Chromatin remodeling finds its place in the DNA double-strand break response

Nucleic Acids Research

Volumn 37, Issue 5, 2009, Pages 1363-1377

  Pandita, Tej K ^a   Richardson, Christine ^b  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH CAROLINA AT CHARLOTTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; ATR PROTEIN; CHECKPOINT KINASE RAD3; HISTONE ACETYLTRANSFERASE; HISTONE H1; HISTONE H2A; HISTONE H2AX; HISTONE H3; HISTONE H4; MRE11 PROTEIN;

ACETYLATION; ARTICLE; CELL CYCLE; CELL DEATH; CELL VIABILITY; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMOSOME BREAKAGE; DNA DAMAGE; DNA METHYLATION; DNA REPAIR; DOUBLE STRANDED DNA BREAK; DOWNSTREAM PROCESSING; EFFECTOR CELL; ENZYME ACTIVITY; EUKARYOTIC CELL; GENOMIC INSTABILITY; HUMAN; IONIZING RADIATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; UBIQUITINATION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; GENETIC DISEASES, INBORN; HUMANS; METHYLATION; PROTEIN KINASES; SIGNAL TRANSDUCTION; UBIQUITINATION;

EUKARYOTA;

EID: 63249124451     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkn1071     Document Type: Article

References (169)

1. Pandita, T.K. and Hittelman, W.N. (1992) Initial chromosome damage but not DNA damage is greater in ataxia telangiectasia cells. Radiat. Res., 130, 94-103.
2. Pandita, T.K. and Hittelman, W.N. (1992) The contribution of DNA and chromosome repair deficiencies to the radiosensitivity of ataxia-telangiectasia. Radiat. Res., 131, 214-223.
3. Richardson,C., Horikoshi,N. and Pandita,T.K. (2004) The role of the DNA double-strand break response network in meiosis. DNA Repair, 3 1149-1164.
4. 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. et al. (2006) ATM stabilizes DNA double-strand-break complexes during V(D)J recombination. Nature, 442, 466-470.
5. Huang,C.Y., Sharma,G.G., Walker,L.M., Bassing,C.H., Pandita,T.K. and Sleckman,B.P. (2007) Defects in coding joint formation in vivo in developing ATM-deficient B and T lymphocytes. J. Exp. Med., 204 1371-1381.
6. Pandita,T.K. (2002) ATM function and telomere stability. Oncogene, 21, 611-618.
7. Pandita,T.K. (2002) Telomeres and Telomerase. Encyclopedia of Cancer 4:355-362
8. Sonoda,E., Hochegger,H., Saberi,A., Taniguchi,Y. and Takeda,S. (2006) Differential usage of non-homologous end-joining and homologous recombination in double strand break repair. DNA Repair, 5, 1021-1029.
9. Rothkamm,K., Kruger,I., Thompson,L.H. and Lobrich,M. (2003) Pathways of DNA double-strand break repair during the mammalian cell cycle. Mol. Cell. Biol., 23, 5706-5715.
10. Cartwright,R., Tambini,C.E., Simpson,P.J. and Thacker,J. (1998) The XRCC2 DNA repair gene from human and mouse encodes a novel member of the recA/RAD51 family. Nucleic Acids Res., 26, 3084-3089.
11. Haber,J.E. (2000) Partners and pathwaysrepairing a double-strand break. Trends Genet., 16, 259-264.
12. Jeggo,P.A. (1998) DNA breakage and repair. Adv. Genet., 38, 185-218.
13. Scott,S.P. and Pandita,T.K. (2006) The cellular control of DNA double-strand breaks. J. Cell Biochem., 99, 1463-1475.
14. Grenon,M., Gilbert,C. and Lowndes,N.F. (2001) Checkpoint activation in response to double-strand breaks requires the Mre11/Rad50/Xrs2 complex. Nat. Cell Biol., 3, 844-847.
15. Shen,Z., Denison,K., Lobb,R., Gatewood,J.M. and Chen,D.J. (1995) The human and mouse homologs of the yeast RAD52 gene: CDNA cloning, sequence analysis, assignment to human chromosome 12p12.2-p13, and mRNA expression in mouse tissues. Genomics, 25, 199-206.
16. Kanaar,R., Hoeijmakers,J.H. and van Gent,D.C. (1998) Molecular mechanisms of DNA double strand break repair. Trends Cell Biol., 8, 483-489.
17. Kagawa,W., Kurumizaka,H., Ishitani,R., Fukai,S., Nureki,O., Shibata,T. and Yokoyama,S. (2002) Crystal structure of the homologous-pairing domain from the human Rad52 recombinase in the undecameric form. Mol. Cell, 10, 359-371.
18. Downs,J.A., Nussenzweig,M.C. and Nussenzweig,A. (2007) Chromatin dynamics and the preservation of genetic information. Nature, 447, 951-958.
19. Mailand,N., Bekker-Jensen,S., Faustrup,H., Melander,F., Bartek,J., Lukas,C. and Lukas,J. (2007) RNF8 ubiquitylates histones at DNA double-strand breaks and promotes assembly of repair proteins. Cell 131, 887-900.
20. Lee,J.H. and Paull,T.T. (2004) Direct activation of the ATM protein kinase by the Mre11/Rad50/Nbs1 complex. Science, 304, 93-96.
21. Lee,J.H. and Paull,T.T. (2005) ATM activation by DNA double-strand breaks through the Mre11-Rad50-Nbs1 complex. Science, 308, 551-554.
