Interplay between chromatin and cell cycle checkpoints in the context of ATR/ATM-dependent checkpoints

DNA Repair

Volumn 3, Issue 8-9, 2004, Pages 969-978

  Koundrioukoff, Stephane ^a   Polo, Sophie ^a   Almouzni, Genevieve ^a  

^a INSTITUT CURIE   (France)

Author keywords

ATM ATR dependent checkpoints; Chromatin; Chromatin assembly; DNA repair; Histone modifications

Indexed keywords

DNA;

CELL CYCLE; CHROMATIN; DNA REPAIR; DROSOPHILA MELANOGASTER; GENE EXPRESSION; GENE TARGETING; GENOME; GENOTOXICITY; NONHUMAN; PRIORITY JOURNAL; REVIEW; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION;

ANIMALS; APOPTOSIS; CELL CYCLE; CELL CYCLE PROTEINS; CHROMATIN; DNA REPAIR; DNA-BINDING PROTEINS; FUNGAL PROTEINS; GENOME; HISTONES; HUMANS; MODELS, BIOLOGICAL; PHOSPHORYLATION; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN-SERINE-THREONINE KINASES; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEINS;

EID: 3242889155     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2004.03.010     Document Type: Review

References (80)

1. Kornberg R.D. Structure of chromatin. Annu. Rev. Biochem. 46:1977;931-954
2. Kornberg R.D., Lorch Y. Twenty-five years of the nucleosome, fundamental particle of the eukaryote chromosome. Cell. 98:1999;285-294
3. Luger K., Mader A.W., Richmond R.K., Sargent D.F., Richmond T.J. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature. 389:1997;251-260
4. Turner B.M. Histone acetylation and an epigenetic code. Bioessays. 22:2000;836-845
5. Jenuwein T. CD Allis Translating the histone code. Science. 293:2001;1074-1080
6. Mello J.A., Almouzni G. The ins and outs of nucleosome assembly. Curr. Opin. Genet. Dev. 11:2001;136-141
7. Loyola A., Almouzni G. Histone chaperones, a supporting role in the limelight. Biochim. Biophys. Acta. 1677:2004;3-11
8. Hartwell L.H., Weinert T.A. Checkpoints: controls that ensure the order of cell cycle events. Science. 246:1989;629-634
9. Foiani M., Pellicioli A., Lopes M., Lucca C., Ferrari M., Liberi G., Muzi Falconi M., Plevani P. DNA damage checkpoints and DNA replication controls in Saccharomyces cerevisiae. Mutat. Res. 451:2000;187-196
10. Zhou B.B., Elledge S.J. The DNA damage response: putting checkpoints in perspective. Nature. 408:2000;433-439
11. Bartek J., Lukas J. Mammalian Gl- and S-phase checkpoints in response to DNA damage. Curr. Opin. Cell Biol. 13:2001;738-747
12. Abraham R.T. Cell cycle checkpoint signaling through the ATM and ATR kinases. Genes Dev. 15:2001;2177-2196
13. Shiloh Y. ATM and related protein kinases: safeguarding genome integrity. Nat. Rev. Cancer. 3:2003;155-168
14. Kastan M.B., Lim D.S. The many substrates and functions of ATM. Nat. Rev. Mol. Cell. Biol. 1:2000;179-186
15. Osley M.A. The regulation of histone synthesis in the cell cycle. Annu. Rev. Biochem. 60:1991;827-861
16. Qin S., Parthun M.R. Histone H3 and the histone acetyltransferase Hatlp contribute to DNA double-strand break repair. Mol. Cell Biol. 22:2002;8353-8365
17. Megee P.C., Morgan B.A., Smith M.M. Histone H4 and the maintenance of genome integrity. Genes Dev. 9:1995;1716-1727
18. Clarke A.S., Lowell J.E., Jacobson S.J., Pillus L. Esalp is an essential histone acetyltransferase required for cell cycle progression. Mol. Cell Biol. 19:1999;2515-2526
19. Briggs S.D., Bryk M., Strahl B.D., Cheung W.L., Davie J.K., Dent S.Y., Winston F., Allis C.D. Histone H3 lysine 4 methylation is mediated by Setl and required for cell growth and rDNA silencing in Saccharomyces cerevisiae. Genes Dev. 15:2001;3286-3295
