γH2AX and MDC1: Anchoring the DNA-damage-response machinery to broken chromosomes

DNA Repair

Volumn 5, Issue 5, 2006, Pages 534-543

  Stucki, Manuel ^a   Jackson, Stephen P ^b  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Chromatin; DNA damage checkpoint; DNA double strand breaks; DNA repair; Foci; Genome stability; Histone H2AX; MDC1

Indexed keywords

ATM PROTEIN; ATR PROTEIN; DEOXYRIBONUCLEOPROTEIN; DNA DEPENDENT PROTEIN KINASE; DOUBLE STRANDED DNA; HISTONE H2AX; MEDIATOR OF DNA DAMAGE CHECKPOINT PROTEIN 1; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN GAMMA H2AX; UNCLASSIFIED DRUG; DNA BINDING PROTEIN; GAMMAH2AX PROTEIN, S CEREVISIAE; HISTONE; MDC1 PROTEIN, HUMAN; NUCLEAR PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN; TRANSACTIVATOR PROTEIN;

CELL ANCHORAGE; CELL CYCLE; CHROMATIN STRUCTURE; CHROMOSOME BREAKAGE; DNA DAMAGE; DNA REPAIR; DNA STRAND BREAKAGE; EPIGENETICS; EUKARYOTE; GENE INDUCTION; GENETIC LINKAGE; MODULATION; MOLECULAR DYNAMICS; MOLECULAR MECHANICS; MOLECULAR RECOGNITION; NONHUMAN; NUCLEOTIDE BINDING SITE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; REGULATORY MECHANISM; REVIEW; TANDEM REPEAT; AMINO ACID SEQUENCE; ANIMAL; BINDING SITE; BIOLOGICAL MODEL; CHEMISTRY; GENETICS; HUMAN; METABOLISM; MOUSE; PHOSPHORYLATION; PROTEIN TERTIARY STRUCTURE;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CHROMOSOME BREAKAGE; DNA DAMAGE; DNA REPAIR; DNA-BINDING PROTEINS; HISTONES; HUMANS; MICE; MODELS, BIOLOGICAL; NUCLEAR PROTEINS; PHOSPHORYLATION; PROTEIN STRUCTURE, TERTIARY; SACCHAROMYCES CEREVISIAE PROTEINS; TRANS-ACTIVATORS;

EID: 33646106590     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2006.01.012     Document Type: Review

References (71)

1. Zhou B.-B.S., and Elledge S.J. The DNA damage response: putting checkpoints in perspective. Nature 408 (2000) 433-439
2. Rouse J., and Jackson S.P. Interfaces between the detection, signaling, and repair of DNA damage. Science 297 (2002) 547-551
3. Khanna K.K., and Jackson S.P. DNA double-strand breaks: signaling, repair and the cancer connection. Nat. Genet. 27 (2001) 247-254
4. Bassing C.H., and Alt F.W. The cellular response to general and programmed DNA double strand breaks. DNA Repair (Amst.) 3 (2004) 781-796
5. Fernandez-Capetillo O., Celeste A., and Nussenzweig A. Focusing on foci: H2AX and the recruitment of DNA-damage response factors. Cell Cycle 2 (2003) 426-427
6. 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., Redon C., Pilch D.R., Olaru A., Eckhaus M., Camerini-Otero R.D., Tessarollo L., Livak F., Manova K., Bonner W.M., Nussenzweig M.C., and Nussenzweig A. Genomic instability in mice lacking histone H2AX. Science 296 (2002) 922-927
7. 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
8. 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
9. 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., Livingston D.M., Ferguson D.O., Scully R., and Alt F.W. Increased ionizing radiation sensitivity and genomic instability in the absence of histone H2AX. Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 8173-8178
10. van Gent D.C., Hoeijmakers J.H., and Kanaar R. Chromosomal stability and the DNA double-stranded break connection. Nat. Rev. Genet. 2 (2001) 196-206
11. 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., Redon C., Ried T., Bonner W.M., Honjo T., Nussenzweig M.C., and Nussenzweig A. AID is required to initiate Nbs1/gamma-H2AX focus formation and mutations at sites of class switching. Nature 414 (2001) 660-665
12. 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
13. 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
14. 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
15. Keogh M.C., Kim J.A., Downey M., Fillingham J., Chowdhury D., Harrison J.C., Onishi M., Datta N., Galicia S., Emili A., Lieberman J., Shen X., Buratowski S., Haber J.E., Durocher D., Greenblatt J.F., and Krogan N.J. A phosphatase complex that dephosphorylates gammaH2AX regulates DNA damage checkpoint recovery. Nature (2005)
16. 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
17. Downs J.A., Allard S., Jobin-Robitaille O., Javaheri A., Auger A., Bouchard N., Kron S.J., Jackson S.P., and Cote J. Binding of chromatin-modifying activities to phosphorylated histone H2A at DNA damage sites. Mol. Cell 16 (2004) 979-990
18. van Attikum H., Fritsch O., Hohn B., and Gasser S.M. Recruitment of the INO80 complex by H2A phosphorylation links ATP-dependent chromatin remodeling with DNA double-strand break repair. Cell 119 (2004) 777-788
19. Morrison A.J., Highland J., Krogan N.J., Arbel-Eden A., Greenblatt J.F., Haber J.E., and Shen X. INO80 and gamma-H2AX interaction links ATP-dependent chromatin remodeling to DNA damage repair. Cell 119 (2004) 767-775
20. 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
21. Kobayashi J., Tauchi H., Sakamoto S., Nakamura A., Morishima K., Matsuura S., Kobayashi T., Tamai K., Tanimoto K., and Komatsu K. NBS1 localizes to gamma-H2AX foci through interaction with the FHA/BRCT domain. Curr. Biol. 12 (2002) 1846-1851
22. Ward I.M., Minn K., Jorda K.G., and Chen J. Accumulation of checkpoint protein 53BP1 at DNA breaks involves its binding to phosphorylated histone H2AX. J. Biol. Chem. 278 (2003) 19579-19582
23. Stewart G.S., Wang B., Bignell C.R., Taylor A.M.R., and Elledge S.J. MDC1 is a mediator of the mammalian DNA damage checkpoint. Nature 421 (2003) 961-966
24. Foster E.R., and Downs J.A. Histone H2A phosphorylation in DNA double-strand break repair. FEBS J. 272 (2005) 3231-3240
25. Durocher D., Smerdon S.J., Yaffe M.B., and Jackson S.P. The FHA domain in DNA repair and checkpoint signaling. Cold Spring Harb. Symp. Quant. Biol. 65 (2000) 423-431
26. Manke I.A., Lowery D.M., Nguyen A., and Yaffe M.B. BRCT repeats as phosphopeptide-binding modules involved in protein targeting. Science 302 (2003) 636-639
27. Yu X., Chini C.C., He M., Mer G., and Chen J. The BRCT domain is a phospho-protein binding domain. Science 302 (2003) 639-642
28. Clapperton J.A., Manke I.A., Lowery D.M., Ho T., Haire L.F., Yaffe M.B., and Smerdon S.J. Structure and mechanism of BRCA1 BRCT domain recognition of phosphorylated BACH1 with implications for cancer. Nat. Struct. Mol. Biol. 11 (2004) 512-518
29. Williams R.S., Lee M.S., Hau D.D., and Glover J.N. Structural basis of phosphopeptide recognition by the BRCT domain of BRCA1. Nat. Struct. Mol. Biol. 11 (2004) 519-525
30. Scully R., Chen J., Ochs R.L., Keegan K., Hoekstra M., Feunteun J., and Livingston D.M. Dynamic changes of BRCA1 subnuclear location and phosphorylation state are initiated by DNA damage. Cell 90 (1997) 425-435
31. Schultz L.B., Chehab N.H., Malikzay A., and Halazonetis T.D. p53 binding protein 1 (53BP1) is an early participant in the cellular response to DNA double-strand breaks. J. Cell Biol. 151 (2000) 1381-1390
32. Goldberg M., Stucki M., Falck J., D'Amours D., Rahman D., Pappin D., Bartek J., and Jackson S.P. MDC1 is required for the intra-S-phase DNA damage checkpoint. Nature 421 (2003) 952-956
33. Lou Z., Minter-Dykhouse K., Wu X., and Chen J. MDC1 is coupled to activated CHK2 in mammalian DNA damage response pathways. Nature 421 (2003) 957-961
34. Carney J.P., Maser R.S., Olivares H., Davis E.M., Le Beau M., Yates III J.R., Hays L., Morgan W.F., and Petrini J.H. The hMre11/hRad50 protein complex and Nijmegen breakage syndrome: linkage of double-strand break repair to the cellular DNA damage response. Cell 93 (1998) 477-486
35. Xu X., Lee J., and Stern D.F. Microcephalin is a DNA damage response protein involved in regulation of CHK1 and BRCA1. J. Biol. Chem. 279 (2004) 34091-34094
36. Jowsey P.A., Doherty A.J., and Rouse J. Human PTIP facilitates ATM-mediated activation of p53 and promotes cellular resistance to ionizing radiation. J. Biol. Chem. 279 (2004) 55562-55569
37. Yamane K., Wu X., and Chen J. A DNA damage-regulated BRCT-containing protein, TopBP1, is required for cell survival. Mol. Cell Biol. 22 (2002) 555-566
38. Rodriguez M., Yu X., Chen J., and Songyang Z. Phosphopeptide binding specificities of BRCA1 COOH-terminal (BRCT) domains. J. Biol. Chem. 278 (2003) 52914-52918
39. Lukas C., Melander F., Stucki M., Falck J., Bekker-Jensen S., Goldberg M., Lerenthal Y., Jackson S.P., Bartek J., and Lukas J. Mdc1 couples DNA double-strand break recognition by Nbs1 with its H2AX-dependent chromatin retention. EMBO J. 23 (2004) 2674-2683
40. Stucki M., Clapperton J.A., Mohammad D., Yaffe M.B., Smerdon S.J., and Jackson S.P. MDC1 directly binds phosphorylated histone H2AX to regulate cellular responses to DNA double-strand breaks. Cell 123 (2005) 1213-1226
41. Glover J.N., Williams R.S., and Lee M.S. Interactions between BRCT repeats and phosphoproteins: tangled up in two. Trends Biochem. Sci. 29 (2004) 579-585
42. Lee M.S., Edwards R.A., Thede G.L., and Glover J.N. Structure of the BRCT repeat domain of MDC1 and its specificity for the free COOH-terminal end of the gamma-H2AX histone tail. J. Biol. Chem. 280 (2005) 32053-32056 Epub 32005 Jul 32027
43. Botuyan M.V., Nomine Y., Yu X., Juranic N., Macura S., Chen J., and Mer G. Structural basis of BACH1 phosphopeptide recognition by BRCA1 tandem BRCT domains. Structure (Camb.) 12 (2004) 1137-1146
44. Shiozaki E.N., Gu L., Yan N., and Shi Y. Structure of the BRCT repeats of BRCA1 bound to a BACH1 phosphopeptide: implications for signaling. Mol. Cell 14 (2004) 405-412
45. 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., Alt F.W., and Chen J. MDC1 maintains genomic stability by participating in the amplification of ATM-dependent DNA damage signals. Mol. Cell 21 (2006) 187-200
46. Stucki M., and Jackson S.P. MDC1/NFBD1: a key regulator of the DNA damage response in higher eukaryotes. DNA Repair (Amst.) 3 (2004) 953-957
47. 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. (2003)
48. Bekker-Jensen S., Lukas C., Melander F., Bartek J., and Lukas J. 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
49. Iwabuchi K., Basu B.P., Kysela B., Kurihara T., Shibata M., Guan D., Cao Y., Hamada T., Imamura K., Jeggo P.A., Date T., and Doherty A.J. Potential role for 53BP1 in DNA end-joining repair through direct interaction with DNA. J. Biol. Chem. 278 (2003) 36487-36495
50. Huyen Y., Zgheib O., Ditullio Jr. R.A., Gorgoulis V.G., Zacharatos P., Petty T.J., Sheston E.A., Mellert H.S., Stavridi E.S., and Halazonetis T.D. Methylated lysine 79 of histone H3 targets 53BP1 to DNA double-strand breaks. Nature 432 (2004) 406-411
51. Falck J., Coates J., and Jackson S.P. Conserved modes of recruitment of ATM, ATR and DNA-PKcs to sites of DNA damage. Nature 434 (2005) 605-611
52. You Z., Chahwan C., Bailis J., Hunter T., and Russell P. ATM activation and its recruitment to damaged DNA require binding to the C terminus of Nbs1. Mol. Cell Biol. 25 (2005) 5363-5379
53. Ward I.M., and Chen J. Histone H2AX is phosphorylated in an ATR-dependent manner in response to replicational stress. J. Biol. Chem. 276 (2001) 47759-47762
54. Ward I.M., Minn K., and Chen J. UV-induced ataxia-telangiectasia-mutated and Rad3-related (ATR) activation requires replication stress. J. Biol. Chem. 279 (2004) 9677-9680
55. 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
56. 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., Carpenter P.B., Bonner W.M., Chen J., and Nussenzweig A. DNA damage-induced G2-M checkpoint activation by histone H2AX and 53BP1. Nat. Cell Biol. 4 (2002) 993-997
57. Wang H., Wang M., Bocker W., and Iliakis G. Complex H2AX phosphorylation patterns by multiple kinases including ATM and DNA-PK in human cells exposed to ionizing radiation and treated with kinase inhibitors. J. Cell Physiol. 202 (2005) 492-502
58. 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
59. Veuger S.J., Curtin N.J., Smith G.C., and Durkacz B.W. Effects of novel inhibitors of poly(ADP-ribose) polymerase-1 and the DNA-dependent protein kinase on enzyme activities and DNA repair. Oncogene 23 (2004) 7322-7329
60. 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
61. Lou Z., Chen B.P., Asaithamby A., Minter-Dykhouse K., Chen D.J., and Chen J. MDC1 regulates DNA-PK autophosphorylation in response to DNA damage. J. Biol. Chem. 279 (2004) 46359-46362
62. 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
63. 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
64. 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
65. 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., Lou Z., Bassing C.H., Manis J.P., Chen J., Carpenter P.B., and Alt F.W. H2AX prevents DNA breaks from progressing to chromosome breaks and translocations. Mol. Cell 21 (2006) 201-214
66. Murr R., Loizou J.I., Yang Y.G., Cuenin C., Li H., Wang Z.Q., and Herceg Z. Histone acetylation by Trrap-Tip60 modulates loading of repair proteins and repair of DNA double-strand breaks. Nat. Cell Biol. 8 (2006) 91-99
67. Strom L., Lindroos H.B., Shirahige K., and Sjogren C. Post-replicative recruitment of cohesin to double-strand breaks is required for DNA repair. Mol. Cell 16 (2004) 1003-1015
68. 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
69. Reaper P.M., di Fagagna F., and Jackson S.P. Activation of the DNA damage response by telomere attrition: a passage to cellular senescence. Cell Cycle 3 (2004) 543-546
70. Bartkova J., Horejsi Z., Koed K., Kramer A., Tort F., Zieger K., Guldberg P., Sehested M., Nesland J.M., Lukas C., Orntoft T., Lukas J., and Bartek J. DNA damage response as a candidate anti-cancer barrier in early human tumorigenesis. Nature 434 (2005) 864-870
71. Gorgoulis V.G., Vassiliou L.V., Karakaidos P., Zacharatos P., Kotsinas A., Liloglou T., Venere M., Ditullio Jr. R.A., Kastrinakis N.G., Levy B., Kletsas D., Yoneta A., Herlyn M., Kittas C., and Halazonetis T.D. Activation of the DNA damage checkpoint and genomic instability in human pre-cancerous lesions. Nature 434 (2005) 907-913