22. Lavin,M.F. (2008) Ataxia-telangiectasia: From a rare disorder to a paradigm for cell signalling and cancer. Nat. Rev. Mol. Cell. Biol. 9, 759-769.
23. 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.
24. Bekker-Jensen,S., Lukas,C., Kitagawa,R., Melander,F., Kastan,M.B., Bartek,J. and Lukas,J. (2006) Spatial organization of the mammalian genome surveillance machinery in response to DNA strand breaks. J. Cell Biol., 173, 195-206.
25. Rattray,A.J., McGill,C.B., Shafer,B.K. and Strathern,J.N. (2001) Fidelity of mitotic double-strand-break repair in Saccharomyces cerevisiae: A role for SAE2/COM1. Genetics, 158, 109-122.
26. Nairz,K. and Klein,F. (1997) mre11S-a yeast mutation that blocks double-strand-break processing and permits nonhomologous synapsis in meiosis. Genes Dev., 11, 2272-2290.
27. Moreau,S., Ferguson,J.R. and Symington,L.S. (1999) The nuclease activity of Mre11 is required for meiosis but not for mating type switching, end joining, or telomere maintenance. Mol. Cell. Biol., 19, 556-566.
28. Usui,T., Ohta,T., Oshiumi,H., Tomizawa,J., Ogawa,H. and Ogawa,T. (1998) Complex formation and functional versatility of Mre11 of budding yeast in recombination. Cell, 95, 705-716.
29. Sartori,A.A., Lukas,C., Coates,J., Mistrik,M., Fu,S., Bartek,J., Baer,R., Lukas,J. and Jackson,S.P. (2007) Human CtIP promotes DNA end resection. Nature, 450, 509-514.
30. Moreau,S., Morgan,E.A. and Symington,L.S. (2001) Overlapping functions of the Saccharomyces cerevisiae Mre11, Exo1 and Rad27 nucleases in DNA metabolism. Genetics, 159, 1423-1433.
31. Limbo,O., Chahwan,C., Yamada,Y., de Bruin,R.A., Wittenberg,C. and Russell,P. (2007) Ctp1 is a cell-cycle-regulated protein that functions with Mre11 complex to control double-strand break repair by homologous recombination. Mol. Cell, 28, 134-146.
32. Chen,L., Nievera,C.J., Lee,A.Y. and Wu,X. (2008) Cell cycle-dependent complex formation of BRCA1.CtIP.MRN is important for DNA double-strand break repair. J. Biol. Chem., 283, 7713-7720.
33. de Jager,M., van Noort,J., van Gent,D.C., Dekker,C., Kanaar,R. and Wyman,C. (2001) Human Rad50/Mre11 is a flexible complex that can tether DNA ends. Mol. Cell, 8, 1129-1135.
34. Hopfner,K.P., Karcher,A., Craig,L., Woo,T.T., Carney,J.P. and Tainer,J.A. (2001) Structural biochemistry and interaction architecture of the DNA double-strand break repair Mre11 nuclease and Rad50-ATPase. Cell, 105, 473-485.
35. Hopfner,K.P., Craig,L., Moncalian,G., Zinkel,R.A., Usui,T., Owen,B.A., Karcher,A., Henderson,B., Bodmer,J.L., McMurray,C.T. et al. (2002) The Rad50 zinc-hook is a structure joining Mre11 complexes in DNA recombination and repair. Nature, 418, 562-566.
36. Wyman,C. and Kanaar,R. (2002) Chromosome organization: Reaching out to embrace new models. Curr. Biol., 12, R446-448.
37. Soutoglou,E., Dorn,J.F., Sengupta,K., Jasin,M., Nussenzweig,A., Ried,T., Danuser,G. and Misteli,T. (2007) Positional stability of single double-strand breaks in mammalian cells. Nat. Cell Biol., 9, 675-682.
38. Lisby,M., Mortensen,U.H. and Rothstein,R. (2003) Colocalization of multiple DNA double-strand breaks at a single Rad52 repair centre. Nat. Cell Biol., 5, 572-577.
39. Richardson,C. and Jasin,M. (2000) Frequent chromosomal translocations induced by DNA double-strand breaks. Nature, 405, 697-700.
40. Richardson,C. and Jasin,M. (2000) Coupled homologous and nonhomologous repair of a double-strand break preserves genomic integrity in mammalian cells. Mol. Cell. Biol., 20, 9068-9075.
41. Crampton,D.J., Mukherjee,S. and Richardson,C.C. (2006) DNA-induced switch from independent to sequential dTTP hydrolysis in the bacteriophage T7 DNA helicase. Mol. Cell, 21, 165-174.
42. Williams,B.R., Mirzoeva,O.K., Morgan,W.F., Lin,J., Dunnick,W. and Petrini,J.H. (2002) A murine model of Nijmegen breakage syndrome. Curr. Biol., 12, 648-653.
43. Bender,C.F., Sikes,M.L., Sullivan,R., Huye,L.E., Le Beau,M.M., Roth,D.B., Mirzoeva,O.K., Oltz,E.M. and Petrini,J.H. (2002) Cancer predisposition and hematopoietic failure in Rad50(S/S) mice. Genes Dev., 16, 2237-2251.
44. Pandita,T.K., Westphal,C.H., Anger,M., Sawant,S.G., Geard,C.R., Pandita,R.K. and Scherthan,H. (1999) Atm inactivation results in aberrant telomere clustering during meiotic prophase. Mol. Cell. Biol., 19, 5096-5105.
45. Scherthan,H., Jerratsch,M., Dhar,S., Wang,Y.A., Goff,S.P. and Pandita,T.K. (2000) Meiotic telomere distribution and Sertoli cell nuclear architecture are altered in Atm- and Atm-p53-deficient mice. Mol. Cell. Biol., 20, 7773-7783.
46. Gupta,A., Sharma,G.G., Young,C.S.H., Agarwal,M., Smith,E.R., Paull,T.T., Lucchesi,J.C., Khanna,K.K., Ludwig,T. and Pandita,T.K. (2005) Involvement of human MOF in ATM function. Mol. Cell. Biol., 25 5292-5305.
47. Kusch,T., Florens,L., Macdonald,W.H., Swanson,S.K., Glaser,R.L., Yates,J.R. 3rd, Abmayr,S.M., Washburn,M.P. and Workman,J.L. (2004) Acetylation by Tip60 is required for selective histone variant exchange at DNA lesions. Science, 306, 2084-2087.
48. Pandita,T.K. (2003) A multifaceted role of ATM in genome maintenance. Expert Rev. Mol. Med., 5, 1-21.
49. Sharma,G.G., Hwang,K.K., Pandita,R.K., Gupta,A., Dhar,S., Parenteau,J., Agarwal,M., Worman,H.J., Wellinger,R.J. and Pandita,T.K. (2003) Human heterochromatin protein 1 isoforms HP1(Hsalpha) and HP1(Hsbeta) interfere with hTERT-telomere interactions and correlate with changes in cell growth and response to ionizing radiation. Mol. Cell. Biol., 23, 8363-8376.
50. Peterson,C.L. and Cote,J. (2004) Cellular machineries for chromosomal DNA repair. Genes Dev., 18, 602-616.
51. Thiriet,C. and Hayes,J.J. (2005) Chromatin in need of a fix: phosphorylation of H2AX connects chromatin to DNA repair. Mol. Cell 18, 617-622.
52. van Attikum,H. and Gasser,S.M. (2005) The histone code at DNA breaks: A guide to repair? Nat. Rev. Mol. Cell. Biol., 6, 757-765.
53. Vaquero,A., Loyola,A. and Reinberg,D. (2003) The constantly changing face of chromatin. Sci. Aging Knowledge Environ., 2003, RE4.
54. Shogren-Knaak,M., Ishii,H., Sun,J.M., Pazin,M.J., Davie,J.R. and Peterson,C.L. (2006) Histone H4-K16 acetylation controls chromatin structure and protein interactions. Science, 311, 844-847.
55. Sharma,G.G., Gupta,A., Wang,H., Scherthan,H., Dhar,S., Gandhi,V., Iliakis,G., Shay,J.W., Young,C.S. and Pandita,T.K. (2003) hTERT associates with human telomeres and enhances genomic stability and DNA repair. Oncogene, 22, 131-146.
56. Sharma,G.G., Hall,E.J., Dhar,S., Gupta,A., Rao,P.H. and Pandita,T.K. (2003) Telomere stability correlates with longevity of human beings exposed to ionizing radiations. Oncol. Rep., 10, 1733-1736.
57. Redon,C., Pilch,D., Rogakou,E., Sedelnikova,O., Newrock,K. and Bonner,W. (2002) Histone H2A variants H2AX and H2AZ. Curr. Opin. Genet. Dev. 12, 162-169.
58. 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.
59. Mahadevaiah,S.K., Turner,J.M., Baudat,F., Rogakou,E.P., de Boer,P., Blanco-Rodriguez,J., Jasin,M., Keeney,S., Bonner,W.M. and Burgoyne,P.S. (2001) Recombinational DNA double-strand breaks in mice precede synapsis. Nat. Genet., 27, 271-276.
60. Hunter,N., Boerner,V., Lichten,M. and Kleckner,N. (2001) Recombinational DNA double strand breaks in mice precede synapsis. Nat. Genet., 27, 236-238.
61. 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. et al. (2000) Response to RAG-mediated VDJ cleavage by NBS1 and gamma-H2AX. Science, 290, 1962-1965.
62. Petersen,S., Casellas,R., Reina-San-Martin,B., Chen,H.T., Difilippantonio,M.J., Wilson,P.C., Hanitsch,L., Celeste,A., Muramatsu,M., Pilch,D.R. et al. (2001) AID is required to initiate Nbs1/gamma-H2AX focus formation and mutations at sites of class switching. Nature, 414, 660-665.
63. 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. (2002) Increased ionizing radiation sensitivity and genomic instability in the absence of histone H2AX. Proc. Natl Acad. Sci. USA 99, 8173-8178.
64. 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. (2002) Genomic instability in mice lacking histone H2AX. Science, 296, 922-927.
65. Fernandez-Capetillo,O., Mahadevaiah,S.K., Celeste,A., Romanienko,P.J., Camerini-Otero,R.D., Bonner,W.M., Manova,K., Burgoyne,P. and Nussenzweig,A. (2003) H2AX is required for chromatin remodeling and inactivation of sex chromosomes in male mouse meiosis. Dev. Cell, 4, 497-508.
66. Reina-San-Martin,B., Difilippantonio,S., Hanitsch,L., Masilamani,R.F., Nussenzweig,A. and Nussenzweig,M.C. (2003) H2AX is required for recombination between immunoglobulin switch regions but not for intra-switch region recombination or somatic hypermutation. J. Exp. Med., 197, 1767-1778.
67. 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. Nat. Cell Biol., 5, 675-679.
68. Altaf,M., Saksouk,N. and Cote,J. (2007) Histone modifications in response to DNA damage. Mutat. Res., 618, 81-90.
69. Cheung,W.L., Turner,F.B., Krishnamoorthy,T., Wolner,B., Ahn,S.H., Foley,M., Dorsey,J.A., Peterson,C.L., Berger,S.L. and Allis,C.D. (2005) Phosphorylation of histone H4 serine 1 during DNA damage requires casein kinase II in S. cerevisiae. Curr. Biol., 15, 656-660.
70. Utley,R.T., Lacoste,N., Jobin-Robitaille,O., Allard,S. and Cote,J. (2005) Regulation of NuA4 histone acetyltransferase activity in transcription and DNA repair by phosphorylation of histone H4. Mol. Cell. Biol., 25, 8179-8190.
71. Goodarzi,A.A., Noon,A.T., Deckbar,D., Ziv,Y., Shiloh,Y., Lobrich,M. and Jeggo,P.A. (2008) ATM signaling facilitates repair of DNA double-strand breaks associated with heterochromatin. Mol. Cell, 31, 167-177.
72. Morgan,S.E., Lovly,C., Pandita,T.K., Shiloh,Y. and Kastan,M.B. (1997) Fragments of ATM which have dominant-negative or complementing activity. Mol. Cell. Biol., 17, 2020-2029.
73. Bakkenist,C.J. and Kastan,M.B. (2003) DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature, 421, 499-506.
74. Ziv,Y., Bielopolski,D., Galanty,Y., Lukas,C., Taya,Y., Schultz,D.C., Lukas,J., Bekker-Jensen,S., Bartek,J. and Shiloh,Y. (2006) Chromatin relaxation in response to DNA double-strand break is modulated by a novel ATM- and KAP-1 dependent pathway. Nat. Cell Biol., 8, 870-876.
75. Lechner,M.S., Levitan,I. and Dressler,G.R. (2000) PTIP, a novel BRCT domain-containing protein interacts with Pax2 and is associated with active chromatin. Nucleic Acids Res., 28, 2741-2751.
76. Schultz,D.C., Ayyanathan,K., Negorev,D., Maul,G.G. and Rauscher,F.J. 3rd (2002) SETDB1: A novel KAP-1-associated histone H3, lysine 9-specific methyltransferase that contributes to HP1-mediated silencing of euchromatic genes by KRAB zinc-finger proteins. Genes Dev., 16 919-932.
77. Ayoub,N., Jeyasekharan,A.D., Bernal,J.A. and Venkitaraman,A.R. (2008) HP1-beta mobilization promotes chromatin changes that initiate the DNA damage response. Nature, 453, 682-686.
78. Aucott,R., Bullwinkel,J., Yu,Y., Shi,W., Billur,M., Brown,J.P., Menzel,U., Kioussis,D., Wang,G., Reisert,I. et al. (2008) HP1β is required for development of the cerebral neocortex and diaphragmatic neuromuscular junctions. J. Cell Biol., 183, 597-606.
79. Gupta,A., Sharma,G.G., Young,C.S., Agarwal,M., Smith,E.R., Paull,T.T., Lucchesi,J.C., Khanna,K.K., Ludwig,T. and Pandita,T.K. (2005) Involvement of human MOF in ATM function. Mol. Cell. Biol., 25 5292-5305.
80. Gupta,A., Guerin-Peyrou,T.G., Sharma,G.G., Park,C., Agarwal,M., Ganju,R.K., Pandita,S., Choi,K., Sukumar,S., Pandita,R.K. et al. (2008) The mammalian ortholog of Drosophila MOF that acetylates histone H4 lysine 16 is essential for embryogenesis and oncogenesis. Mol. Cell. Biol., 28, 397-409.
81. Yamamoto,T. and Horikoshi,M. (1997) Novel substrate specificity of the histone acetyltransferase activity of HIV-1-Tat interactive protein Tip60. J. Biol. Chem., 272, 30595-30598.
82. Kimura,A. and Horikoshi,M. (1998) Tip60 acetylates six lysines of a specific class in core histones in vitro. Genes Cells, 3, 789-800.
83. Ikura,T., Ogryzko,V.V., Grigoriev,M., Groisman,R., Wang,J., Horikoshi,M., Scully,R., Qin,J. and Nakatani,Y. (2000) Involvement of the TIP60 histone acetylase complex in DNA repair and apoptosis. Cell 102, 463-473.
84. Murr,R., Loizou,J.I., Yang,Y.G., Cuenin,C., Li,H., Wang,Z.Q. and Herceg,Z. (2006) Histone acetylation by Trrap-Tip60 modulates loading of repair proteins and repair of DNA double-strand breaks. Nat. Cell Biol., 8, 91-99.
85. Downs,J.A., Allard,S., Jobin-Robitaille,O., Javaheri,A., Auger,A., Bouchard,N., Kron,S.J., Jackson,S.P. and Cote,J. (2004) Binding of chromatin-modifying activities to phosphorylated histone H2A at DNA damage sites. Mol. Cell, 16, 979-990.
86. Sun,Y., Jiang,X., Chen,S., Fernandes,N. and Price,B.D. (2005) A role for the Tip60 histone acetyltransferase in the acetylation and activation of ATM. Proc. Natl Acad. Sci. USA, 102, 13182-13187.