20. Kanoh J., Francesconi S., Collura A., Schramke V., Ishikawa F., Baldacci G., Geli V. The fission yeast spSetlp is a histone H3-K4 methyltransferase that functions in telomere maintenance and DNA repair in an ATM kinase Rad3-dependent pathway. J. Mol. Biol. 326:2003;1081-1094
21. Nislow C., Ray E., Pillus L. SET1, a yeast member of the trithorax family, functions in transcriptional silencing and diverse cellular processes. Mol. Biol. Cell. 8:1997;2421-2436
22. Schramke V., Neecke H., Brevet V., Corda Y., Lucchini G., Longhese M.P., Gilson E., Geli V. The setlDelta mutation unveils a novel signaling pathway relayed by the Rad53-dependent hyperphosphorylation of replication protein A that leads to transcriptional activation of repair genes. Genes Dev. 15:2001;1845-1858
23. Gunjan A., Verreault A. A Rad53 kinase-dependent surveillance mechanism that regulates histone protein levels in S. cerevisiae. Cell. 115:2003;537-549
24. Ray-Gallet D., Quivy J.P., Scamps C., Martini E.M., Lipinski M., Almouzni G. HIRA is critical for a nucleosome assembly pathway independent of DNA synthesis. Mol. Cell. 9:2002;1091-1100
25. Spector M.S., Raff A., DeSilva H., Lee K., Osley M.A. Hirlp and Hir2p function as transcriptional corepressors to regulate histone gene transcription in the Saccharomyces cerevisiae cell cycle. Mol. Cell Biol. 17:1997;545-552
26. Ye X., Franco A.A., Santos H., Nelson D.M., Kaufman P.D., Adams P.D. Defective S phase chromatin assembly causes DNA damage, activation of the S phase checkpoint, and S phase arrest. Mol. Cell. 11:2003;341-351
27. Nelson D.M., Ye X., Hall C., Santos H., Ma T., Kao G.D., Yen T.J., Harper J.W., Adams P.D. Coupling of DNA synthesis and histone synthesis in S phase independent of cyclin/cdk2 activity. Mol. Cell Biol. 22:2002;7459-7472
28. Stillman B. Chromatin assembly during SV40 DNA replication in vitro. Cell. 45:1986;555-565
29. Gaillard P.H., Martini E.M., Kaufman P.D., Stillman B., Moustacchi E., Almouzni G. Chromatin assembly coupled to DNA repair: a new role for chromatin assembly factor I. Cell. 86:1996;887-896
30. Shibahara K., Stillman B. Replication-dependent marking of DNA by PCNA facilitates CAF-1-coupled inheritance of chromatin. Cell. 96:1999;575-585
31. Moggs J.G., Grandi P., Quivy J.P., Jonsson Z.O., Hubscher U., Becker P.B., Almouzni G. A CAF-1-PCNA-mediated chromatin assembly pathway triggered by sensing DNA damage. Mol. Cell Biol. 20:2000;1206-1218
32. Venclovas C., Thelen M.P. Structure-based predictions of Radl, Rad9 Husl and Radl7, participation in sliding clamp and clamp-loading complexes. Nucl. Acids Res. 28:2000;2481-2493
33. Burtelow M.A., Roos-Mattjus P.M., Rauen M., Babendure J.R., Karnitz L.M. Reconstitution and molecular analysis of the hRad9-hHusl-hRadl (9-1-1) DNA damage responsive checkpoint complex. J. Biol. Chem. 276:2001;25903-25909
34. Zou L., Cortez D., Elledge S.J. Regulation of ATR substrate selection by Radl7-dependent loading of Rad9 complexes onto chromatin. Genes Dev. 16:2002;198-208
35. Hoek M., Stillman B. Chromatin assembly factor 1 is essential and couples chromatin assembly to DNA replication in vivo. Proc. Natl. Acad. Sci. USA. 30:2003;30
36. Myung K., Pennaneach V., Kats E.S., Kolodner R.D. Saccharomyces cerevisiae chromatin-assembly factors that act during DNA replication function in the maintenance of genome stability. Proc. Natl. Acad. Sci. USA. 100:2003;6640-6645
37. Tyler J.K., Adams C.R., Chen S.R., Kobayashi R., Kamakaka R.T., Kadonaga J.T. The RCAF complex mediates chromatin assembly during DNA replication and repair. Nature. 402:1999;555-560
38. Mello J.A., Sillje H.H., Roche D.M., Kirschner D.B., Nigg E.A., Almouzni G. Human Asfl and CAF-1 interact and synergize in a repair-coupled nucleosome assembly pathway. EMBO Rep. 3:2002;329-334
