H2AX prevents DNA breaks from progressing to chromosome breaks and translocations

Molecular Cell

Volumn 21, Issue 2, 2006, Pages 201-214

  Franco, Sonia ^a   Gostissa, Monica ^a   Zha, Shan ^a   Lombard, David B ^a,b   Murphy, Michael M ^a   Zarrin, Ali A ^a   Yan, Catherine ^a   Tepsuporn, Suprawee ^a   Morales, Julio C ^c   Adams, Melissa M ^c   Lou, Zhenkun ^d   Bassing, Craig H ^e,f   Manis, John P ^a,g   Chen, Junjie ^d   Carpenter, Phillip B ^c   Alt, Frederick W ^a  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^d MAYO CLINIC   (United States)

^e UNIVERSITY OF PENNSYLVANIA   (United States)

^f UNIVERSITY OF PENNSYLVANIA   (United States)

^g HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; CYTIDINE DEAMINASE; DNA; DOUBLE STRANDED DNA; HISTONE H2AX; IMMUNOGLOBULIN HEAVY CHAIN; PROTEIN P53;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; B LYMPHOCYTE; CELL ACTIVATION; CELL STIMULATION; CHROMOSOME BREAKAGE; CHROMOSOME TRANSLOCATION; DNA STRAND BREAKAGE; ENZYME INHIBITION; GENE TRANSLOCATION; LYMPHOMA; METAPHASE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; T LYMPHOCYTE;

ANIMALS; B-LYMPHOCYTES; CHROMOSOME BREAKAGE; CYTIDINE DEAMINASE; DNA DAMAGE; DNA REPAIR; HISTONES; IMMUNOGLOBULIN CLASS SWITCHING; IMMUNOGLOBULIN HEAVY CHAINS; IN SITU HYBRIDIZATION, FLUORESCENCE; MICE; MICE, KNOCKOUT; TRANSLOCATION, GENETIC; TUMOR SUPPRESSOR PROTEIN P53;

ANIMALIA;

EID: 30744445418     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2006.01.005     Document Type: Article

References (57)

1. C.H. Bassing, and F.W. Alt H2AX may function as an anchor to hold broken chromosomal DNA ends in close proximity Cell Cycle 3 2004 149 153
2. C.H. Bassing, K.F. Chua, J. Sekiguchi, H. Suh, S.R. Whitlow, J.C. Fleming, B.C. Monroe, D.N. Ciccone, C. Yan, and K. Vlasakova Increased ionizing radiation sensitivity and genomic instability in the absence of histone H2AX Proc. Natl. Acad. Sci. USA 99 2002 8173 8178
3. C.H. Bassing, H. Suh, D.O. Ferguson, K.F. Chua, J. Manis, M. Eckersdorff, M. Gleason, R. Bronson, C. Lee, and F.W. Alt Histone H2AX: a dosage-dependent suppressor of oncogenic translocations and tumors Cell 114 2003 359 370
4. S. Bekker-Jensen, C. Lukas, F. Melander, J. Bartek, and J. Lukas Dynamic assembly and sustained retention of 53BP1 at the sites of DNA damage are controlled by Mdc1/NFBD1 J. Cell Biol. 170 2005 201 211
5. P.R. Borghesani, F.W. Alt, A. Bottaro, L. Davidson, S. Aksoy, G.A. Rathbun, T.M. Roberts, W. Swat, R.A. Segal, and Y. Gu Abnormal development of Purkinje cells and lymphocytes in Atm mutant mice Proc. Natl. Acad. Sci. USA 97 2000 3336 3341
6. N. Catalan, F. Selz, K. Imai, P. Revy, A. Fischer, and A. Durandy The block in immunoglobulin class switch recombination caused by activation-induced cytidine deaminase deficiency occurs prior to the generation of DNA double strand breaks in switch mu region J. Immunol. 171 2003 2504 2509
7. A. Celeste, S. Petersen, P.J. Romanienko, O. Fernandez-Capetillo, H.T. Chen, O.A. Sedelnikova, B. Reina-San-Martin, V. Coppola, E. Meffre, and M.J. Difilippantonio Genomic instability in mice lacking histone H2AX Science 296 2002 922 927
8. A. Celeste, S. Difilippantonio, M.J. Difilippantonio, O. Fernandez-Capetillo, D.R. Pilch, O.A. Sedelnikova, M. Eckhaus, T. Ried, W.M. Bonner, and A. Nussenzweig H2AX haploinsufficiency modifies genomic stability and tumor susceptibility Cell 114 2003 371 383
9. A. Celeste, O. Fernandez-Capetillo, M.J. Kruhlak, D.R. Pilch, D.W. Staudt, A. Lee, R.F. Bonner, W.M. Bonner, and A. Nussenzweig Histone H2AX phosphorylation is dispensable for the initial recognition of DNA breaks Nat. Cell Biol. 5 2003 675 679
10. J. Chaudhuri, and F.W. Alt Class-switch recombination: interplay of transcription, DNA deamination and DNA repair Nat. Rev. Immunol. 4 2004 541 552
11. H.T. Chen, A. Bhandoola, M.J. Difilippantonio, J. Zhu, M.J. Brown, X. Tai, E.P. Rogakou, T.M. Brotz, W.M. Bonner, T. Ried, and A. Nussenzweig Response to RAG-mediated VDJ cleavage by NBS1 and gamma-H2AX Science 290 2000 1962 1965
12. L.A. Donehower, M. Harvey, B.L. Slagle, M.J. McArthur, C.A. Montgomery Jr., J.S. Butel, and A. Bradley Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumours Nature 356 1992 215 221
13. J.A. Downs, N.F. Lowndes, and S.P. Jackson A role for Saccharomyces cerevisiae histone H2A in DNA repair Nature 408 2000 1001 1004
14. D.D. Dudley, J.P. Manis, A.A. Zarrin, L. Kaylor, M. Tian, and F.W. Alt Internal IgH class switch region deletions are position-independent and enhanced by AID expression Proc. Natl. Acad. Sci. USA 99 2002 9984 9989
15. D.D. Dudley, J. Chaudhuri, C.H. Bassing, and F.W. Alt Mechanism and control of V(D)J recombination versus class switch recombination: similarities and differences Adv. Immunol. 86 2005 43 112
16. W. Dunnick, G.Z. Hertz, L. Scappino, and C. Gritzmacher DNA sequences at immunoglobulin switch region recombination sites Nucleic Acids Res. 21 1993 365 372
17. O. Fernandez-Capetillo, H.T. Chen, A. Celeste, I. Ward, P.J. Romanienko, J.C. Morales, K. Naka, Z. Xia, R.D. Camerini-Otero, and N. Motoyama DNA damage-induced G2-M checkpoint activation by histone H2AX and 53BP1 Nat. Cell Biol. 4 2002 993 997
18. O. Fernandez-Capetillo, S.K. Mahadevaiah, A. Celeste, P.J. Romanienko, R.D. Camerini-Otero, W.M. Bonner, K. Manova, P. Burgoyne, and A. Nussenzweig H2AX is required for chromatin remodeling and inactivation of sex chromosomes in male mouse meiosis Dev. Cell 4 2003 497 508
