protein A and gamma-H2AX foci assembly is triggered by cellular response to DNA double-strand breaks. Exp Cell Res 300: 320-334.
4. Bassing CH, Chua KF, Sekiguchi J, Suh H, Whitlow SR, Fleming JC et al. (2002). Increased ionizing radiation sensitivity and genomic instability in the absence of histone H2AX. Proc Natl Acad Sci USA 99: 8173-8178.
5. Bassing CH, Suh H, Ferguson DO, Chua KF, Manis J, Eckersdorff M et al. (2003). Histone H2AX: a dosage-dependent suppressor of oncogenic translocations and tumors. Cell 114: 359-370.
6. Beardsley DI, Kim WJ, Brown KD. (2005). N-methyl-N′- nitro-N-nitrosoguanidine activates cell-cycle arrest through distinct mechanisms activated in a dose-dependent manner. Mol Pharmacol 68: 1049-1060.
7. Beranek DT. (1990). Distribution of methyl and ethyl adducts following alkylation with monofunctional alkylating agents. Mutat Res 231: 11-30.
8. Bouchard VJ, Rouleau M, Poirier GG. (2003). PARP-1, a determinant of cell survival in response to DNA damage. Exp Hematol 31: 446-454.
9. Celeste A, Difilippantonio S, Difilippantonio MJ, Fernandez-Capetillo O, Pilch DR, Sedelnikova OA et al. (2003a). H2AX haploinsufficiency modifies genomic stability and tumor susceptibility. Cell 114: 371-383.
10. Celeste A, Fernandez-Capetillo O, Kruhlak MJ, Pilch DR, Staudt DW, Lee A et al. (2003b). Histone H2AX phosphorylation is dispensable for the initial recognition of DNA breaks. Nat Cell Biol 5: 675-679.
11. Celeste A, Petersen S, Romanienko PJ, Fernandez-Capetillo O, Chen HT, Sedelnikova OA et al. (2002). Genomic instability in mice lacking histone H2AX. Science 296: 922-927.
12. Chou YH, Ho YS, Wu CC, Chai CY, Chen SC, Lee CH et al. (2007). Tubulozole-induced G2/M cell cycle arrest in human colon cancer cells through formation of microtubule polymerization mediated by ERK1/2 and Chk1 kinase activation. Food Chem Toxicol 45: 1356-1367.
13. Cohen-Armon M, Visochek L, Rozensal D, Kalal A, Geistrikh I, Klein R et al. (2007). DNA-independent PARP-1 activation by phosphorylated ERK2 increases Elk1 activity: a link to histone acetylation. Mol Cell 25: 297-308.
14. d'Adda di Fagagna F, Reaper PM, Clay-Farrace L, Fiegler H, Carr P, Von Zglinicki T et al. (2003). A DNA damage checkpoint response in telomere-initiated senescence. Nature 426: 194-198.
15. Downs JA, Lowndes NF, Jackson SP. (2000). A role for Saccharomyces cerevisiae histone H2A in DNA repair. Nature 408: 1001-1004.
16. Ethier C, Labelle Y, Poirier GG. (2007). PARP-1-induced cell death through inhibition of the MEK/ERK pathway in MNNG-treated HeLa cells. Apoptosis 12: 2037-2049.
17. 2-M checkpoint activation by histone H2AX and 53BP1. Nat Cell Biol 4: 993-997.
18. Fernandez-Capetillo O, Lee A, Nussenzweig M, Nussenzweig A. (2004). H2AX: the histone guardian of the genome. DNA Repair (Amst) 3: 959-967.
19. Furuta T, Takemura H, Liao ZY, Aune GJ, Redon C, Sedelnikova OA 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.
20. Hoeijmakers JH. (2001). Genome maintenance mechanisms for preventing cancer. Nature 411: 366-374.
21. Horton JK, Stefanick DF, Naron JM, Kedar PS, Wilson SH. (2005). Poly(ADP-ribose) polymerase activity prevents signaling pathways for cell cycle arrest after DNA methylating agent exposure. J Biol Chem 280: 15773-15785.
