Histone γ-H2AX Involvement in DNA Double-Strand Break Repair Pathways

DNA Damage Recognition

Volumn , Issue , 2005, Pages 723-735

  Balatsos, Nikolaos A A ^a,b   Rogakou, Emmy P ^a  

^a BIOMEDICAL SCIENCES RESEARCH CENTER ALEXANDER FLEMING   (Greece)

^b UNIVERSITY OF THESSALY   (Greece)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 33846313836     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1201/9780849352683-41     Document Type: Chapter

References (60)

1. Strahl BD, Allis CD. The language of covalent histone modifications. Nature 2000; 403:41-45.
2. Redon C, Pilch D, Rogakou E, Sedelnikova O, Newrock K, Bonner W. Histone H2A variants H2AX and H2AZ. Curr Opin Genet Dev 2002; 12:162-169.
3. Luger K, Mader AW, Richmond RK, Sargent DF, Richmond TJ. Crystal structure of the nucleosome core particle at 2.8A resolution. Nature 1997; 389:251-260.
4. Hatch CL, Bonner WM, Moudrianakis EN. Minor histone 2A variants and ubiquinated forms in the native H2A:H2B dimer. Science 1983; 221:468-470.
5. Rogakou EP, Pilch DR, Orr AH, Ivanova VS, Bonner WM. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem 1998; 273: 5858-5868.
6. Redon C, Pilch DR, Rogakou EP, Orr AH, Lowndes NF, Bonner WM. Yeast histone 2A serine 129 is essential for the efficient repair of checkpoint-blind DNA damage. EMBO Rep 2003; 4:678-684.
7. Rogakou EP, Boon C, Redon C, Bonner WM. Megabase chromatin domains involved in DNA double-strand breaks in vivo. J Cell Biol 1999; 146:905-916.
8. Paull TT, Rogakou EP, Yamazaki V, Kirchgessner CU, Gellert M, Bonner WM. A critical role for histone H2AX in recruitment of repair factors to nuclear foci after DNA damage. Curr Biol 2000; 10:886-895.
9. Madigan JP, Chotkowski HL, Glaser RL. DNA double-strand break-induced phosphorylation of Drosophila histone variant H2Av helps prevent radiation-induced apoptosis. Nucleic Acids Res 2002; 30:3698-3705.
10. Tomilin NV, Solovjeva LV, Svetlova MP, Pleskach NM, Zalenskaya IA, Yau PM, Bradbury EM. Visualization of focal nuclear sites of DNA repair synthesis induced by bleomycin in human cells. Radiat Res 2001; 156:347-354.
11. Sedelnikova OA, Rogakou EP, Panyutin IG, Bonner WM. Quantitative detection of (125)IdU-induced DNA double-strand breaks with gamma-H2AX antibody. Radiat Res 2002; 158:486-492.
12. Banath JP, Olive PL. Expression of phosphorylated histone H2AX an a surrogate of cell killing by drugs that create DNA double-strand breaks. Cancer Res 2003; 63:4347-4350.
13. Huang X, Traganos F, Darzynkiewicz Z. DNA Damage Induced by DNA Topoisome-rase I-and Topoisomerase II Inhibitors Detected by Histone H2AX Phosphorylation in Relation to the Cell Cycle Phase and Apoptosis. Cell Cycle 2003; 2:614-619.
14. Furuta T, Takemura H, Liao ZY, Aune GJ, Redon C, Sedelnikova OA, Pilch DR, Rogakou EP, Celeste A, Chen HT, Nussenzweig A, Aladjem MI, Bonner WM, Pommier Y. 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 2003; 278:20303-20312.
15. Xiao H, Li TK, Yang JM, Liu LF. Acidic pH induces topoisomerase II-mediated DNA damage. Proc Natl Acad Sci USA 2003; 100: 5205-5210.