19. O. Fernandez-Capetillo, A. Lee, M. Nussenzweig, and A. Nussenzweig H2AX: the histone guardian of the genome DNA Repair (Amst.) 3 2004 959 967
20. M. Gellert V(D)J recombination: RAG proteins, repair factors, and regulation Annu. Rev. Biochem. 71 2002 101 132
21. M.T. Hemann, A. Bric, J. Teruya-Feldstein, A. Herbst, J.A. Nilsson, C. Cordon-Cardo, J.L. Cleveland, W.P. Tansey, and S.W. Lowe Evasion of the p53 tumour surveillance network by tumour-derived MYC mutants Nature 436 2005 807 811
22. T. Honjo, M. Muramatsu, and S. Fagarasan AID: how does it aid antibody diversity? Immunity 20 2004 659 668
23. Y. Huyen, O. Zgheib, R.A. Ditullio Jr., V.G. Gorgoulis, P. Zacharatos, T.J. Petty, E.A. Sheston, H.S. Mellert, E.S. Stavridi, and T.D. Halazonetis Methylated lysine 79 of histone H3 targets 53BP1 to DNA double-strand breaks Nature 432 2004 406 411
24. G. Iliakis, Y. Wang, J. Guan, and H. Wang DNA damage checkpoint control in cells exposed to ionizing radiation Oncogene 22 2003 5834 5847
25. J. Kobayashi, H. Tauchi, S. Sakamoto, A. Nakamura, K. Morishima, S. Matsuura, T. Kobayashi, K. Tamai, K. Tanimoto, and K. Komatsu NBS1 localizes to gamma-H2AX foci through interaction with the FHA/BRCT domain Curr. Biol. 12 2002 1846 1851
26. S. Kracker, Y. Bergmann, I. Demuth, P.O. Frappart, G. Hildebrand, R. Christine, Z.Q. Wang, K. Sperling, M. Digweed, and A. Radbruch Nibrin functions in Ig class-switch recombination Proc. Natl. Acad. Sci. USA 102 2005 1584 1589
27. R. Kuppers, and R. Dalla-Favera Mechanisms of chromosomal translocations in B cell lymphomas Oncogene 20 2001 5580 5594
28. Z. Lou, K. Minter-Dykhouse, S. Franco, M. Gostissa, M.A. Rivera, A. Celeste, J. Manis, J. van Deursen, A. Nussenzweig, and T.T. Paull MDC1 maintains genomic stability by participating in the amplification of ATM-dependent DNA damage signals Mol. Cell 21 2006 187 200 this issue
29. J.M. Lumsden, T. McCarty, L.K. Petiniot, R. Shen, C. Barlow, T.A. Wynn, H.C. Morse III, P.J. Gearhart, A. Wynshaw-Boris, E.E. Max, and R.J. Hodes Immunoglobulin class switch recombination is impaired in Atm-deficient mice J. Exp. Med. 200 2004 1111 1121
30. J.P. Manis, J.C. Morales, Z. Xia, J.L. Kutok, F.W. Alt, and P.B. Carpenter 53BP1 links DNA damage-response pathways to immunoglobulin heavy chain class-switch recombination Nat. Immunol. 5 2004 481 487
31. K.D. Mills, D.O. Ferguson, and F.W. Alt The role of DNA breaks in genomic instability and tumorigenesis Immunol. Rev. 194 2003 77 95
32. J.C. Morales, Z. Xia, T. Lu, M.B. Aldrich, B. Wang, C. Rosales, R.E. Kellems, W.N. Hittelman, S.J. Elledge, and P.B. Carpenter Role for the BRCA1 C-terminal repeats (BRCT) protein 53BP1 in maintaining genomic stability J. Biol. Chem. 278 2003 14971 14977
33. J.C. Morales, S. Franco, M.M. Murphy, C.H. Bassing, K.D. Mills, M.M. Adams, J.P. Manis, G.Z. Rassidakis, F.W. Alt, and P.B. Carpenter 53BP1 and p53 synergize to suppress genomic instability and lymphomagenesis Proc. Natl. Acad. Sci. USA 2006 in press
34. M. Muramatsu, K. Kinoshita, S. Fagarasan, S. Yamada, Y. Shinkai, and T. Honjo Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme Cell 102 2000 553 563
35. Q. Pan-Hammarstrom, A.M. Jones, A. Lahdesmaki, W. Zhou, R.A. Gatti, L. Hammarstrom, A.R. Gennery, and M.R. Ehrenstein Impact of DNA ligase IV on nonhomologous end joining pathways during class switch recombination in human cells J. Exp. Med. 201 2005 189 194
36. S. Petersen, R. Casellas, B. Reina-San-Martin, H.T. Chen, M.J. Difilippantonio, P.C. Wilson, L. Hanitsch, A. Celeste, M. Muramatsu, and D.R. Pilch AID is required to initiate Nbs1/gamma-H2AX focus formation and mutations at sites of class switching Nature 414 2001 660 665
37. A.R. Ramiro, M. Jankovic, T. Eisenreich, S. Difilippantonio, S. Chen-Kiang, M. Muramatsu, T. Honjo, A. Nussenzweig, and M.C. Nussenzweig AID is required for c-myc/IgH chromosome translocations in vivo Cell 118 2004 431 438
