Focus on histone variant H2AX: To be or not to be

FEBS Letters

Volumn 584, Issue 17, 2010, Pages 3717-3724

  Yuan, Jingsong ^a   Adamski, Rachel ^a   Chen, Junjie ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

DNA damage; DNA repair; H2AX; Homologous recombination; MRE11 RAD50 NBS1; Non homologous end joining

Indexed keywords

ATM PROTEIN; ATR PROTEIN; BRCA1 ASSOCIATED RING DOMAIN PROTEIN 1; BRCA1 PROTEIN; DNA; DNA DEPENDENT PROTEIN KINASE; HISTONE H2AX; MRE11 PROTEIN; NIBRIN; RAD50 PROTEIN; RAD51 PROTEIN; SERINE; SUMO PROTEIN;

ACETYLATION; APOPTOSIS; CELL DEATH; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA REPAIR; DOUBLE STRANDED DNA BREAK; HOMOLOGOUS RECOMBINATION; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; REVIEW; SIGNAL TRANSDUCTION; UBIQUITINATION;

ANIMALS; DNA; DNA BREAKS, DOUBLE-STRANDED; DNA DAMAGE; DNA REPAIR; GENETIC VARIATION; HISTONES; HUMANS; MAMMALS; PHOSPHORYLATION; PHOSPHOSERINE; SERINE; UBIQUITIN;

ANIMALIA; MAMMALIA;

EID: 77955841541     PISSN: 00145793     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.febslet.2010.05.021     Document Type: Review

References (140)

1. Jeggo P.A., Lobrich M. DNA double-strand breaks: their cellular and clinical impact?. Oncogene 2007, 26:7717-7719.
2. McKinnon P.J., Caldecott K.W. DNA strand break repair and human genetic disease. Annu. Rev. Genomics Hum. Genet. 2007, 8:37-55.
3. Rogakou E.P., Pilch D.R., Orr A.H., Ivanova V.S., Bonner W.M. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J. Biol. Chem. 1998, 273:5858-5868.
4. Ismail I.H., Wadhra T.I., Hammarsten O. An optimized method for detecting gamma-H2AX in blood cells reveals a significant interindividual variation in the gamma-H2AX response among humans. Nucleic Acids Res. 2007, 35:e36.
5. Takahashi A., Ohnishi T. Does gammaH2AX foci formation depend on the presence of DNA double strand breaks?. Cancer Lett. 2005, 229:171-179.
6. Pommier Y. Topoisomerase I inhibitors: camptothecins and beyond. Nat. Rev. Cancer 2006, 6:789-802.
7. Guirouilh-Barbat J., Redon C., Pommier Y. Transcription-coupled DNA double-strand breaks are mediated via the nucleotide excision repair and the Mre11-Rad50-Nbs1 complex. Mol. Biol. Cell 2008, 19:3969-3981.
8. Yuan J., Ghosal G., Chen J. The annealing helicase HARP protects stalled replication forks. Genes Dev. 2009, 23:2394-2399.
9. Marti T.M., Hefner E., Feeney L., Natale V., Cleaver J.E. H2AX phosphorylation within the G1 phase after UV irradiation depends on nucleotide excision repair and not DNA double-strand breaks. Proc. Natl. Acad. Sci. USA 2006, 103:9891-9896.
10. Ward I.M., Chen J. Histone H2AX is phosphorylated in an ATR-dependent manner in response to replicational stress. J. Biol. Chem. 2001, 276:47759-47762.
11. Edry E., Melamed D. Class switch recombination: a friend and a foe. Clin. Immunol. 2007, 123:244-251.
12. Soulas-Sprauel P., Rivera-Munoz P., Malivert L., Le Guyader G., Abramowski V., Revy P., de Villartay J.P. V(D)J and immunoglobulin class switch recombinations: a paradigm to study the regulation of DNA end-joining. Oncogene 2007, 26:7780-7791.
