Formation of Dynamic γ-H2AX Domains along Broken DNA Strands Is Distinctly Regulated by ATM and MDC1 and Dependent upon H2AX Densities in Chromatin

Molecular Cell

Volumn 34, Issue 3, 2009, Pages 298-310

  Savic, Velibor ^a,b   Yin, Bu ^a,b   Maas, Nancy L ^a,b   Bredemeyer, Andrea L ^c   Carpenter, Andrea C ^a,b   Helmink, Beth A ^c   Yang Iott, Katherine S ^b   Sleckman, Barry P ^c   Bassing, Craig H ^a,b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

DNA

Indexed keywords

ATM PROTEIN; DOUBLE STRANDED DNA; HISTONE H2AX; MDC1 PROTEIN; PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL CYCLE G1 PHASE; CHROMATIN; CONTROLLED STUDY; DNA STRAND; DNA STRAND BREAKAGE; ENZYME PHOSPHORYLATION; MOUSE; NONHUMAN; PROTEIN DOMAIN;

ANIMALS; B-LYMPHOCYTES; CELL CYCLE PROTEINS; CHROMATIN; DNA; DNA DAMAGE; DNA-BINDING PROTEINS; G1 PHASE; GENES, T-CELL RECEPTOR ALPHA; HISTONES; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MICE, KNOCKOUT; NUCLEAR PROTEINS; PROTEIN-SERINE-THREONINE KINASES; RECOMBINATION, GENETIC; THYMUS GLAND; TUMOR SUPPRESSOR PROTEIN P53; TUMOR SUPPRESSOR PROTEINS;

EID: 65549129613     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2009.04.012     Document Type: Article

References (46)