39. Umehara T., Chimura T., Ichikawa N., Horikoshi M. Polyanionic stretch-deleted histone chaperone cial/Asf lp is functional both in vivo and in vitro. Genes Cells. 7:2002;59-73
40. Bird A.W., Yu D.Y., Pray-Grant M.G., Qiu Q., Harmon K.E., Megee P.C., Grant P.A., Smith M.M., Christman M.F. Acetylation of histone H4 by Esal is required for DNA double-strand break repair. Nature. 419:2002;411-415
41. Bakkenist C.J., Kastan M.B. DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature. 421:2003;499-506
42. Green C.M., Almouzni G. When repair meets chromatin. First in series on chromatin dynamics. EMBO Rep. 3:2002;28-33
43. Downs J.A., Lowndes N.F., Jackson S.P. A role for Saccharomyces cerevisiae histone H2A in DNA repair. Nature. 408:2000;1001-1004
44. Madigan J.P., Chotkowski H.L., Glaser R.L. DNA double-strand break-induced phosphorylation of Drosophila histone variant H2Av helps prevent radiation-induced apoptosis. Nucl. Acids Res. 30:2002;3698-3705
45. 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. 273:1998;5858-5868
46. 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., Alt F.W. Increased ionizing radiation sensitivity and genomic instability in the absence of histone H2AX. Proc. Natl. Acad. Sci. USA. 99:2002;8173-8178
47. 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., Nussenzweig A. Genomic instability in mice lacking histone H2AX. Science. 296:2002;922-927
48. Bassing C.H., Suh H., Ferguson D.O., Chua K.F., Manis J., Eckersdorff M., Gleason M., Bronson R., Lee C., Alt F.W. Histone H2AX: a dosage-dependent suppressor of oncogenic translocations and tumors. Cell. 114:2003;359-370
49. Celeste A., Difilippantonio S., Difilippantonio M.J., Fernandez-Capetillo O., Pilch D.R., Sedelnikova O.A., Eckhaus M., Ried T., Bonner W.M., Nussenzweig A. H2AX haploinsufficiency modifies genomic stability and tumor susceptibility. Cell. 114:2003;371-383
50. Redon C., Pilch D., Rogakou E., Sedelnikova O., Newrock K., Bonner W. Histone H2A variants H2AX and H2AZ. Curr. Opin. Genet. Dev. 12:2002;162-169
51. Rogakou E.P., Boon C., Redon C., Bonner W.M. Megabase chromatin domains involved in DNA double-strand breaks in vivo. J. Cell Biol. 146:1999;905-916
52. 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. 10:2000;886-895
53. Celeste A., Fernandez-Capetillo O., Kruhlak M.J., Pilch D.R., Staudt D.W., Lee A., Bonner R.F., Bonner W.M., Nussenzweig A. Histone H2AX phosphorylation is dispensable for the initial recognition of DNA breaks. Nat. Cell Biol. 5:2003;675-679
54. Burma S., Chen B.P., Murphy M., Kurimasa A., Chen D.J. ATM phosphorylates histone H2AX in response to DNA double-strand breaks. J. Biol. Chem. 276:2001;42462-42467
55. Ward I.M., Chen J. Histone H2AX is phosphorylated in an ATR-dependent manner in response to replicational stress. J. Biol. Chem. 276:2001;47759-47762
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., Nussenzweig A. DNA damage-induced G2-M checkpoint activation by histone H2AX and 53BP1. Nat. Cell Biol. 4:2002;993-997
57. Shen X., Mizuguchi G., Hamiche A., Wu C. A chromatin remodelling complex involved in transcription and DNA processing. Nature. 406:2000;541-544
58. Elledge R.M., Lee W.H. Life and death by p53. Bioessays. 17:1995;923-930
59. Avantaggiati M.L., Ogryzko V., Gardner K., Giordano A., Levine A.S., Kelly K. Recruitment of p300/CBP in p53-dependent signal pathways. Cell. 89:1997;1175-1184
60. Lill N.L., Grossman S.R., Ginsberg D., DeCaprio J., Livingston D.M. Binding and modulation of p53 by p300/CBP coactivators. Nature. 387:1997;823-827