13. Chicheportiche A., Bernardino-Sgherri J., de Massy B., Dutrillaux B. Characterization of Spo11-dependent and independent phospho-H2AX foci during meiotic prophase I in the male mouse. J. Cell Sci. 2007, 120:1733-1742.
14. Takai H., Smogorzewska A., de Lange T. DNA damage foci at dysfunctional telomeres. Curr. Biol. 2003, 13:1549-1556.
15. Nakamura A.J., Chiang Y.J., Hathcock K.S., Horikawa I., Sedelnikova O.A., Hodes R.J., Bonner W.M. Both telomeric and non-telomeric DNA damage are determinants of mammalian cellular senescence. Epigenetics Chromatin 2008, 1:6.
16. Daniel R., et al. Histone H2AX is phosphorylated at sites of retroviral DNA integration but is dispensable for postintegration repair. J. Biol. Chem. 2004, 279:45810-45814.
17. Moynahan M.E., Jasin M. Mitotic homologous recombination maintains genomic stability and suppresses tumorigenesis. Nat. Rev. Mol. Cell Biol. 2010, 11:196-207.
18. d'Adda di Fagagna F. Living on a break: cellular senescence as a DNA-damage response. Nat. Rev. Cancer 2008, 8:512-522.
19. Bonner W.M., Redon C.E., Dickey J.S., Nakamura A.J., Sedelnikova O.A., Solier S., Pommier Y. GammaH2AX and cancer. Nat. Rev. Cancer 2008, 8:957-967.
20. Bartova E., Krejci J., Harnicarova A., Galiova G., Kozubek S. Histone modifications and nuclear architecture: a review. J. Histochem. Cytochem. 2008, 56:711-721.
21. Paull T.T., Rogakou E.P., Yamazaki V., Kirchgessner C.U., Gellert M., Bonner W.M. A critical role for histone H2AX in recruitment of repair factors to nuclear foci after DNA damage. Curr. Biol. 2000, 10:886-895.
22. Celeste A., et al. Genomic instability in mice lacking histone H2AX. Science 2002, 296:922-927.
23. Celeste A., et al. H2AX haploinsufficiency modifies genomic stability and tumor susceptibility. Cell 2003, 114:371-383.
24. Bassing C.H., et al. Histone H2AX: a dosage-dependent suppressor of oncogenic translocations and tumors. Cell 2003, 114:359-370.
25. Huen M.S., Chen J. Assembly of checkpoint and repair machineries at DNA damage sites. Trends Biochem. Sci. 2010, 35:101-108.
26. Chowdhury D., Keogh M.C., Ishii H., Peterson C.L., Buratowski S., Lieberman J. Gamma-H2AX dephosphorylation by protein phosphatase 2A facilitates DNA double-strand break repair. Mol. Cell 2005, 20:801-809.
27. Chowdhury D., et al. A PP4-phosphatase complex dephosphorylates gamma-H2AX generated during DNA replication. Mol. Cell 2008, 31:33-46.
28. Nakada S., Chen G.I., Gingras A.C., Durocher D. PP4 is a gamma H2AX phosphatase required for recovery from the DNA damage checkpoint. EMBO Rep. 2008, 9:1019-1026.
29. Douglas P., Zhong J., Ye R., Moorhead G.B., Xu X., Lees-Miller S.P. Protein phosphatase 6 interacts with the DNA-dependent protein kinase catalytic subunit and dephosphorylates gamma-H2AX. Mol. Cell Biol. 2010, 30:1368-1381.
30. Macurek, L., Lindqvist, A., Voets, O., Kool, J., Vos, H.R. and Medema, R.H. (2010). Wip1 phosphatase is associated with chromatin and dephosphorylates gammaH2AX to promote checkpoint inhibition. Oncogene doi:10.1038/onc.2009.501.
31. Lou Z., et al. MDC1 maintains genomic stability by participating in the amplification of ATM-dependent DNA damage signals. Mol. Cell 2006, 21:187-200.
