Histone H3 lysine 56 acetylation: A new twist in the chromosome cycle

Cell Cycle

Volumn 5, Issue 22, 2006, Pages 2602-2608

  Ozdemir, Anil ^a   Masumoto, Hiroshi ^b   Fitzjohn, Paul ^c   Verreault, Alain ^d   Logie, Colin ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b OSAKA UNIVERSITY   (Japan)

^c IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^d INSTITUTE FOR RESEARCH IN IMMUNOLOGY AND CANCER   (Canada)

Author keywords

Acetylation; Cell cycle; Chromatin; DNA damage; Histone; Nucleosome

Indexed keywords

HISTONE H3; LYSINE 56; LYSINE DERIVATIVE; NICOTINAMIDE ADENINE DINUCLEOTIDE; UNCLASSIFIED DRUG;

ACETYLATION; CELL CYCLE; CELL CYCLE S PHASE; CELL DIVISION; CELL SURVIVAL; CHROMATIN; DNA BINDING; DNA DAMAGE; GENE REPLICATION; GENOMIC INSTABILITY; PROTEIN EXPRESSION; REVIEW;

EID: 33751241119     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.5.22.3473     Document Type: Review

References (85)

1. Mersfelder EL, Parthun MR. The tale beyond the tail: Histone core domain modifications and the regulation of chromatin structure. Nucleic Acids Res 2006; 34:2653-62.
2. Zhang L, Eugeni EE, Parthun MR, Freitas MA. Identification of novel histone post-translational modifications by peptide mass fingerprinting. Chromosoma 2003; 112:77-86.
3. Hyland EM, Cosgrove MS, Molina H, Wang D, Pandey A, Cottee RJ, Boeke JD. Insights into the role of histone H3 and histone H4 core modifiable residues in Saccharomyces cerevisiae. Mol Cell Biol 2005; 25:10060-70.
4. Masumoto H, Hawke D, Kobayashi R, Verreault A. A role for cell-cycle-regulated histone H3 lysine 56 acetylation in the DNA damage response. Nature 2005; 436:294-8.
5. Ozdemir A, Spicuglia S, Lasonder E, Vermeulen M, Campsteijn C, Stunnenberg HG, Logie C. Characterization of lysine 56 of histone H3 as an acetylation site in Saccharomyces cerevisiae. J Biol Chem 2005; 280:25949-52.
6. Recht J, Tsubota T, Tanny JC, Diaz RL, Berger JM, Zhang X, Garcia BA, Shabanowitz J, Burlingame AL, Hunt DF, Kaufman PD, Allis CD. Histone chaperone Asf1 is required for histone H3 lysine 56 acetylation, a modification associated with S phase in mitosis and meiosis. Proc Natl Acad Sci USA 2006; 103:6988-93.
7. Xu F, Zhang K, Grunstein M. Acetylation in histone H3 globular domain regulates gene expression in yeast. Cell 2005; 121:375-85.
8. Zhou H, Madden BJ, Muddiman DC, Zhang Z. Chromatin assembly factor 1 interacts with histone H3 methylated at lysine 79 in the processes of epigenetic silencing and DNA repair. Biochemistry 2006; 45:2852-61.
9. Sipiczki M. Where does fission yeast sit on the tree of life? Genome Biol 2000; 1:1011.
10. Davey CA, Sargent DF, Luger K, Maeder AW, Richmond TJ. Solvent mediated interactions in the structure of the nucleosome core particle at 1.9Å resolution. J Mol Biol 2002; 319:1097-113.
11. Li G, Levitus M, Bustamante C, Widom J. Rapid spontaneous accessibility of nucleosomal DNA. Nat Struct Mol Biol 2005; 12:46-53.
12. Tomschik M, Zheng H, van Holde K, Zlatanova J, Leuba SH. Fast, long-range, reversible conformational fluctuations in nucleosomes revealed by single-pair fluorescence resonance energy transfer. Proc Natl Acad Sci USA 2005; 102:3278-83.
13. Adkins MW, Tyler JK. The histone chaperone Asf1p mediates global chromatin disassembly in vivo. J Biol Chem 2004; 279:52069-74.
14. Prado F, Cortes-Ledesma F, Aguilera A. The absence of the yeast chromatin assembly factor Asf1 increases genomic instability and sister chromatid exchange. EMBO Rep 2004; 5:497-502.
15. Maas NL, Miller KM, DeFazio LG, Toczyski DP. Cell cycle and checkpoint regulation of histone H3 K56 acetylation by Hst3 and Hst4. Mol Cell 2006; 23:109-19.
16. Koç A, Wheeler LJ, Mathews CK, Merrill GF. Hydroxyurea arrests DNA replication by a mechanism that preserves basal dNTP pools. J Biol Chem 2004; 279:223-30.
17. Petitjean A, Hilger F, Tatchell K. Comparison of thermosensitive alleles of the CDC25 gene involved in the cAMP metabolism of Saccharomyces cerevisiae. Genetics 1990; 124:797-806.
18. Sia RA, Herald HA, Lew DJ. Cdc28 tyrosine phosphorylation and the morphogenesis checkpoint in budding yeast. Mol Biol Cell 1996; 7:1657-66.
19. