Chromatin disassembly and reassembly during DNA repair

Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis

Volumn 618, Issue 1-2, 2007, Pages 52-64

  Linger, Jeffrey G ^a   Tyler, Jessica K ^a  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

ATP dependent remodelers; Chromatin assembly; Chromatin disassembly; Histone chaperone

Indexed keywords

CHAPERONE; DOUBLE STRANDED DNA; HISTONE;

ARTICLE; CELL SURVIVAL; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA DAMAGE; DNA REPAIR; EXCISION REPAIR; HUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION;

ADENOSINE TRIPHOSPHATE; ANIMALS; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA; DNA REPAIR; HISTONES; HUMANS; MODELS, BIOLOGICAL; MODELS, GENETIC; SACCHAROMYCES CEREVISIAE;

EUKARYOTA;

EID: 34147139806     PISSN: 00275107     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mrfmmm.2006.05.039     Document Type: Article

References (100)

1. Luger K., Mader A.W., Richmond R.K., Sargent D.F., and Richmond T.J. Crystal structure of the nucleosome core particle at 2.8 Å resolution. Nature 389 (1997) 251-260
2. Liu X., and Smerdon M.J. Nucleotide excision repair of the 5 S ribosomal RNA gene assembled into a nucleosome. J. Biol. Chem. 275 (2000) 23729-23735
3. Hara R., Mo J., and Sancar A. DNA damage in the nucleosome core is refractory to repair by human excision nuclease. Mol. Cell. Biol. 20 (2000) 9173-9181
4. Nilsen H., Lindahl T., and Verreault A. DNA base excision repair of uracil residues in reconstituted nucleosome core particles. EMBO J. 21 (2002) 5943-5952
5. Schieferstein U., and Thoma F. Site-specific repair of cyclobutane pyrimidine dimers in a positioned nucleosome by photolyase and T4 endonuclease V in vitro. EMBO J. 17 (1998) 306-316
6. Wang Z.G., Wu X.H., and Friedberg E.C. Nucleotide excision repair of DNA by human cell extracts is suppressed in reconstituted nucleosomes. J. Biol. Chem. 266 (1991) 22472-22478
7. Araki M., Masutani C., Maekawa T., Watanabe Y., Yamada A., Kusumoto R., Sakai D., Sugasawa K., Ohkuma Y., and Hanaoka F. Reconstitution of damage DNA excision reaction from SV40 minichromosomes with purified nucleotide excision repair proteins. Mutat. Res. 459 (2000) 147-160
8. Allen M.D., Buckle A.M., Cordell S.C., Lowe J., and Bycroft M. The crystal structure of AF1521 a protein from Archaeoglobus fulgidus with homology to the non-histone domain of macroH2A. J. Mol. Biol. 330 (2003) 503-511
9. Ura K., Araki M., Saeki H., Masutani C., Ito T., Iwai S., Mizukoshi T., Kaneda Y., and Hanaoka F. ATP-dependent chromatin remodeling facilitates nucleotide excision repair of UV-induced DNA lesions in synthetic dinucleosomes. EMBO J. 20 (2001) 2004-2014
10. Sogo J.M., Stahl H., Koller T., and Knippers R. Structure of replicating simian virus 40 minichromosomes. The replication fork, core histone segregation and terminal structures. J. Mol. Biol. 189 (1986) 189-204
11. Tyler J.K. Chromatin assembly. Cooperation between histone chaperones and ATP-dependent nucleosome remodeling machines. Eur. J. Biochem. 269 (2002) 2268-2274
12. Stillman B. Chromatin assembly during SV40 DNA replication in vitro. Cell 45 (1986) 555-565
13. Tyler J.K., Adams C.R., Chen S.R., Kobayashi R., Kamakaka R.T., and Kadonaga J.T. The RCAF complex mediates chromatin assembly during DNA replication and repair. Nature 402 (1999) 555-560
14. Smith S., and Stillman B. Purification and characterization of CAF-I, a human cell factor required for chromatin assembly during DNA replication in vitro. Cell 58 (1989) 15-25
15. Tyler J.K., Collins K.A., Prasad-Sinha J., Amiott E., Bulger M., Harte P.J., Kobayashi R., and Kadonaga J.T. Interaction between the Drosophila CAF-1 and ASF1 chromatin assembly factors. Mol. Biol. Cell 21 (2001) 6574-6584