32. Stucki M., Clapperton J.A., Mohammad D., Yaffe M.B., Smerdon S.J., Jackson S.P. MDC1 directly binds phosphorylated histone H2AX to regulate cellular responses to DNA double-strand breaks. Cell 2005, 123:1213-1226.
33. Wu L., Luo K., Lou Z., Chen J. MDC1 regulates intra-S-phase checkpoint by targeting NBS1 to DNA double-strand breaks. Proc. Natl. Acad. Sci. USA 2008, 105:11200-11205.
34. Spycher C., Miller E.S., Townsend K., Pavic L., Morrice N.A., Janscak P., Stewart G.S., Stucki M. Constitutive phosphorylation of MDC1 physically links the MRE11-RAD50-NBS1 complex to damaged chromatin. J. Cell Biol. 2008, 181:227-240.
35. Melander F., Bekker-Jensen S., Falck J., Bartek J., Mailand N., Lukas J. Phosphorylation of SDT repeats in the MDC1 N terminus triggers retention of NBS1 at the DNA damage-modified chromatin. J. Cell Biol. 2008, 181:213-226.
36. Chapman J.R., Jackson S.P. Phospho-dependent interactions between NBS1 and MDC1 mediate chromatin retention of the MRN complex at sites of DNA damage. EMBO Rep. 2008, 9:795-801.
37. Huen M.S., Grant R., Manke I., Minn K., Yu X., Yaffe M.B., Chen J. RNF8 transduces the DNA-damage signal via histone ubiquitylation and checkpoint protein assembly. Cell 2007, 131:901-914.
38. Kolas N.K., et al. Orchestration of the DNA-damage response by the RNF8 ubiquitin ligase. Science 2007, 318:1637-1640.
39. Mailand N., Bekker-Jensen S., Faustrup H., Melander F., Bartek J., Lukas C., Lukas J. RNF8 ubiquitylates histones at DNA double-strand breaks and promotes assembly of repair proteins. Cell 2007, 131:887-900.
40. Wang B., Elledge S.J. Ubc13/Rnf8 ubiquitin ligases control foci formation of the Rap80/Abraxas/Brca1/Brcc36 complex in response to DNA damage. Proc. Natl. Acad. Sci. USA 2007, 104:20759-20763.
41. Sobhian B., Shao G., Lilli D.R., Culhane A.C., Moreau L.A., Xia B., Livingston D.M., Greenberg R.A. RAP80 targets BRCA1 to specific ubiquitin structures at DNA damage sites. Science 2007, 316:1198-1202.
42. Stucki M., Jackson S.P. GammaH2AX and MDC1: anchoring the DNA-damage-response machinery to broken chromosomes. DNA Repair (Amst) 2006, 5:534-543.
43. Wood J.L., Singh N., Mer G., Chen J. MCPH1 functions in an H2AX-dependent but MDC1-independent pathway in response to DNA damage. J. Biol. Chem. 2007, 282:35416-35423.
44. Wood J.L., Liang Y., Li K., Chen J. Microcephalin/MCPH1 associates with the Condensin II complex to function in homologous recombination repair. J. Biol. Chem. 2008, 283:29586-29592.
45. Peng G., et al. BRIT1/MCPH1 links chromatin remodelling to DNA damage response. Nat. Cell Biol. 2009, 11:865-872.
46. Alderton G.K., Galbiati L., Griffith E., Surinya K.H., Neitzel H., Jackson A.P., Jeggo P.A., O'Driscoll M. Regulation of mitotic entry by microcephalin and its overlap with ATR signalling. Nat. Cell Biol. 2006, 8:725-733.
47. Chaplet M., Rai R., Jackson-Bernitsas D., Li K., Lin S.Y. BRIT1/MCPH1: a guardian of genome and an enemy of tumors. Cell Cycle 2006, 5:2579-2583.
48. Artus C., et al. AIF promotes chromatinolysis and caspase-independent programmed necrosis by interacting with histone H2AX. EMBO J. 2010, 29:1585-1599.