1. Andegeko Y., Moyal L., Mittelman L., Tsarfaty I., Shiloh Y., and Rotman G. Nuclear retention of ATM at sites of DNA double strand breaks. J. Biol. Chem. 276 (2001) 38224-38230
2. Bassing C.H., and Alt F.W. H2AX may function as an anchor to hold broken chromosomal DNA ends in close proximity. Cell Cycle 3 (2004) 149-153
3. Bassing C.H., Chua K.F., Sekiguchi J., Suh H., Whitlow S.R., Fleming J.C., Monroe B.C., Ciccone D.N., Yan C., Vlasakova K., et al. Increased ionizing radiation sensitivity and genomic instability in the absence of histone H2AX. Proc. Natl. Acad. Sci. USA 99 (2002) 8173-8178
4. Bassing C.H., Swat W., and Alt F.W. The mechanism and regulation of chromosomal V(D)J recombination. Cell 109 Suppl (2002) S45-S55
5. Bassing C.H., Suh H., Ferguson D.O., Chua K.F., Manis J., Eckersdorff M., Gleason M., Bronson R., Lee C., and Alt F.W. Histone H2AX: A dosage-dependent suppressor of oncogenic translocations and tumors. Cell 114 (2003) 359-370
6. Bassing C.H., Ranganath S., Murphy M., Savic V., Gleason M., and Alt F.W. Aberrant V(D)J recombination is not required for rapid development of H2ax/p53 deficient thymic lymphomas with clonal translocations. Blood 111 (2007) 2163-2169
7. Bewersdorf J., Bennett B.T., and Knight K.L. H2AX chromatin structures and their response to DNA damage revealed by 4Pi microscopy. Proc. Natl. Acad. Sci. USA 103 (2006) 18137-18142
8. Bredemeyer A.L., Sharma G.G., Huang C.Y., Helmink B.A., Walker L.M., Khor K.C., Nuskey B., Sullivan K.E., Pandita T.K., Bassing C.H., and Sleckman B.P. ATM stabilizes DNA double-strand-break complexes during V(D)J recombination. Nature 442 (2006) 466-470
9. Bredemeyer A.L., Helmink B.A., Innes C.L., Calderon B., McGinnis L.M., Mahowald G.K., Gapud E.J., Walker L.M., Collins J.B., Weaver B.K., et al. DNA double-strand breaks activate a multi-functional genetic program in developing lymphocytes. Nature 456 (2008) 819-823
10. Burma S., Chen B.P., Murphy M., Kurimasa A., and Chen D.J. ATM phosphorylates histone H2AX in response to DNA double-strand breaks. J. Biol. Chem. 276 (2001) 42462-42467
11. Celeste A., Petersen S., Romanienko P.J., Fernandez-Capetillo O., Chen H.T., Sedelnikova O.A., Reina-San-Martin B., Coppola V., Meffre E., Difilippantonio M.J., et al. Genomic instability in mice lacking histone H2AX. Science 296 (2002) 922-927
12. Celeste A., Difilippantonio S., Difilippantonio M.J., Fernandez-Capetillo O., Pilch D.R., Sedelnikova O.A., Eckhaus M., Ried T., Bonner W.M., and Nussenzweig A. H2AX haploinsufficiency modifies genomic stability and tumor susceptibility. Cell 114 (2003) 371-383
13. 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. Histone H2AX phosphorylation is dispensable for the initial recognition of DNA breaks. Nat. Cell Biol. 5 (2003) 675-679
14. Chen H.T., Bhandoola A., Difilippantonio M.J., Zhu J., Brown M.J., Tai X., Rogakou E.P., Brotz T.M., Bonner W.M., Ried T., and Nussenzweig A. Response to RAG-mediated VDJ cleavage by NBS1 and gamma-H2AX. Science 290 (2000) 1962-1965
15. Chowdhury D., Keogh M.C., Ishii H., Peterson C.L., Buratowski S., and Lieberman J. gamma-H2AX dephosphorylation by protein phosphatase 2A facilitates DNA double-strand break repair. Mol. Cell 20 (2005) 801-809
16. Chowdhury D., Xu X., Zhong X., Ahmed F., Zhong J., Liao J., Dykxhoorn D.M., Weinstock D.M., Pfeifer G.P., and Lieberman J. A PP4-phosphatase complex dephosphorylates gamma-H2AX generated during DNA replication. Mol. Cell 31 (2008) 33-46
17. Downs J.A., Lowndes N.F., and Jackson S.P. A role for Saccharomyces cerevisiae histone H2A in DNA repair. Nature 408 (2000) 1001-1004
18. Fernandez-Capetillo O., Chen H.T., Celeste A., Ward I., Romanienko P.J., Morales J.C., Naka K., Xia Z., Camerini-Otero R.D., Motoyama N., et al. DNA damage-induced G2-M checkpoint activation by histone H2AX and 53BP1. Nat. Cell Biol. 4 (2002) 993-997
19. Franco S., Gostissa M., Zha S., Lombard D.B., Murphy M.M., Zarrin A.A., Yan C., Tepsuporn S., Morales J.C., Adams M.M., et al. H2AX prevents DNA breaks from progressing to chromosome breaks and translocations. Mol. Cell 21 (2006) 201-214
20. Guidos C.J., Williams C.J., Grandal I., Knowles G., Huang M.T., and Danska J.S. V(D)J recombination activates a p53-dependent DNA damage checkpoint in scid lymphocyte precursors. Genes Dev. 10 (1996) 2038-2054
21. Heo K., Kim H., Choi S.H., Choi J., Kim K., Gu J., Lieber M.R., Yang A.S., and An W. FACT-mediated exchange of histone variant H2AX regulated by phosphorylation of H2AX and ADP-ribosylation of Spt16. Mol. Cell 30 (2008) 86-97
22. Hickson I., Zhao Y., Richardson C.J., Green S.J., Martin N.M., Orr A.I., Reaper P.M., Jackson S.P., Curtin N.J., and Smith G.C. Identification and characterization of a novel and specific inhibitor of the ataxia-telangiectasia mutated kinase ATM. Cancer Res. 64 (2004) 9152-9159
23. Hochedlinger K., and Jaenisch R. Monoclonal mice generated by nuclear transfer from mature B and T donor cells. Nature 415 (2002) 1035-1038