16. Krawitz D.C., Kama T., and Kaufman P.D. Chromatin assembly factor I mutants defective for PCNA binding require Asf1/Hir proteins for silencing. Mol. Cell. Biol. 22 (2002) 614-625
17. Mello J.A., Sillje H.H., Roche D.M., Kirschner D.B., Nigg E.A., and Almouzni G. Human Asf1 and CAF-1 interact and synergize in a repair-coupled nucleosome assembly pathway. EMBO Rep. 3 (2002) 329-334
18. Shibahara K., and Stillman B. Replication-dependent marking of DNA by PCNA facilitates CAF-1-coupled inheritance of chromatin. Cell 96 (1999) 575-585
19. English C.M., Maluf N.K., Tripet B., Churchill M.E., and Tyler J.K. ASF1 binds to a heterodimer of histones H3 and H4: a two-step mechanism for the assembly of the H3-H4 heterotetramer on DNA. Biochemistry 44 (2005) 13673-13682
20. Tagami H., Ray-Gallet D., Almouzni G., and Nakatani Y. Histone H3.1 and H3.3 complexes mediate nucleosome assembly pathways dependent or independent of DNA synthesis. Cell 116 (2004) 51-61
21. Krude T. Chromatin assembly factor 1 (CAF-1) colocalizes with replication foci in HeLa cell nuclei. Exp. Cell Res. 220 (1995) 304-311
22. Schulz L.L., and Tyler J.K. The histone chaperone ASF1 localizes to active DNA replication forks to mediate efficient DNA replication. FASEB J. (2006)
23. Nabatiyan A., and Krude T. Silencing of chromatin assembly factor 1 in human cells leads to cell death and loss of chromatin assembly during DNA synthesis. Mol. Cell. Biol. 24 (2004) 2853-2862
24. Sanematsu F., Takami Y., Barman H.K., Fukagawa T., Ono T., Shibahara K.I., and Nakayama T. Asf1 is required for viability and chromatin assembly during DNA replication in vertebrate cells. J. Biol. Chem. (2006) 13817-13827
25. Adams C.R., and Kamakaka R.T. Chromatin assembly: biochemical identities and genetic redundancy. Curr. Opin. Genet. Dev. 9 (1999) 185-190
26. Formosa T. Changing the DNA landscape: putting a SPN on chromatin. Curr. Top. Microbiol. Immunol. 274 (2003) 171-201
27. Fyodorov D.V., and Kadonaga J.T. Dynamics of ATP-dependent chromatin assembly by ACF. Nature 418 (2002) 897-900
28. Ito T., Bulger M., Pazin M.J., Kobayashi R., and Kadonaga J.T. ACF, an ISWI-containing and ATP-utilizing chromatin assembly and remodeling factor. Cell 90 (1997) 145-155
29. Loyola A., LeRoy G., Wang Y.H., and Reinberg D. Reconstitution of recombinant chromatin establishes a requirement for histone-tail modifications during chromatin assembly and transcription. Genes Dev. 15 (2001) 2837-2851
30. Fyodorov D.V., Blower M.D., Karpen G.H., and Kadonaga J.T. Acf1 confers unique activities to ACF/CHRAC and promotes the formation rather than disruption of chromatin in vivo. Genes Dev. 18 (2004) 170-183
31. Lorch Y., Maier-Davis B., and Kornberg R.D. Chromatin remodeling by nucleosome disassembly in vitro. Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 3090-3093
32. Adkins M.W., Howar S.R., and Tyler J.K. Chromatin disassembly mediated by the histone chaperone Asf1 is essential for transcriptional activation of the yeast PHO5 and PHO8 genes. Mol. Cell. 14 (2004) 657-666
33. Belotserkovskaya R., Oh S., Bondarenko V.A., Orphanides G., Studitsky V.M., and Reinberg D. FACT facilitates transcription-dependent nucleosome alteration. Science 301 (2003) 1090-1093
34. Kaplan C.D., Laprade L., and Winston F. Transcription elongation factors repress transcription initiation from cryptic sites. Science 301 (2003) 1096-1099
35. Adkins M.W., and Tyler J.K. Transcriptional activators are dispensable for transcription in the absence of Spt6-mediated chromatin reassembly of promoter regions. Mol. Cell. 21 (2006) 405-416