49. Rogakou E.P., Nieves-Neira W., Boon C., Pommier Y., Bonner W.M. Initiation of DNA fragmentation during apoptosis induces phosphorylation of H2AX histone at serine 139. J. Biol. Chem. 2000, 275:9390-9395.
50. Mukherjee B., Kessinger C., Kobayashi J., Chen B.P., Chen D.J., Chatterjee A., Burma S. DNA-PK phosphorylates histone H2AX during apoptotic DNA fragmentation in mammalian cells. DNA Repair (Amst) 2006, 5:575-590.
51. Solier S., Sordet O., Kohn K.W., Pommier Y. Death receptor-induced activation of the Chk2- and histone H2AX-associated DNA damage response pathways. Mol. Cell Biol. 2009, 29:68-82.
52. Lu C., Zhu F., Cho Y.Y., Tang F., Zykova T., Ma W.Y., Bode A.M., Dong Z. Cell apoptosis: requirement of H2AX in DNA ladder formation, but not for the activation of caspase-3. Mol. Cell 2006, 23:121-132.
53. Lu C., Shi Y., Wang Z., Song Z., Zhu M., Cai Q., Chen T. Serum starvation induces H2AX phosphorylation to regulate apoptosis via p38 MAPK pathway. FEBS Lett. 2008, 582:2703-2708.
54. Smith G.C., d'Adda di Fagagna F., Lakin N.D., Jackson S.P. Cleavage and inactivation of ATM during apoptosis. Mol. Cell Biol. 1999, 19:6076-6084.
55. Cook P.J., Ju B.G., Telese F., Wang X., Glass C.K., Rosenfeld M.G. Tyrosine dephosphorylation of H2AX modulates apoptosis and survival decisions. Nature 2009, 458:591-596.
56. Xiao A., et al. WSTF regulates the H2A.X DNA damage response via a novel tyrosine kinase activity. Nature 2009, 457:57-62.
57. Palm W., de Lange T. How shelterin protects mammalian telomeres. Annu. Rev. Genet. 2008, 42:301-334.
58. Blackburn E.H. Switching and signaling at the telomere. Cell 2001, 106:661-673.
59. Wright W.E., Shay J.W. Telomere-binding factors and general DNA repair. Nat. Genet. 2005, 37:116-118.
60. Hao L.Y., Strong M.A., Greider C.W. Phosphorylation of H2AX at short telomeres in T cells and fibroblasts. J. Biol. Chem. 2004, 279:45148-45154.
61. Kim J.A., Kruhlak M., Dotiwala F., Nussenzweig A., Haber J.E. Heterochromatin is refractory to gamma-H2AX modification in yeast and mammals. J. Cell Biol. 2007, 178:209-218.
62. Fernandez-Capetillo O., et al. DNA damage-induced G2-M checkpoint activation by histone H2AX and 53BP1. Nat. Cell Biol. 2002, 4:993-997.
63. Messick T.E., Greenberg R.A. The ubiquitin landscape at DNA double-strand breaks. J. Cell Biol. 2009, 187:319-326.
64. van Attikum H., Gasser S.M. Crosstalk between histone modifications during the DNA damage response. Trends Cell Biol. 2009, 19:207-217.
65. Huen M.S., Huang J., Yuan J., Yamamoto M., Akira S., Ashley C., Xiao W., Chen J. Noncanonical E2 variant-independent function of UBC13 in promoting checkpoint protein assembly. Mol. Cell Biol. 2008, 28:6104-6112.
66. Stewart G.S., et al. The RIDDLE syndrome protein mediates a ubiquitin-dependent signaling cascade at sites of DNA damage. Cell 2009, 136:420-434.
67. Doil C., et al. RNF168 binds and amplifies ubiquitin conjugates on damaged chromosomes to allow accumulation of repair proteins. Cell 2009, 136:435-446.
68. Wu J., Huen M.S., Lu L.Y., Ye L., Dou Y., Ljungman M., Chen J., Yu X. Histone ubiquitination associates with BRCA1-dependent DNA damage response. Mol. Cell Biol. 2009, 29:849-860.
69. Bekker-Jensen S., Rendtlew Danielsen J., Fugger K., Gromova I., Nerstedt A., Bartek J., Lukas J., Mailand N. HERC2 coordinates ubiquitin-dependent assembly of DNA repair factors on damaged chromosomes. Nat. Cell Biol. 2010, 12:80-86. (suppl. pp. 1-12).
70. Galanty Y., Belotserkovskaya R., Coates J., Polo S., Miller K.M., Jackson S.P. Mammalian SUMO E3-ligases PIAS1 and PIAS4 promote responses to DNA double-strand breaks. Nature 2009, 462:935-939.
71. Morris J.R., et al. The SUMO modification pathway is involved in the BRCA1 response to genotoxic stress. Nature 2009, 462:886-890.
72. Kim H., Huang J., Chen J. CCDC98 is a BRCA1-BRCT domain-binding protein involved in the DNA damage response. Nat. Struct. Mol. Biol. 2007, 14:710-715.
73. Liu Z., Wu J., Yu X. CCDC98 targets BRCA1 to DNA damage sites. Nat. Struct. Mol. Biol. 2007, 14:716-720.
74. Wang B., Matsuoka S., Ballif B.A., Zhang D., Smogorzewska A., Gygi S.P., Elledge S.J. Abraxas and RAP80 form a BRCA1 protein complex required for the DNA damage response. Science 2007, 316:1194-1198.
75. Deng C.X. BRCA1: cell cycle checkpoint, genetic instability, DNA damage response and cancer evolution. Nucleic Acids Res. 2006, 34:1416-1426.
76. Durant S.T., Nickoloff J.A. Good timing in the cell cycle for precise DNA repair by BRCA1. Cell Cycle 2005, 4:1216-1222.
77. Huang J., Huen M.S., Kim H., Leung C.C., Glover J.N., Yu X., Chen J. RAD18 transmits DNA damage signalling to elicit homologous recombination repair. Nat. Cell Biol. 2009, 11:592-603.
78. Huyen Y., et al. Methylated lysine 79 of histone H3 targets 53BP1 to DNA double-strand breaks. Nature 2004, 432:406-411.
79. Sanders S.L., Portoso M., Mata J., Bahler J., Allshire R.C., Kouzarides T. Methylation of histone H4 lysine 20 controls recruitment of Crb2 to sites of DNA damage. Cell 2004, 119:603-614.
80. Botuyan M.V., Lee J., Ward I.M., Kim J.E., Thompson J.R., Chen J., Mer G. Structural basis for the methylation state-specific recognition of histone H4-K20 by 53BP1 and Crb2 in DNA repair. Cell 2006, 127:1361-1373.
81. Bird A.W., et al. Acetylation of histone H4 by Esa1 is required for DNA double-strand break repair. Nature 2002, 419:411-415.
82. Ikura T., et al. Involvement of the TIP60 histone acetylase complex in DNA repair and apoptosis. Cell 2000, 102:463-473.
83. Murr R., Loizou J.I., Yang Y.G., Cuenin C., Li H., Wang Z.Q., Herceg Z. Histone acetylation by Trrap-Tip60 modulates loading of repair proteins and repair of DNA double-strand breaks. Nat. Cell Biol. 2006, 8:91-99.
84. Sun Y., Jiang X., Chen S., Fernandes N., Price B.D. A role for the Tip60 histone acetyltransferase in the acetylation and activation of ATM. Proc. Natl. Acad. Sci. USA 2005, 102:13182-13187.
85. Ikura T., et al. DNA damage-dependent acetylation and ubiquitination of H2AX enhances chromatin dynamics. Mol. Cell Biol. 2007, 27:7028-7040.