87. Morrison,A.J., Highland,J., Krogan,N.J., Arbel-Eden,A., Greenblatt,J.F., Haber,J.E. and Shen,X. (2004) INO80 and gamma-H2AX interaction links ATP-dependent chromatin remodeling to DNA damage repair. Cell, 119, 767-775.
88. van Attikum,H., Fritsch,O., Hohn,B. and Gasser,S.M. (2004) Recruitment of the INO80 complex by H2A phosphorylation links ATP-dependent chromatin remodeling with DNA double-strand break repair. Cell, 119, 777-788.
89. Tsukuda,T., Fleming,A.B., Nickoloff,J.A. and Osley,M.A. (2005) Chromatin remodelling at a DNA double-strand break site in Saccharomyces cerevisiae. Nature, 438, 379-383.
90. Loizou,J.I., Murr,R., Finkbeiner,M.G., Sawan,C., Wang,Z.Q. and Herceg,Z. (2006) Epigenetic information in chromatin: The code of entry for DNA repair. Cell Cycle, 5, 696-701.
91. Fernandez,P.C., Frank,S.R., Wang,L., Schroeder,M., Liu,S., Greene,J., Cocito,A. and Amati,B. (2003) Genomic targets of the human c-Myc protein. Genes Dev., 17, 1115-1129.
92. Hassan,A.H., Prochasson,P., Neely,K.E., Galasinski,S.C., Chandy,M., Carrozza,M.J. and Workman,J.L. (2002) Function and selectivity of bromodomains in anchoring chromatin-modifying complexes to promoter nucleosomes. Cell, 111, 369-379.
93. Neely,K.E., Hassan,A.H., Brown,C.E., Howe,L. and Workman,J.L. (2002) Transcription activator interactions with multiple SWI/SNF subunits. Mol. Cell. Biol. 22, 1615-1625.
94. Dhalluin,C., Carlson,J.E., Zeng,L., He,C., Aggarwal,A.K. and Zhou,M.M. (1999) Structure and ligand of a histone acetyltransferase bromodomain. Nature, 399, 491-496.
95. Lukas,C., Melander,F., Stucki,M., Falck,J., Bekker-Jensen,S., Goldberg,M., Lerenthal,Y., Jackson,S.P., Bartek,J. and Lukas,J. (2004) Mdc1 couples DNA double-strand break recognition by Nbs1 with its H2AX-dependent chromatin retention. EMBO J., 23, 2674-2683.
96. 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. (2006) MDC1 maintains genomic stability by participating in the amplification of ATM-dependent DNA damage signals. Mol. Cell, 21, 187-200.
97. Stucki,M., Clapperton,J.A., Mohammad,D., Yaffe,M.B., Smerdon,S.J. and Jackson,S.P. (2005) MDC1 directly binds phosphorylated histone H2AX to regulate cellular responses to DNA double-strand breaks. Cell, 123, 1213-1226.
98. Huen,M.S., Grant,R., Manke,I., Minn,K., Yu,X., Yaffe,M.B. and Chen,J. (2007) RNF8 transduces the DNA-damage signal via histone ubiquitylation and checkpoint protein assembly. Cell, 131, 901-914.
99. Lancelot,N., Charier,G., Couprie,J., Duband-Goulet,I., Alpha-Bazin,B., Quemeneur,E., Ma,E., Marsolier-Kergoat,M.C., Ropars,V., Charbonnier,J.B. et al. (2007) The checkpoint Saccharomyces cerevisiae Rad9 protein contains a tandem tudor domain that recognizes DNA. Nucleic Acids Res., 35, 5898-5912.
100. Wang,B. and Elledge,S.J. (2007) Ubc13/Rnf8 ubiquitin ligases control foci formation of the Rap80/Abraxas/Brca1/Brcc36 complex in response to DNA damage. Proc. Natl Acad. Sci. USA, 104, 20759-20763.
101. Kolas,N.K., Chapman,J.R., Nakada,S., Ylanko,J., Chahwan,R., Sweeney,F.D., Panier,S., Mendez,M., Wildenhain,J., Thomson,T.M. et al. (2007) Orchestration of the DNA-damage response by the RNF8 ubiquitin ligase. Science, 318, 1637-1640.
102. Zhao,G.Y., Sonoda,E., Barber,L.J., Oka,H., Murakawa,Y., Yamada,K., Ikura,T., Wang,X., Kobayashi,M., Yamamoto,K. et al. (2007) A critical role for the ubiquitin-conjugating enzyme Ubc13 in initiating homologous recombination. Mol. Cell, 25, 663-675.
103. Yan,J. and Jetten,A.M. (2008) RAP80 and RNF8, key players in the recruitment of repair proteins to DNA damage sites. Cancer Lett., 271, 179-190.
104. Wang,B., Matsuoka,S., Ballif,B.A., Zhang,D., Smogorzewska,A., Gygi,S.P. and Elledge,S.J. (2007) Abraxas and RAP80 form a BRCA1 protein complex required for the DNA damage response. Science, 316, 1194-1198.
105. Yan,J., Yang,X.P., Kim,Y.S., Joo,J.H. and Jetten,A.M. (2007) RAP80 interacts with the SUMO-conjugating enzyme UBC9 and is a novel target for sumoylation. Biochem. Biophys. Res. Commun., 362, 132-138.
106. Maeda,D., Seki,M., Onoda,F., Branzei,D., Kawabe,Y. and Enomoto,T. (2004) Ubc9 is required for damage-tolerance and damage-induced interchromosomal homologous recombination in S. cerevisiae. DNA Repair, 3, 335-341.
107. Botuyan,M.V., Lee,J., Ward,I.M., Kim,J.E., Thompson,J.R., Chen,J. and Mer,G. (2006) Structural basis for the methylation state-specific recognition of histone H4-K20 by 53BP1 and Crb2 in DNA repair. Cell 127, 1361-1373.
108. Huyen,Y., Zgheib,O., Ditullio,R.A. Jr, Gorgoulis,V.G., Zacharatos,P., Petty,T.J., Sheston,E.A., Mellert,H.S., Stavridi,E.S. and Halazonetis,T.D. (2004) Methylated lysine 79 of histone H3 targets 53BP1 to DNA double-strand breaks. Nature, 432, 406-411.
109. Xie,A., Hartlerode,A., Stucki,M., Odate,S., Puget,N., Kwok,A., Nagaraju,G., Yan,C., Alt,F.W., Chen,J. et al. (2007) Distinct roles of chromatin-associated proteins MDC1 and 53BP1 in mammalian double-strand break repair. Mol. Cell, 28, 1045-1057.
110. Lavin,M.F. and Kozlov,S. (2007) ATM activation and DNA damage response. Cell Cycle, 6, 931-942.
111. Bentley,N.J., Holtzman,D.A., Flaggs,G., Keegan,K.S., DeMaggio,A., Ford,J.C., Hoekstra,M. and Carr,A.M. (1996) The Schizosaccharomyces pombe rad3 checkpoint gene. EMBO J., 15, 6641-6651.
112. Lydall,D., Nikolsky,Y., Bishop,D.K. and Weinert,T. (1996) A meiotic recombination checkpoint controlled by mitotic checkpoint genes. Nature, 383, 840-843.
113. Keith,C.T. and Schreiber,S.L. (1995) PIK-related kinases: DNA repair, recombination, and cell cycle checkpoints. Science, 270, 50-51.
114. Savitsky,K., Bar-Shira,A., Gilad,S., Rotman,G., Ziv,Y., Vanagaite,L., Tagle,D.A., Smith,S., Uziel,T., Sfez,S. et al. (1995) A single ataxia telangiectasia gene with a product similar to PI-3 kinase. Science, 268, 1749-1753.
115. Barlow,C., Hirotsune,S., Paylor,R., Liyanage,M., Eckhaus,M., Collins,F., Shiloh,Y., Crawley,J.N., Ried,T., Tagle,D. et al. (1996) Atm-deficient mice: A paradigm of ataxia telangiectasia. Cell, 86, 159-171.
116. Elson,A., Wang,Y., Daugherty,C.J., Morton,C.C., Zhou,F., Campos-Torres,J. and Leder,P. (1996) Pleiotropic defects in ataxia-telangiectasia protein-deficient mice. Proc. Natl Acad. Sci. USA, 93, 13084-13089.
117. Xu,Y., Ashley,T., Brainerd,E.E., Bronson,R.T., Meyn,M.S. and Baltimore,D. (1996) Targeted disruption of ATM leads to growth retardation, chromosomal fragmentation during meiosis, immune defects, and thymic lymphoma. Genes Dev., 10, 2411-2422.
118. Kozlov,S.V., Graham,M.E., Peng,C., Chen,P., Robinson,P.J. and Lavin,M.F. (2006) Involvement of novel autophosphorylation sites in ATM activation. EMBO J., 25, 3504-3514.
119. Callen,E., Jankovic,M., Difilippantonio,S., Daniel,J.A., Chen,H.T., Celeste,A., Pellegrini,M., McBride,K., Wangsa,D., Bredemeyer,A.L. et al. (2007) ATM prevents the persistence and propagation of chromosome breaks in lymphocytes. Cell, 130, 63-75.
120. Richard,D.J., Bolderson,E., Cubeddu,L., Wadsworth,R.I., Savage,K., Sharma,G.G., Nicolette,M.L., Tsvetanov,S., McIlwraith,M.J., Pandita,R.K. et al. (2008) Single-stranded DNA-binding protein hSSB1 is critical for genomic stability. Nature, 453, 677-681.
121. Usui,T., Ogawa,H. and Petrini,J.H. (2001) A DNA damage response pathway controlled by Tel1 and the Mre11 complex. Mol. Cell, 7, 1255-1266.
122. Trenz,K., Smith,E., Smith,S. and Costanzo,V. (2006) ATM and ATR promote Mre11 dependent restart of collapsed replication forks and prevent accumulation of DNA breaks. EMBO J., 25, 1764-1774.
123. Myers,J.S. and Cortez,D. (2006) Rapid activation of ATR by ionizing radiation requires ATM and Mre11. J. Biol. Chem., 281, 9346-9350.
124. Moens,P.B., Tarsounas,M., Morita,T., Habu,T., Rottinghaus,S.T., Freire,R., Jackson,S.P., Barlow,C. and Wynshaw-Boris,A. (1999) The association of ATR protein with mouse meiotic chromosome cores. Chromosoma, 108, 95-102.
125. Barlow,C., Liyanage,M., Moens,P.B., Tarsounas,M., Nagashima,K., Brown,K., Rottinghaus,S., Jackson,S.P., Tagle,D., Ried,T. et al. (1998) Atm deficiency results in severe meiotic disruption as early as leptonema of prophase I. Development, 125, 4007-4017.
126. Flaggs,G., Plug,A.W., Dunks,K.M., Mundt,K.E., Ford,J.C., Quiggle,M.R., Taylor,E.M., Westphal,C.H., Ashley,T., Hoekstra,M.F. et al. (1997) Atm-dependent interactions of a mammalian chk1 homolog with meiotic chromosomes. Curr. Biol., 7, 977-986.
127. Grushcow,J.M., Holzen,T.M., Park,K.J., Weinert,T., Lichten,M. and Bishop,D.K. (1999) Saccharomyces cerevisiae checkpoint genes MEC1, RAD17 and RAD24 are required for normal meiotic recombination partner choice. Genetics, 153, 607-620.
128. Brush,G.S., Morrow,D.M., Hieter,P. and Kelly,T.J. (1996) The ATM homologue MEC1 is required for phosphorylation of replication protein A in yeast. Proc. Natl Acad. Sci. USA, 93, 15075-15080.
129. Shinohara,A., Ogawa,H. and Ogawa,T. (1992) Rad51 protein involved in repair and recombination in S. cerevisiae is a RecA-like protein. Cell, 69, 457-470.
130. Shinohara,A., Gasior,S., Ogawa,T., Kleckner,N. and Bishop,D.K. (1997) Saccharomyces cerevisiae recA homologues RAD51 and DMC1 have both distinct and overlapping roles in meiotic recombination. Genes Cells 2, 615-629.
131. Anderson,L.K., Offenberg,H.H., Verkuijlen,W.M. and Heyting,C. (1997) RecA-like proteins are components of early meiotic nodules in lily. Proc. Natl Acad. Sci. USA, 94, 6868-6873.
132. Tarsounas,M., Morita,T., Pearlman,R.E. and Moens,P.B. (1999) RAD51 and DMC1 form mixed complexes associated with mouse meiotic chromosome cores and synaptonemal complexes. J. Cell Biol., 147, 207-220.
133. Terasawa,M., Shinohara,A., Hotta,Y., Ogawa,H. and Ogawa,T. (1995) Localization of RecA-like recombination proteins on chromosomes of the lily at various meiotic stages. Genes Dev., 9, 925-934.
134. Stucki,M., Jonsson,Z.O. and Hubscher,U. (2001) In eukaryotic flap endonuclease 1, the C terminus is essential for substrate binding. J. Biol. Chem., 276, 7843-7849.
135. Kysela,B., Chovanec,M. and Jeggo,P.A. (2005) Phosphorylation of linker histones by DNA-dependent protein kinase is required for DNA ligase IV-dependent ligation in the presence of histone H1. Proc. Natl Acad. Sci. USA, 102, 1877-1882.
136. Hamer,G., Roepers-Gajadien,H.L., van Duyn-Goedhart,A., Gademan,I.S., Kal,H.B., van Buul,P.P. and de Rooij,D.G. (2003) DNA double-strand breaks and gamma-H2AX signaling in the testis. Biol. Reprod., 68, 628-634.
137. Gurley,K.E., Moser,R., Gu,Y., Hasty,P. and Kemp,C.J. (2008) DNA-PK suppresses a p53-independent apoptotic response to DNA damage. EMBO Rep., 10, 87-93.
138. Gao,Y., Chaudhuri,J., Zhu,C., Davidson,L., Weaver,D.T. and Alt,F.W. (1998) A targeted DNA-PKcs-null mutation reveals DNA-PK-independent functions for KU in V(D)J recombination. Immunity, 9, 367-376.
139. Keeney,S., Giroux,C.N. and Kleckner,N. (1997) Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell, 88, 375-384.
140. McKim,K.S., Green-Marroquin,B.L., Sekelsky,J.J., Chin,G., Steinberg,C., Khodosh,R. and Hawley,R.S. (1998) Meiotic synapsis in the absence of recombination. Science, 279, 876-878.
141. McKim,K.S. and Hayashi-Hagihara,A. (1998) mei-W68 in Drosophila melanogaster encodes a Spo11 homolog: Evidence that the mechanism for initiating meiotic recombination is conserved. Genes Dev., 12 2932-2942.
142. Romanienko,P.J. and Camerini-Otero,R.D. (1999) Cloning, characterization, and localization of mouse and human SPO11. Genomics 61, 156-169.
143. Keeney,S., Baudat,F., Angeles,M., Zhou,Z.H., Copeland,N.G., Jenkins,N.A., Manova,K. and Jasin,M. (1999) A mouse homolog of the Saccharomyces cerevisiae meiotic recombination DNA transesterase Spo11p. Genomics, 61, 170-182.
144. Lichten,M. (2001) Meiotic recombination: Breaking the genome to save it. Curr. Biol., 11, R253-256.
145. Menees,T.M., Ross-MacDonald,P.B. and Roeder,G.S. (1992) MEI4, a meiosis-specific yeast gene required for chromosome synapsis. Mol. Cell. Biol., 12, 1340-1351.
146. Rockmill,B., Engebrecht,J.A., Scherthan,H., Loidl,J. and Roeder,G.S. (1995) The yeast MER2 gene is required for chromosome synapsis and the initiation of meiotic recombination. Genetics, 141, 49-59.
147. Molnar,M., Parisi,S., Kakihara,Y., Nojima,H., Yamamoto,A., Hiraoka,Y., Bozsik,A., Sipiczki,M. and Kohli,J. (2001) Characterization of rec7, an early meiotic recombination gene in Schizosaccharomyces pombe. Genetics, 157, 519-532.