16. Downs JA, Lowndes NF, Jackson SP. A role for Saccharomyces cerevisiae histone H2A in DNA repair. Nature 2000; 408:1001-1004.
17. Takai H, Smogorzewska A, de Lange T. DNA damage foci at dysfunctional telomeres. Curr Biol 2003; 13:1549-1556.
18. d’Adda diFagagna F, Reaper PM, Clay-Farrace L, Fiegler H, Carr P, Von Zglinicki T, Saretzki G, Carter NP, Jackson SP. A DNA damage checkpoint response in telomere-initiated senescence. Nature 2003; 426:194-198.
19. Sedelnikova OA, Horikawa I, Zimonjic DB, Popescu NC, Bonner WM, Barrett JC. Senescing human cells and ageing mice accumulate DNA lesions with unrepairable double-strand breaks. Nat Cell Biol 2004; 6:168-170.
20. Chen HT, Bhandoola A, Difilippantonio MJ, Zhu J, Brown MJ, Tai X, Rogakou EP, Brotz TM, Bonner WM, Ried T, Nussenzweig A. Response to RAG-mediated VDJ cleavage by NBS1 and gamma-H2AX. Science 2000; 290:1962-1965.
21. Petersen S, Casellas R, Reina-San-Martin B, Chen HT, Difilippantonio MJ, Wilson PC, Hanitsch L, Celeste A, Muramatsu M, Pilch DR, Redon C, Ried T, Bonner WM, Honjo T, Nussenzweig MC, Nussenzweig A. AID is required to initiate Nbs1/gamma-H2AX focus formation and mutations at sites of class switching. Nature 2001; 414:660-665.
22. Reina-San-Martin B, Difilippantonio S, Hanitsch L, Masilamani RF, Nussenzweig A, Nussenzweig MC. H2AX is required for recombination between immunoglobulin switch regions but not for intra-switch region recombination or somatic hypermutation. J Exp Med 2003; 197:1767-1778.
23. Mahadevaiah SK, Turner JM, Baudat F, Rogakou EP, de Boer P, Blanco-Rodriguez J, Jasin M, Keeney S, Bonner WM, Burgoyne PS. Recombinational DNA double-strand breaks in mice precede synapsis. Nat Genet 2001; 27:271-276.
24. Rogakou EP, Nieves-Neira W, Boon C, Pommier Y, Bonner WM. Initiation of DNA fragmentation during apoptosis induces phosphorylation of H2AX histone at serine 139. J Biol Chem 2000; 275:9390-9395.
25. Siino JS, Nazarov IB, Svetlova MP, Solovjeva LV, Adamson RH, Zalenskaya IA, Yau PM, Bradbury EM, Tomilin NV. Photobleaching of GFP-labeled H2AX in chromatin: H2AX has low diffusional mobility in the nucleus. Biochem Biophys Res Commun 2002; 297:1318-1323.
26. MacPhail SH, Banath JP, Yu Y, Chu E, Olive PL. Cell cycle-dependent expression of phosphorylated histone H2AX: reduced expression in unirradiated but not X-irradiated G1-phase cells. Radiat Res 2003; 159:759-767.
27. Burma S, Chen BP, Murphy M, Kurimasa A, Chen DJ. ATM phosphorylates histone H2AX in response to DNA double-strand breaks. J Biol Chem 2001; 276: 42462-42467.
28. Fernandez-Capetillo O, Chen HT, Celeste A, Ward I, Romanienko PJ, Morales JC, Naka K, Xia Z, Camerini-Otero RD, Motoyama N, Carpenter PB, Bonner WM, Chen J, Nussenzweig A. DNA damage-induced G2-M checkpoint activation by histone H2AX and 53BP1. Nat Cell Biol 2002; 4:993-997.
29. Fernandez-Capetillo O, Mahadevaiah SK, Celeste A, Romanienko PJ, Camerini-Otero RD, Bonner WM, Manova K, Burgoyne P, Nussenzweig A. H2AX is required for chromatin remodeling and inactivation of sex chromosomes in male mouse meiosis. Dev Cell 2003; 4:497-508.