24. Huen M.S., Grant R., Manke I., Minn K., Yu X., Yaffe M.B., and Chen J. RNF8 transduces the DNA-damage signal via histone ubiquitylation and checkpoint protein assembly. Cell 131 (2007) 901-914
25. Ikura T., Tashiro S., Kakino A., Shima H., Jacob N., Amunugama R., Yoder K., Izumi S., Kuraoka I., Tanaka K., et al. DNA damage-dependent acetylation and ubiquitination of H2AX enhances chromatin dynamics. Mol. Cell. Biol. 27 (2007) 7028-7040
26. Jonkers J., Meuwissen R., van der Gulden H., Peterse H., van der Valk M., and Berns A. Synergistic tumor suppressor activity of BRCA2 and p53 in a conditional mouse model for breast cancer. Nat. Genet. 29 (2001) 418-425
27. Kimura H., Takizawa N., Allemand E., Hori T., Iborra F.J., Nozaki N., Muraki M., Hagiwara M., Krainer A.R., Fukagawa T., and Okawa K. A novel histone exchange factor, protein phosphatase 2Cgamma, mediates the exchange and dephosphorylation of H2A-H2B. J. Cell Biol. 175 (2006) 389-400
28. Kinner A., Wu W., Staudt C., and Iliakis G. Gamma-H2AX in recognition and signaling of DNA double-strand breaks in the context of chromatin. Nucleic Acids Res. 36 (2008) 5678-5694
29. Kusch T., Florens L., Macdonald W.H., Swanson S.K., Glaser R.L., Yates III J.R., Abmayr S.M., Washburn M.P., and Workman J.L. Acetylation by Tip60 is required for selective histone variant exchange at DNA lesions. Science 306 (2004) 2084-2087
30. Lee P.P., Fitzpatrick D.R., Beard C., Jessup H.K., Lehar S., Makar K.W., Perez-Melgosa M., Sweetser M.T., Schlissel M.S., Nguyen S., et al. A critical role for Dnmt1 and DNA methylation in T cell development, function, and survival. Immunity 15 (2001) 763-774
31. Lou Z., Minter-Dykhouse K., Franco S., Gostissa M., Rivera M.A., Celeste A., Manis J.P., van Deursen J., Nussenzweig A., Paull T.T., et al. MDC1 maintains genomic stability by participating in the amplification of ATM-dependent DNA damage signals. Mol. Cell 21 (2006) 187-200
32. Ma Y., Pannicke U., Schwarz K., and Lieber M.R. Hairpin opening and overhang processing by an Artemis/DNA-dependent protein kinase complex in nonhomologous end joining and V(D)J recombination. Cell 108 (2002) 781-794
33. Mailand N., Bekker-Jensen S., Faustrup H., Melander F., Bartek J., Lukas C., and Lukas J. RNF8 ubiquitylates histones at DNA double-strand breaks and promotes assembly of repair proteins. Cell 131 (2007) 887-900
34. Muljo S.A., and Schlissel M.S. A small molecule Abl kinase inhibitor induces differentiation of Abelson virus-transformed pre-B cell lines. Nat. Immunol. 4 (2003) 31-37
35. Paull T.T., Rogakou E.P., Yamazaki V., Kirchgessner C.U., Gellert M., and Bonner W.M. A critical role for histone H2AX in recruitment of repair factors to nuclear foci after DNA damage. Curr. Biol. 10 (2000) 886-895
36. Ramiro A.R., Jankovic M., Callen E., Difilippantonio S., Chen H.T., McBride K.M., Eisenreich T.R., Chen J., Dickins R.A., Lowe S.W., et al. Role of genomic instability and p53 in AID-induced c-myc-Igh translocations. Nature 440 (2006) 105-109
37. Rogakou E.P., Pilch D.R., Orr A.H., Ivanova V.S., and Bonner W.M. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J. Biol. Chem. 273 (1998) 5858-5868
38. Rogakou E.P., Boon C., Redon C., and Bonner W.M. Megabase chromatin domains involved in DNA double-strand breaks in vivo. J. Cell Biol. 146 (1999) 905-916
39. Rooney S., Sekiguchi J., Zhu C., Cheng H.L., Manis J., Whitlow S., DeVido J., Foy D., Chaudhuri J., Lombard D., and Alt F.W. Leaky Scid phenotype associated with defective V(D)J coding end processing in Artemis-deficient mice. Mol. Cell 10 (2002) 1379-1390
40. Shinkai Y., Rathbun G., Lam K.P., Oltz E.M., Stewart V., Mendelsohn M., Charron J., Datta M., Young F., Stall A.M., et al. RAG-2-deficient mice lack mature lymphocytes owing to inability to initiate V(D)J rearrangement. Cell 68 (1992) 855-867
41. Shroff R., Arbel-Eden A., Pilch D., Ira G., Bonner W.M., Petrini J.H., Haber J.E., and Lichten M. Distribution and dynamics of chromatin modification induced by a defined DNA double-strand break. Curr. Biol. 14 (2004) 1703-1711
42. Stewart G.S., Wang B., Bignell C.R., Taylor A.M., and Elledge S.J. MDC1 is a mediator of the mammalian DNA damage checkpoint. Nature 421 (2003) 961-966
43. Stiff T., O'Driscoll M., Rief N., Iwabuchi K., Lobrich M., and Jeggo P.A. ATM and DNA-PK function redundantly to phosphorylate H2AX after exposure to ionizing radiation. Cancer Res. 64 (2004) 2390-2396
44. Stucki M., and Jackson S.P. gammaH2AX and MDC1: Anchoring the DNA-damage-response machinery to broken chromosomes. DNA Repair (Amst.) 5 (2006) 534-543
45. Unal E., Arbel-Eden A., Sattler U., Shroff R., Lichten M., Haber J.E., and Koshland D. DNA damage response pathway uses histone modification to assemble a double-strand break-specific cohesin domain. Mol. Cell 16 (2004) 991-1002
46. Xie A., Puget N., Shim I., Odate S., Jarzyna I., Bassing C.H., Alt F.W., and Scully R. Control of sister chromatid recombination by histone H2AX. Mol. Cell 16 (2004) 1017-1025