36. Le S., Davis C., Konopka J.B., and Sternglanz R. Two new S-phase-specific genes from Saccharomyces cerevisiae. Yeast 13 (1997) 1029-1042
37. Qin S., and Parthun M.R. Histone H3 and the histone acetyltransferase Hat1p contribute to DNA double-strand break repair. Mol. Cell. Biol. 22 (2002) 8353-8365
38. Lewis L.K., Karthikeyan G., Cassiano J., and Resnick M.A. Reduction of nucleosome assembly during new DNA synthesis impairs both major pathways of double-strand break repair. Nucleic Acids Res. 33 (2005) 4928-4939
39. Kaufman P.D., Kobayashi R., and Stillman B. Ultraviolet radiation sensitivity and reduction of telomeric silencing in Saccharomyces cerevisiae cells lacking chromatin assembly factor-I. Genes Dev. 11 (1997) 345-357
40. Bennett C.B., Lewis L.K., Karthikeyan G., Lobachev K.S., Jin Y.H., Sterling J.F., Snipe J.R., and Resnick M.A. Genes required for ionizing radiation resistance in yeast. Nat. Genet. 29 (2001) 426-434
41. Linger J., and Tyler J.K. The yeast histone chaperone chromatin assembly factor 1 protects against double-strand DNA-damaging agents. Genetics 171 (2005) 1513-1522
42. Takeda S., Tadele Z., Hofmann I., Probst A.V., Angelis K.J., Kaya H., Araki T., Mengiste T., Scheid O.M., Shibahara K., Scheel D., and Paszkowski J. BRU1, a novel link between responses to DNA damage and epigenetic gene silencing in Arabidopsis. Genes Dev. 18 (2004) 782-793
43. Shen X., Mizuguchi G., Hamiche A., and Wu C. A chromatin remodelling complex involved in transcription and DNA processing. Nature 406 (2000) 541-544
44. Koyama H., Itoh M., Miyahara K., and Tsuchiya E. Abundance of the RSC nucleosome-remodeling complex is important for the cells to tolerate DNA damage in Saccharomyces cerevisiae. FEBS Lett. 531 (2002) 215-221
45. Chai B., Huang J., Cairns B.R., and Laurent B.C. Distinct roles for the RSC and Swi/Snf ATP-dependent chromatin remodelers in DNA double-strand break repair. Genes Dev. 19 (2005) 1656-1661
46. Klochendler-Yeivin A., Picarsky E., and Yaniv M. Increased DNA damage sensitivity and apoptosis in cells lacking the Snf5/Ini1 subunit of the SWI/SNF chromatin remodeling complex. Mol. Cell. Biol. 26 (2006) 2661-2674
47. Mizuguchi G., Shen X., Landry J., Wu W.H., Sen S., and Wu C. ATP-driven exchange of histone H2AZ variant catalyzed by SWR1 chromatin remodeling complex. Science (2003) 343-348
48. Smerdon M.J., and Lieberman M.W. Nucleosome rearrangement in human chromatin during UV-induced DNA-repair synthesis. Proc. Natl. Acad. Sci. U.S.A. 75 (1978) 4238-4241
49. Smerdon M.J. DNA repair and the role of chromatin structure. Curr. Opin. Cell Biol. 3 (1991) 422-428
50. Green C.M., and Almouzni G. Local action of the chromatin assembly factor CAF1 at sites of nucleotide excision repair in vivo. EMBO J. 22 (2003) 5163-5174
51. Gaillard P.H., Martini E.M., Kaufman P.D., Stillman B., Moustacchi E., and Almouzni G. Chromatin assembly coupled to DNA repair: a new role for chromatin assembly factor I. Cell 86 (1996) 887-896
52. Gaillard P.H., Moggs J.G., Roche D.M., Quivy J.P., Becker P.B., Wood R.D., and Almouzni G. Initiation and bidirectional propagation of chromatin assembly from a target site for nucleotide excision repair. EMBO J. 16 (1997) 6281-6289
53. Maga G., and Hubscher U. Proliferating cell nuclear antigen (PCNA): a dancer with many partners. J. Cell Sci. 116 (2003) 3051-3060
54. Moggs J.G., Grandi P., Quivy J.P., Jonsson Z.O., Hubscher U., Becker P.B., and Almouzni G. A CAF-1-PCNA-mediated chromatin assembly pathway triggered by sensing DNA damage. Mol. Cell. Biol. 20 (2000) 1206-1218