30. Andegeko Y, Moyal L, Mittelman L, Tsarfaty I, Shiloh Y, Rotman G. Nuclear retention of ATM at sites of DNA double strand breaks. J Biol Chem 2001; 276:38224-38230.
31. Hammond EM, Dorie MJ, Giaccia AJ. ATR/ATM targets are phosphorylated by ATR in response to hypoxia and ATM in response to reoxygenation. J Biol Chem 2003; 278:12207-12213.
32. Ward IM, Chen J. Histone H2AX is phosphorylated in an ATR-dependent manner in response to replicational stress. J Biol Chem 2001; 276:47759-47762.
33. Chan DW, Chen BP, Prithivirajsingh S, Kurimasa A, Story MD, Qin J, Chen DJ. Autophosphorylation of the DNA-dependent protein kinase catalytic subunit is required for rejoining of DNA double-strand breaks. Genes Dev 2002; 16:2333-2338.
34. Kobayashi J, Tauchi H, Sakamoto S, Nakamura A, Morishima K, Matsuura S, Kobayashi T, Tamai K, Tanimoto K, Komatsu K. NBS1 localizes to gamma-H2AX foci through interaction with the FHA/BRCT domain. Curr Biol 2002; 12:1846-1851.
35. Carbone R, Pearson M, Minucci S, Pelicci PG. PML NBs associate with the hMre11 complex and p53 at sites of irradiation induced DNA damage. Oncogene 2002; 21:1633-1640.
36. Limoli CL, Laposa R, Cleaver JE. DNA replication arrest in XP variant cells after UV exposure is diverted into an Mre11-dependent recombination pathway by the kinase inhibitor wortmannin. Mutat Res 2002; 510:121-129.
37. Limoli CL, Giedzinski E, Bonner WM, Cleaver JE. UV-induced replication arrest in the xeroderma pigmentosum variant leads to DNA double-strand breaks, gamma -H2AX formation, and Mre11 relocalization. Proc Natl Acad Sci USA 2002; 99:233-238.
38. Mirzoeva OK, Petrini JH. DNA replication-dependent nuclear dynamics of the Mre11 complex. Mol Cancer Res 2003; 1:207-218.
39. Greer DA, Besley BD, Kennedy KB, Davey S. hRad9 rapidly blinds DNA containing double-strand breaks and is required for damage-dependent topoisomerase II beta binding protein 1 focus formation. Cancer Res 2003; 63:4829-4835.
40. Bassing CH, Chua KF, Sekiguchi J, Suh H, Whitlow SR, Fleming JC, Monroe BC, Ciccone DN, Yan C, Vlasakova K, Livingston DM, Ferguson DO, Scully R, Alt FW. Increased ionizing radiation sensitivity and genomic instability in the absence of histone H2AX. Proc Natl Acad Sci USA 2002; 99:8173-8178.
41. Celeste A, Petersen S, Romanienko PJ, Fernandez-Capetillo O, Chen HT, Sedelnikova OA, Reina-San-Martin B, Coppola V, Meffre E, Difilippantonio MJ, Redon C, Pilch DR, Olaru A, Eckhaus M, Camerini-Otero RD, Tessarollo L, Livak F, Manova K, Bonner WM, Nussenzweig MC, Nussenzweig A. Genomic instability in mice lacking his-tone H2AX. Science 2002; 296:922-927.
42. Celeste A, Fernandez-Capetillo O, Kruhlak MJ, Pilch DR, Staudt DW, Lee A, Bonner RF, Bonner WM, Nussenzweig A. Histone H2AX phosphorylation is dispensable for the initial recognition of DNA breaks. Nat Cell Biol 2003; 5:675-679.
43. Foray N, Marot D, Gabriel A, Randrianarison V, Carr AM, Perricaudet M, Ashworth A, Jeggo P. A subset of ATM-and ATR-dependent phosphorylation events requires the BRCA1 protein. Embo J 2003; 22:2860-2871.