22. Hurley LH. (2002). DNA and its associated processes as targets for cancer therapy. Nat Rev Cancer 2: 188-200.
23. Ichijima Y, Sakasai R, Okita N, Asahina K, Mizutani S, Teraoka H. (2005). Phosphorylation of histone H2AX at M phase in human cells without DNA damage response. Biochem Biophys Res Commun 336: 807-812.
24. Karran P, Offman J, Bignami M. (2003). Human mismatch repair, drug-induced DNA damage, and secondary cancer. Biochimie 85: 1149-1160.
25. Kauppinen TM, Chan WY, Suh SW, Wiggins AK, Huang EJ, Swanson RA. (2006). Direct phosphorylation and regulation of poly(ADP-ribose) polymerase-1 by extracellular signal-regulated kinases 1/2. Proc Natl Acad Sci USA 103: 7136-7141.
26. Lomax ME, Cunniffe S, O'Neill P. (2004). Efficiency of repair of an abasic site within DNA clustered damage sites by mammalian cell nuclear extracts. Biochemistry 43: 11017-11026.
27. McManus KJ, Hendzel MJ. (2005). ATM-dependent DNA damage-independent mitotic phosphorylation of H2AX in normally growing mammalian cells. Mol Biol Cell 16: 5013-5025.
28. Mischo HE, Hemmerich P, Grosse F, Zhang S. (2005). Actinomycin D induces histone gamma-H2AX foci and complex formation of gamma-H2AX with Ku70 and nuclear DNA helicase II. J Biol Chem 280: 9586-9594.
29. Mitra S, Kaina B. (1993). Regulation of repair of alkylation damage in mammalian genomes. Prog Nucleic Acid Res Mol Biol 44: 109-142.
30. Ochs K, Sobol RW, Wilson SH, Kaina B. (1999). Cells deficient in DNA polymerase beta are hypersensitive to alkylating agent-induced apoptosis and chromosomal breakage. Cancer Res 59: 1544-1551.
31. Redon C, Pilch DR, Rogakou EP, Orr AH, Lowndes NF, Bonner WM. (2003). Yeast histone 2A serine 129 is essential for the efficient repair of checkpoint-blind DNA damage. EMBO Rep 4: 678-684.
32. Rogakou EP, Boon C, Redon C, Bonner WM. (1999). Megabase chromatin domains involved in DNA double-strand breaks in vivo. J Cell Biol 146: 905-916.
33. Rogakou EP, Nieves-Neira W, Boon C, Pommier Y, Bonner WM. (2000). Initiation of DNA fragmentation during apoptosis induces phosphorylation of H2AX histone at serine 139. J Biol Chem 275: 9390-9395.
34. Rogakou EP, Pilch DR, Orr AH, Ivanova VS, Bonner WM. (1998). DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem 273: 5858-5868.
35. Soldani C, Scovassi AI. (2002). Poly(ADP-ribose) polymerase-1 cleavage during apoptosis: an update. Apoptosis 7: 321-328.
36. Stiff T, O'Driscoll M, Rief N, Iwabuchi K, Lobrich M, Jeggo PA. (2004). ATM and DNA-PK function redundantly to phosphorylate H2AX after exposure to ionizing radiation. Cancer Res 64: 2390-2396.
37. Takai H, Smogorzewska A, de Lange T. (2003). DNA damage foci at dysfunctional telomeres. Curr Biol 13: 1549-1556.
38. Tibbles LA, Woodgett JR. (1999). The stress-activated protein kinase pathways. Cell Mol Life Sci 55: 1230-1254.
39. Wang H, Wang M, Bocker W, Iliakis G. (2005). Complex H2AX phosphorylation patterns by multiple kinases including ATM and DNA-PK in human cells exposed to ionizing radiation and treated with kinase inhibitors. J Cell Physiol 202: 492-502.
40. Ward IM, Chen J. (2001). Histone H2AX is phosphorylated in an ATR-dependent manner in response to replicational stress. J Biol Chem 276: 47759-47762.
41. Xu B, Kim ST, Lim DS, Kastan MB. (2002). Two molecularly distinct G(2)/M checkpoints are induced by ionizing irradiation. Mol Cell Biol 22: 1049-1059.
42. 2/M checkpoint response requires ERK1/2 activation. Oncogene 26: 4689-4698.