55. Martini E., Roche D.M., Marheineke K., Verreault A., and Almouzni G. Recruitment of phosphorylated chromatin assembly factor 1 to chromatin after UV irradiation of human cells. J. Cell Biol. 143 (1998) 563-575
56. Okano S., Lan L., Caldecott K.W., Mori T., and Yasui A. Spatial and temporal cellular responses to single-strand breaks in human cells. Mol. Cell. Biol. 23 (2003) 3974-3981
57. Hara R., and Sancar A. The SWI/SNF chromatin-remodeling factor stimulates repair by human excision nuclease in the mononucleosome core particle. Mol. Cell. Biol. 22 (2002) 6779-6787
58. Huggins C.F., Chafin D.R., Aoyagi S., Henricksen L.A., Bambara R.A., and Hayes J.J. Flap endonuclease 1 efficiently cleaves base excision repair and DNA replication intermediates assembled into nucleosomes. Mol. Cell. 10 (2002) 1201-1211
59. Chafin D.R., Vitolo J.M., Henricksen L.A., Bambara R.A., and Hayes J.J. Human DNA ligase I efficiently seals nicks in nucleosomes. EMBO J. 19 (2000) 5492-5501
60. Beard B.C., Wilson S.H., and Smerdon M.J. Suppressed catalytic activity of base excision repair enzymes on rotationally positioned uracil in nucleosomes. Proc. Natl. Acad. Sci. U.S.A. 100 (2003) 7465-7470
61. Nabatiyan A., Szuts D., and Krude T. Induction of CAF-1 expression in response to DNA strand breaks in quiescent human cells. Mol. Cell. Biol. 26 (2006) 1839-1849
62. Wyman C., Ristic D., and Kanaar R. Homologous recombination-mediated double-strand break repair. DNA Rep. (Amst.) 3 (2004) 827-833
63. Aylon Y., and Kupiec M. DSB repair: the yeast paradigm. DNA Rep. (Amst.) 3 (2004) 797-815
64. Ivanov E.L., Sugawara N., White C.I., Fabre F., and Haber J.E. Mutations in XRS2 and RAD50 delay but do not prevent mating-type switching in Saccharomyces cerevisiae. Mol. Cell. Biol. 14 (1994) 3414-3425
65. Sugawara N., and Haber J.E. Characterization of double-strand break-induced recombination: homology requirements and single-stranded DNA formation. Mol. Cell. Biol. 12 (1992) 563-575
66. Dudasova Z., Dudas A., and Chovanec M. Non-homologous end-joining factors of Saccharomyces cerevisiae. FEMS Microbiol. Rev. 28 (2004) 581-601
67. Jiao R., Bachrati C.Z., Pedrazzi G., Kuster P., Petkovic M., Li J.L., Egli D., Hickson I.D., and Stagljar I. Physical and functional interaction between the Bloom's syndrome gene product and the largest subunit of chromatin assembly factor 1. Mol. Cell. Biol. 24 (2004) 4710-4719
68. Balajee A.S., and Geard C.R. Chromatin-bound PCNA complex formation triggered by DNA damage occurs independent of the ATM gene product in human cells. Nucleic Acids Res. 29 (2001) 1341-1351
69. Holmes A.M., and Haber J.E. Double-strand break repair in yeast requires both leading and lagging strand DNA polymerases. Cell 96 (1999) 415-424
70. Pospiech H., Rytkonen A.K., and Syvaoja J.E. The role of DNA polymerase activity in human non-homologous end joining. Nucleic Acids Res. 29 (2001) 3277-3288
71. Adkins M.W., and Tyler J.K. The histone chaperone Asf1p mediates global chromatin disassembly in vivo. J. Biol. Chem. 279 (2004) 52069-52074
72. Giavara S., Kosmidou E., Hande M.P., Bianchi M.E., Morgan A., d'Adda di Fagagna F., and Jackson S.P. Yeast Nhp6A/B and mammalian Hmgb1 facilitate the maintenance of genome stability. Curr. Biol. 15 (2005) 68-72
73. Qin S., and Parthun M.R. Recruitment of the type B histone acetyltransferase hat1p to chromatin is linked to DNA double-strand breaks. Mol. Cell. Biol. 26 (2006) 3649-3658
74. Ai X., and Parthun M.R. The nuclear Hat1p/Hat2p complex: a molecular link between type B histone acetyltransferases and chromatin assembly. Mol. Cell. 14 (2004) 195-205
75. Tsukuda T., Fleming A.B., Nickoloff J.A., and Osley M.A. Chromatin remodelling at a DNA double-strand break site in Saccharomyces cerevisiae. Nature 438 (2005) 379-383