86. Pandita T.K., Richardson C. Chromatin remodeling finds its place in the DNA double-strand break response. Nucleic Acids Res. 2009, 37:1363-1377.
87. Shogren-Knaak M., Ishii H., Sun J.M., Pazin M.J., Davie J.R., Peterson C.L. Histone H4-K16 acetylation controls chromatin structure and protein interactions. Science 2006, 311:844-847.
88. Conaway R.C., Conaway J.W. The INO80 chromatin remodeling complex in transcription, replication and repair. Trends Biochem. Sci. 2009, 34:71-77.
89. Morrison A.J., Shen X. Chromatin remodelling beyond transcription: the INO80 and SWR1 complexes. Nat. Rev. Mol. Cell Biol. 2009, 10:373-384.
90. Morrison A.J., Highland J., Krogan N.J., Arbel-Eden A., Greenblatt J.F., Haber J.E., Shen X. INO80 and gamma-H2AX interaction links ATP-dependent chromatin remodeling to DNA damage repair. Cell 2004, 119:767-775.
91. van Attikum H., Fritsch O., Hohn B., Gasser S.M. Recruitment of the INO80 complex by H2A phosphorylation links ATP-dependent chromatin remodeling with DNA double-strand break repair. Cell 2004, 119:777-788.
92. Lan L., Nakajima S., Komatsu K., Nussenzweig A., Shimamoto A., Oshima J., Yasui A. Accumulation of Werner protein at DNA double-strand breaks in human cells. J. Cell Sci. 2005, 118:4153-4162.
93. Karmakar P., et al. BLM is an early responder to DNA double-strand breaks. Biochem. Biophys. Res. Commun. 2006, 348:62-69.
94. Zeitlin S.G., Baker N.M., Chapados B.R., Soutoglou E., Wang J.Y., Berns M.W., Cleveland D.W. Double-strand DNA breaks recruit the centromeric histone CENP-A. Proc. Natl. Acad. Sci. USA 2009, 106:15762-15767.
95. Celeste A., et al. Histone H2AX phosphorylation is dispensable for the initial recognition of DNA breaks. Nat. Cell Biol. 2003, 5:675-679.
96. Yuan J., Chen J. MRE11-RAD50-NBS1 complex dictates DNA repair independent of H2AX. J. Biol. Chem. 2010, 285:1097-1104.
97. Bassing C.H., Alt F.W. H2AX may function as an anchor to hold broken chromosomal DNA ends in close proximity. Cell Cycle 2004, 3:149-153.
98. Bassing C.H., et al. Increased ionizing radiation sensitivity and genomic instability in the absence of histone H2AX. Proc. Natl. Acad. Sci. USA 2002, 99:8173-8178.
99. Lieber, M.R. (2010). The mechanism of double-strand DNA break repair by the nonhomologous DNA end-joining pathway. Annu. Rev. Biochem. 79 [Epub ahead of print].
100. Xie A., Kwok A., Scully R. Role of mammalian Mre11 in classical and alternative nonhomologous end joining. Nat. Struct. Mol. Biol. 2009, 16:814-818.
101. Jazayeri A., Balestrini A., Garner E., Haber J.E., Costanzo V. Mre11-Rad50-Nbs1-dependent processing of DNA breaks generates oligonucleotides that stimulate ATM activity. EMBO J. 2008, 27:1953-1962.
102. Lee J.H., Paull T.T. Direct activation of the ATM protein kinase by the Mre11/Rad50/Nbs1 complex. Science 2004, 304:93-96.
103. Lee J.H., Paull T.T. ATM activation by DNA double-strand breaks through the Mre11-Rad50-Nbs1 complex. Science 2005, 308:551-554.
104. Williams R.S., et al. Mre11 dimers coordinate DNA end bridging and nuclease processing in double-strand-break repair. Cell 2008, 135:97-109.
105. Buis J., et al. Mre11 nuclease activity has essential roles in DNA repair and genomic stability distinct from ATM activation. Cell 2008, 135:85-96.
106. Adams M.M., Carpenter P.B. Tying the loose ends together in DNA double strand break repair with 53BP1. Cell Div. 2006, 1:19.
107. Orsburn, B., Escudero, B., Prakash, M., Gesheva, S., Liu, G., Huso, D.L. and Franco, S. (2010). Differential requirement for H2AX and 53BP1 in organismal development and genome maintenance in the absence of PARP1. Mol. Cell Biol. doi:10.1128/MCB.00091-10.
108. Difilippantonio S., et al. 53BP1 facilitates long-range DNA end-joining during V(D)J recombination. Nature 2008, 456:529-533.
109. Manis J.P., Morales J.C., Xia Z., Kutok J.L., Alt F.W., Carpenter P.B. 53BP1 links DNA damage-response pathways to immunoglobulin heavy chain class-switch recombination. Nat. Immunol. 2004, 5:481-487.
110. Ward I.M., et al. 53BP1 is required for class switch recombination. J. Cell Biol. 2004, 165:459-464.
111. Boisvert F.M., Rhie A., Richard S., Doherty A.J. The GAR motif of 53BP1 is arginine methylated by PRMT1 and is necessary for 53BP1 DNA binding activity. Cell Cycle 2005, 4:1834-1841.
112. Pryde F., Khalili S., Robertson K., Selfridge J., Ritchie A.M., Melton D.W., Jullien D., Adachi Y. 53BP1 exchanges slowly at the sites of DNA damage and appears to require RNA for its association with chromatin. J. Cell Sci. 2005, 118:2043-2055.
113. Lee J.H., Goodarzi A.A., Jeggo P.A., Paull T.T. 53BP1 promotes ATM activity through direct interactions with the MRN complex. EMBO J. 2010, 29:574-585.
114. Wei L., Lan L., Hong Z., Yasui A., Ishioka C., Chiba N. Rapid recruitment of BRCA1 to DNA double-strand breaks is dependent on its association with Ku80. Mol. Cell Biol. 2008, 28:7380-7393.
115. Bekker-Jensen S., Lukas C., Kitagawa R., Melander F., Kastan M.B., Bartek J., Lukas J. Spatial organization of the mammalian genome surveillance machinery in response to DNA strand breaks. J. Cell Biol. 2006, 173:195-206.
116. Kim J.S., Krasieva T.B., Kurumizaka H., Chen D.J., Taylor A.M., Yokomori K. Independent and sequential recruitment of NHEJ and HR factors to DNA damage sites in mammalian cells. J. Cell Biol. 2005, 170:341-347.
117. Stiff T., O'Driscoll M., Rief N., Iwabuchi K., Lobrich M., Jeggo P.A. ATM and DNA-PK function redundantly to phosphorylate H2AX after exposure to ionizing radiation. Cancer Res. 2004, 64:2390-2396.
118. Yin B., et al. Histone H2AX stabilizes broken DNA strands to suppress chromosome breaks and translocations during V(D)J recombination. J. Exp. Med. 2009, 206:2625-2639.
119. Petersen S., et al. AID is required to initiate Nbs1/gamma-H2AX focus formation and mutations at sites of class switching. Nature 2001, 414:660-665.
120. Reina-San-Martin B., Difilippantonio S., Hanitsch L., Masilamani R.F., Nussenzweig A., Nussenzweig M.C. 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.
121. Xie A., Puget N., Shim I., Odate S., Jarzyna I., Bassing C.H., Alt F.W., Scully R. Control of sister chromatid recombination by histone H2AX. Mol. Cell 2004, 16:1017-1025.
122. Yuan J., Chen J. N terminus of CtIP is critical for homologous recombination-mediated double-strand break repair. J. Biol. Chem. 2009, 284:31746-31752.
123. New J.H., Sugiyama T., Zaitseva E., Kowalczykowski S.C. Rad52 protein stimulates DNA strand exchange by Rad51 and replication protein A. Nature 1998, 391:407-410.
124. Sugiyama T., Kantake N., Wu Y., Kowalczykowski S.C. Rad52-mediated DNA annealing after Rad51-mediated DNA strand exchange promotes second ssDNA capture. EMBO J. 2006, 25:5539-5548.
125. Liu J.S., Kuo S.R., Melendy T. DNA damage-induced RPA focalization is independent of gamma-H2AX and RPA hyper-phosphorylation. J. Cell Biochem. 2006, 99:1452-1462.
126. Sy S.M., Huen M.S., Zhu Y., Chen J. PALB2 regulates recombinational repair through chromatin association and oligomerization. J. Biol. Chem. 2009, 284:18302-18310.
127. Kim H., Chen J., Yu X. Ubiquitin-binding protein RAP80 mediates BRCA1-dependent DNA damage response. Science 2007, 316:1202-1205.
128. Riballo E., et al. A pathway of double-strand break rejoining dependent upon ATM, Artemis, and proteins locating to gamma-H2AX foci. Mol. Cell 2004, 16:715-724.
129. Brown E.J., Baltimore D. ATR disruption leads to chromosomal fragmentation and early embryonic lethality. Genes Dev. 2000, 14:397-402.
130. de Klein A., Muijtjens M., van Os R., Verhoeven Y., Smit B., Carr A.M., Lehmann A.R., Hoeijmakers J.H. Targeted disruption of the cell-cycle checkpoint gene ATR leads to early embryonic lethality in mice. Curr. Biol. 2000, 10:479-482.
131. Zhu J., Petersen S., Tessarollo L., Nussenzweig A. Targeted disruption of the Nijmegen breakage syndrome gene NBS1 leads to early embryonic lethality in mice. Curr. Biol. 2001, 11:105-109.
132. Xiao Y., Weaver D.T. Conditional gene targeted deletion by Cre recombinase demonstrates the requirement for the double-strand break repair Mre11 protein in murine embryonic stem cells. Nucleic Acids Res. 1997, 25:2985-2991.
133. Luo G., Yao M.S., Bender C.F., Mills M., Bladl A.R., Bradley A., Petrini J.H. Disruption of mRad50 causes embryonic stem cell lethality, abnormal embryonic development, and sensitivity to ionizing radiation. Proc. Natl. Acad. Sci. USA 1999, 96:7376-7381.
134. Chen P.L., et al. Inactivation of CtIP leads to early embryonic lethality mediated by G1 restraint and to tumorigenesis by haploid insufficiency. Mol. Cell Biol. 2005, 25:3535-3542.
135. Ludwig T., Chapman D.L., Papaioannou V.E., Efstratiadis A. Targeted mutations of breast cancer susceptibility gene homologs in mice. Lethal phenotypes of Brca1, Brca2, Brca1/Brca2, Brca1/p53, and Brca2/p53 nullizygous embryos. Genes Dev. 1997, 11:1226-1241.
136. Sharan S.K., et al. Embryonic lethality and radiation hypersensitivity mediated by Rad51 in mice lacking Brca2. Nature 1997, 386:804-810.
137. Tsuzuki T., et al. Targeted disruption of the Rad51 gene leads to lethality in embryonic mice. Proc. Natl. Acad. Sci. USA 1996, 93:6236-6240.
138. Barlow C., et al. Atm-deficient mice. A paradigm of ataxia telangiectasia. Cell 1996, 86:159-171.
139. Elson A., Wang Y., Daugherty C.J., Morton C.C., Zhou F., Campos-Torres J., Leder P. Pleiotropic defects in ataxia-telangiectasia protein-deficient mice. Proc. Natl. Acad. Sci. USA 1996, 93:13084-13089.
140. Xu Y., Ashley T., Brainerd E.E., Bronson R.T., Meyn M.S., Baltimore D. Targeted disruption of ATM leads to growth retardation, chromosomal fragmentation during meiosis, immune defects, and thymic lymphoma. Genes Dev. 1996, 10:2411-2422.