148. Molnar,M., Bahler,J., Kohli,J. and Hiraoka,Y. (2001) Live observation of fission yeast meiosis in recombination-deficient mutants: A study on achiasmate chromosome segregation. J. Cell Sci., 114, 2843-2853.
149. Gardiner,J.M., Bullard,S.A., Chrome,C. and Malone,R.E. (1997) Molecular and genetic analysis of REC103, an early meiotic recombination gene in yeast. Genetics, 146, 1265-1274.
150. Ajimura,M., Leem,S.H. and Ogawa,H. (1993) Identification of new genes required for meiotic recombination in Saccharomyces cerevisiae. Genetics, 133, 51-66.
151. Ivanov,E.L., Korolev,V.G. and Fabre,F. (1992) XRS2, a DNA repair gene of Saccharomyces cerevisiae, is needed for meiotic recombination. Genetics, 132, 651-664.
152. Johzuka,K. and Ogawa,H. (1995) Interaction of Mre11 and Rad50: Two proteins required for DNA repair and meiosis-specific double-strand break formation in Saccharomyces cerevisiae. Genetics, 139, 1521-1532.
153. Baudat,F., Manova,K., Yuen,J.P., Jasin,M. and Keeney,S. (2000) Chromosome synapsis defects and sexually dimorphic meiotic progression in mice lacking Spo11. Mol. Cell, 6, 989-998.
154. Romanienko,P.J. and Camerini-Otero,R.D. (2000) The mouse Spo11 gene is required for meiotic chromosome synapsis. Mol. Cell, 6, 975-987.
155. Tokuyama,H. and Tokuyama,Y. (2000) Mouse homolog of Saccharomyces cerevisiae spo11 is induced in normal mu(+)B-cells by stimuli that cause germline C(H) transcription and subsequent class switch recombination. Cell Immunol., 202, 1-5.
156. Tokuyama,H. and Tokuyama,Y. (2001) Class switch recombination signals induce lymphocyte-derived Spo11 expression and Spo11 antisense oligonucleotide inhibits class switching. Cell Immunol., 211 123-130.
157. Klein,U., Esposito,G., Baudat,F., Keeney,S. and Jasin,M. (2002) Mice deficient for the type II topoisomerase-like DNA transesterase Spo11 show normal immunoglobulin somatic hypermutation and class switching. Eur. J. Immunol., 32, 316-321.
158. Petukhova,G.V., Romanienko,P.J. and Camerini-Otero,R.D. (2003) The Hop2 protein has a direct role in promoting interhomolog interactions during mouse meiosis. Dev. Cell, 5, 927-936.
159. Liu,Y., Subrahmanyam,R., Chakraborty,T., Sen,R. and Desiderio,S. (2007) A plant homeodomain in RAG-2 that binds Hypermethylated lysine 4 of histone H3 is necessary for efficient antigen-receptor-gene rearrangement. Immunity, 27, 561-571.
160. Matthews,A.G., Kuo,A.J., Ramon-Maiques,S., Han,S., Champagne,K.S., Ivanov,D., Gallardo,M., Carney,D., Cheung,P., Ciccone,D.N. et al. (2007) RAG2 PHD finger couples histone H3 lysine 4 trimethylation with V(D)J recombination. Nature, 450, 1106-1110.
161. Elledge,S.J. (1996) Cell cycle checkpoints: Preventing an identity crisis. Science, 274, 1664-1672.
162. O'Driscoll,M. and Jeggo,P.A. (2006) The role of double-strand break repair - insights from human genetics. Nat. Rev. Genet., 7, 45-54.
163. Luo,G., Yao,M.S., Bender,C.F., Mills,M., Bladl,A.R., Bradley,A. and Petrini,J.H. (1999) Disruption of mRad50 causes embryonic stem cell lethality, abnormal embryonic development, and sensitivity to ionizing radiation. Proc. Natl Acad. Sci. USA, 96, 7376-7381.
164. Zhu,J., Petersen,S., Tessarollo,L. and Nussenzweig,A. (2001) Targeted disruption of the Nijmegen breakage syndrome gene NBS1 leads to early embryonic lethality in mice. Curr. Biol., 11, 105-109.
165. Shim,E.Y., Hong,S.J., Oum,J.H., Yanez,Y., Zhang,Y. and Lee,S.E. (2007) RSC mobilizes nucleosomes to improve accessibility of repair machinery to the damaged chromatin. Mol. Cell. Biol., 27, 1602-1613.
166. Shim,E.Y., Ma,J.L., Oum,J.H., Yanez,Y. and Lee,S.E. (2005) The yeast chromatin remodeler RSC complex facilitates end joining repair of DNA double-strand breaks. Mol. Cell. Biol., 25, 3934-3944.
167. Chowdhury,D., Keogh,M.C., Ishii,H., Peterson,C.L., Buratowski,S. and Lieberman,J. (2005) gamma-H2AX dephosphorylation by protein phosphatase 2A facilitates DNA double-strand break repair. Mol. Cell, 20 801-809.
168. Keogh,M.C., Kim,J.A., Downey,M., Fillingham,J., Chowdhury,D., Harrison,J.C., Onishi,M., Datta,N., Galicia,S., Emili,A. et al. (2006) A phosphatase complex that dephosphorylates gammaH2AX regulates DNA damage checkpoint recovery. Nature, 439, 497-501.
169. Tamburini,B.A. and Tyler,J.K. (2005) Localized histone acetylation and deacetylation triggered by the homologous recombination pathway of double-strand DNA repair. Mol. Cell. Biol., 25, 4903-4913.