76. Haber J.E. Mating-type gene switching in Saccharomyces cerevisiae. Annu. Rev. Genet. 32 (1998) 561-599
77. Lee S.E., Moore J.K., Holmes A., Umezu K., Kolodner R.D., and Haber J.E. Saccharomyces Ku70, mre11/rad50 and RPA proteins regulate adaptation to G2/M arrest after DNA damage. Cell 94 (1998) 399-409
78. 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
79. Qin J., and Li L. Molecular anatomy of the DNA damage and replication checkpoints. Radiat. Res. 159 (2003) 139-148
80. Melo J., and Toczyski D. A unified view of the DNA-damage checkpoint. Curr. Opin. Cell Biol. 14 (2002) 237-245
81. Gilbert C.S., Green C.M., and Lowndes N.F. Budding yeast Rad9 is an ATP-dependent Rad53 activating machine. Mol. Cell. 8 (2001) 129-136
82. Pasero P., Shimada K., and Duncker B.P. Multiple roles of replication forks in S phase checkpoints: sensors, effectors and targets. Cell Cycle 2 (2003) 568-572
83. 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
84. 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
85. 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)
86. Hu F., Alcasabas A.A., and Elledge S.J. Asf1 links Rad53 to control of chromatin assembly. Genes Dev. 15 (2001) 1061-1066
87. Emili A., Schieltz D.M., Yates III J.R., and Hartwell L.H. Dynamic interaction of DNA damage checkpoint protein Rad53 with chromatin assembly factor Asf1. Mol. Cell. 7 (2001) 13-20
88. Schwartz M.F., Lee S.J., Duong J.K., Eminaga S., and Stern D.F. FHA domain-mediated DNA checkpoint regulation of Rad53. Cell Cycle 2 (2003) 384-396
89. Sillje H.H., and Nigg E.A. Identification of human Asf1 chromatin assembly factors as substrates of Tousled-like kinases. Curr. Biol. 11 (2001) 1068-1073
90. Tamburini B.A., Carson J.J., Adkins M.W., and Tyler J.K. Functional conservation and specialization among eukaryotic anti-silencing function 1 histone chaperones. Eukaryot. Cell 4 (2005) 1583-1590
91. Carrera P., Moshkin Y.M., Gronke S., Sillje H.H., Nigg E.A., Jackle H., and Karch F. Tousled-like kinase functions with the chromatin assembly pathway regulating nuclear divisions. Genes Dev. 17 (2003) 2578-2590
92. Groth A., Lukas J., Nigg E.A., Sillje H.H., Wernstedt C., Bartek J., and Hansen K. Human Tousled like kinases are targeted by an ATM- and Chk1-dependent DNA damage checkpoint. EMBO J. 22 (2003) 1676-1687
93. Sunavala-Dossabhoy G., Balakrishnan S.K., Sen S., Nuthalapaty S., and De Benedetti A. The radioresistance kinase TLK1B protects the cells by promoting repair of double strand breaks. BMC Mol. Biol. 6 (2005) 19
94. Ramey C.J., Howar S., Adkins M., Linger J., Spicer J., and Tyler J.K. Activation of the DNA damage checkpoint in yeast lacking the histone chaperone anti-silencing function 1. Mol. Cell. Biol. 24 (2004) 10313-10327
95. Bakkenist C.J., and Kastan M.B. DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 421 (2003) 499-506
96. Ye X., Franco A.A., Santos H., Nelson D.M., Kaufman P.D., and 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
97. Prado F., Cortes-Ledesma F., and Aguilera A. The absence of the yeast chromatin assembly factor Asf1 increases genomic instability and sister chromatid exchange. EMBO Rep. 5 (2004) 497-502
98. Myung K., Pennaneach V., Kats E.S., and Kolodner R.D. Saccharomyces cerevisiae chromatin-assembly factors that act during DNA replication function in the maintenance of genome stability. Proc. Natl. Acad. Sci. U.S.A. 100 (2003) 6640-6645
99. 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
100. Doyon Y., and Cote J. The highly conserved and multifunctional NuA4 HAT complex. Curr. Opin. Genet. Dev. 14 (2004) 147-154