44. Chen A, Kleiman FE, Manley JL, Ouchi T, Pan ZQ. Autoubiquitination of the BRAC1 ‘BARD1 RING ubiquitin ligase. J Biol Chem 2002; 277:22085-22092.
45. Schultz LB, Chehab NH, Malikzay A, Halazonetis TD. p53 binding protein 1 (53BP1) is an early participant in the cellular response to DNA double-strand breaks. J Cell Biol 2000; 151:1381-1390.
46. Ward IM, Minn K, Jorda KG, Chen J. Accumulation of checkpoint protein 53BP1 at DNA breaks involves its binding to phosphorylated histone H2AX. J Biol Chem 2003; 278:19579-19582.
47. Rappold I, Iwabuchi K, Date T, Chen J. Tumor suppressor p53 binding protein 1 (53BP1) is involved in DNA damage-signaling pathways. J Cell Biol 2001; 153:613-620.
48. Goldberg M, Stucki M, Falck J, D’Amours D, Rahman D, Pappin D, Bartek J, Jackson SP. MDC1 is required for the intra-S-phase DNA damage checkpoint. Nature 2003; 421:952-956.
49. Stewart GS, Wang B, Bignell CR, Taylor AM, Elledge SJ. MDC1 is a mediator of the mammalian DNA damage checkpoint. Nature 2003; 421:961-966.
50. Peng A, Chen PL. NFBD1, like 53BP1, is an early and redundant transducer mediating Chk2 phosphorylation in response to DNA damage. J Biol Chem 2003; 278:8873-8876.
51. Xu X, Stern DF. NFBD1/KIAA0170 is a chromatin-associated protein involved in DNA damage signaling pathways. J Biol Chem 2003; 278:8795-8803.
52. Shang YL, Bodero AJ, Chen PL. NFBD1, a novel nuclear protein with signature motifs of FHA and BRCT, and an internal 41-amino acid repeat sequence, is an early participant in DNA damage response. J Biol Chem 2003; 278:6323-6329.
53. Lou Z, Chini CCS, Minter-Dykhouse K, Chen J. Mediator of DNA Damage Checkpoint Protein 1 Regulates BRCA1 Localization and Phosphorylation in DNA Damage Checkpoint Control. J Biol Chem 2003; 278:13599-13602.
54. Bassing CH, Suh H, Ferguson DO, Chua KF, Manis J, Eckersdorff M, Gleason M, Bronson R, Lee C, Alt FW. Histone H2AX: a dosage-dependent suppressor of oncogenic translocations and tumors. Cell 2003; 114:359-370.
55. Celeste A, Difilippantonio S, Difilippantonio MJ, Fernandez-Capetillo O, Pilch DR, Sedel-nikova OA, Eckhaus M, Ried T, Bonner WM, Nussenzweig A. H2AX haploinsufficiency modifies genomic stability and tumor susceptibility. Cell 2003; 114:371-383.
56. Fernandez-Capetillo O, Celeste A, Nussenzweig A. Focusing on Foci: H2AX and the Recruitment of DNA-Damage Response Factors. Cell Cycle 2003; 2:426-427.
57. Aten JA, Stap J, Krawczyk PM, van Oven CH, Hoebe RA, Essers J, Kanaar R. Dynamics of DNA double-strand breaks revealed by clustering of damaged chromosome domains. Science 2004; 303:92-95.
58. Downs JA, Kosmidou E, Morgan A, Jackson SP. Suppression of homologous recombination by the Saccharomyces cerevisiae linker histone. Mol Cell 2003; 11:1685-1692.
59. Bird AW, Yu DY, Pray-Grant MG, Qiu Q, Harmon KE, Megee PC, Grant PA, Smith MM, Christman MF. Acetylation of histone H4 by Esa1 is required for DNA doublestrand break repair. Nature 2002; 419:411-415.
60. Jazayeri A, McAinsh AD, Jackson SP. Saccharomyces cerevisiae Sin3p facilitates DNA double-strand break repair. Proc Natl Acad Sci USA 2004; 101:1644-1649.