61. Rubbi C.P., Milner J. p53 is a chromatin accessibility factor for nucleotide excision repair of DNA damage. Embo. J. 22:2003;975-986
62. Mills K.D., Sinclair D.A., Guarente L. MEC1-dependent redistribution of the Sir3 silencing protein from telomeres to DNA double-strand breaks. Cell. 97:1999;609-620
63. Martin S.G., Laroche T., Suka N., Grunstein M., Gasser S.M. Relocalization of telomeric Ku and SIR proteins in response to DNA strand breaks in yeast. Cell. 97:1999;621-633
64. Longhese M.P., Paciotti V., Neecke H., Lucchini G. Checkpoint proteins influence telomeric silencing and length maintenance in budding yeast. Genetics. 155:2000;1577-1591
65. Green C.M., Almouzni G. Local action of the chromatin assembly factor CAF-1 at sites of nucleotide excision repair in vivo. Embo. J. 22:2003;5163-5174
66. Krawitz D.C., Kama T., Kaufman P.D. Chromatin assembly factor I mutants defective for PCNA binding require Asf 1/Hir proteins for silencing. Mol. Cell Biol. 22:2002;614-625
67. Sharp J.A., Fouts E.T., Krawitz D.C., Kaufman P.D. Yeast histone deposition protein Asflp requires Hir proteins and PCNA for heterochromatic silencing. Curr. Biol. 11:2001;463-473
68. Emili A., Schieltz D.M., Yates J.R. 3rd, Hartwell L.H. Dynamic interaction of DNA damage checkpoint protein Rad53 with chromatin assembly factor Asfl. Mol. Cell. 7:2001;13-20
69. Hu F., Alcasabas A.A., Elledge S.J. Asfl links Rad53 to control of chromatin assembly. Genes Dev. 15:2001;1061-1066
70. Lee S.J., Schwartz M.F., Duong J.K., Stern D.F. Rad53 phosphorylation site clusters are important for Rad53 regulation and signaling. Mol. Cell Biol. 23:2003;6300-6314
71. Sillje H.H., Nigg E.A. Identification of human Asfl chromatin assembly factors as substrates of Tousled-like kinases. Curr. Biol. 11:2001;1068-1073
72. Groth A., Lukas J., Nigg E.A., Sillje H.H., Wernstedt C., Bartek J., Hansen K. Human Tousled like kinases are targeted by an ATM- and Chkl-dependent DNA damage checkpoint. Embo. J. 22:2003;1676-1687
73. Krause D.R., Jonnalagadda J.C., Gatei M.H., Sillje H.H., Zhou B.B., Nigg E.A., Khanna K. Suppression of Tousled-like kinase activity after DNA damage or replication block requires ATM, NBS1 and Chkl. Oncogene. 22:2003;5927-5937
74. Daganzo S.M., Erzberger J.P., Lam W.M., Skordalakes E., Zhang R., Franco A.A., Brill S.J., Adams P.D., Berger J.M., Kaufman P.D. Structure and function of the conserved core of histone deposition protein Asfl. Curr. Biol. 13:2003;2148-2158
75. Moshkin Y.M., Armstrong J.A., Maeda R.K., Tamkun J.W., Verrijzer P., Kennison J.A., Karch F. Histone chaperone ASF1 cooperates with the Brahma chromatin-remodelling machinery. Genes Dev. 16:2002;2621-2626
76. Osada S., Sutton A., Muster N., Brown C.E., Yates J.R. 3rd, Sternglanz R., Workman J.L. The yeast SAS (something about silencing) protein complex contains a MYST-type putative acetyltransferase and functions with chromatin assembly factor ASF1. Genes Dev. 15:2001;3155-3168
77. Chimura T., Kuzuhara T., Horikoshi M. Identification and characterization of CIA/ASF1 as an interactor of bromodomains associated with TFIID. Proc. Natl. Acad. Sci. USA. 99:2002;9334-9339
78. Shin H.J., Baek K.H., Jeon A.H., Kim S.J., Jang K.L., Sung Y.C., Kim C.M., Lee C.W. Inhibition of histone deacetylase activity increases chromosomal instability by the aberrant regulation of mitotic checkpoint activation. Oncogene. 22:2003;3853-3858
79. Krude T. Chromatin assembly: the kinetochore connection. Curr. Biol. 12:2002;R256-258
80. San-Segundo P.A., Roeder G.S. Pch2 links chromatin silencing to meiotic checkpoint control. Cell. 97:1999;313-324