38. B. Reina-San-Martin, S. Difilippantonio, L. Hanitsch, R.F. Masilamani, A. Nussenzweig, and M.C. Nussenzweig H2AX is required for recombination between immunoglobulin switch regions but not for intra-switch region recombination or somatic hypermutation J. Exp. Med. 197 2003 1767 1778
39. B. Reina-San-Martin, H.T. Chen, A. Nussenzweig, and M.C. Nussenzweig ATM is required for efficient recombination between immunoglobulin switch regions J. Exp. Med. 200 2004 1103 1110
40. B. Reina-San-Martin, M.C. Nussenzweig, A. Nussenzweig, and S. Difilippantonio Genomic instability, endoreduplication, and diminished Ig class-switch recombination in B cells lacking Nbs1 Proc. Natl. Acad. Sci. USA 102 2005 1590 1595
41. R. Riblet Immunoglobulin heavy chain genes of mouse T.A. Honjo F.W. Alt M. Neuberger Molecular Biology of B Cells 2004 Elsevier Academic Press London 19 26
42. E.P. Rogakou, C. Boon, C. Redon, and W.M. Bonner Megabase chromatin domains involved in DNA double-strand breaks in vivo J. Cell Biol. 146 1999 905 916
43. E.P. Rogakou, D.R. Pilch, A.H. Orr, V.S. Ivanova, and W.M. Bonner DNA double-stranded breaks induce histone H2AX phosphorylation of serine 139 J. Biol. Chem. 273 2000 5858 5868
44. J.S. Rush, S.D. Fugmann, and D.G. Schatz Staggered AID-dependent DNA double strand breaks are the predominant DNA lesions targeted to S mu in Ig class switch recombination Int. Immunol. 16 2004 549 557
45. J.S. Rush, M. Liu, V.H. Odegard, S. Unniraman, and D.G. Schatz Expression of activation-induced cytidine deaminase is regulated by cell division, providing a mechanistic basis for division-linked class switch recombination Proc. Natl. Acad. Sci. USA 102 2005 13242 13247
46. C.E. Schrader, E.K. Linehan, S.N. Mochegova, R.T. Woodland, and J. Stavnezer Inducible DNA breaks in Ig S regions are dependent on AID and UNG J. Exp. Med. 202 2005 561 568
47. J. Sekiguchi, D.O. Ferguson, H.T. Chen, E.M. Yang, J. Earle, K. Frank, S. Whitlow, Y. Gu, Y. Xu, A. Nussenzweig, and F.W. Alt Genetic interactions between ATM and the nonhomologous end-joining factors in genomic stability and development Proc. Natl. Acad. Sci. USA 98 2001 3243 3248
48. G.S. Stewart, B. Wang, C.R. Bignell, A.M. Taylor, and S.J. Elledge MDC1 is a mediator of the mammalian DNA damage checkpoint Nature 421 2003 961 966
49. M. Stucki, J.A. Clapperton, D. Mohammad, M.B. Yaffe, S.J. Smerdon, and S.P. Jackson MDC1 directly binds phosphorylated histone H2AX to regulate cellular responses to DNA double-strand breaks Cell 123 2005 1213 1226
50. S. Unniraman, S. Zhou, and D.G. Schatz Identification of an AID-independent pathway for chromosomal translocations between the Igh switch region and Myc Nat. Immunol. 5 2004 1117 1123
51. H. van Attikum, and S.M. Gasser The histone code at DNA breaks: a guide to repair? Nat. Rev. Mol. Cell Biol. 6 2005 757 765
52. B. Vogelstein, D. Lane, and A.J. Levine Surfing the p53 network Nature 408 2000 307 310
53. I.M. Ward, K. Minn, K.G. Jorda, and J. Chen Accumulation of checkpoint protein 53BP1 at DNA breaks involves its binding to phosphorylated histone H2AX J. Biol. Chem. 278 2003 19579 19582
54. I.M. Ward, K. Minn, J. van Deursen, and J. Chen p53 binding protein 53BP1 is required for DNA damage responses and tumor suppression in mice Mol. Cell. Biol. 23 2003 2556 2563
55. I.M. Ward, B. Reina-San-Martin, A. Olaru, K. Minn, K. Tamada, J.S. Lau, M. Cascalho, L. Chen, A. Nussenzweig, and F. Livak 53BP1 is required for class switch recombination J. Cell Biol. 165 2004 459 464
56. R.A. Wuerffel, J. Du, R.J. Thompson, and A.L. Kenter Ig Sgamma3 DNA-specifc double strand breaks are induced in mitogen-activated B cells and are implicated in switch recombination J. Immunol. 159 1997 4139 4144
57. A. Xie, N. Puget, I. Shim, S. Odate, I. Jarzyna, C.H. Bassing, F.W. Alt, and R. Scully Control of sister chromatid recombination by histone H2AX Mol. Cell 16 2004 1017 1025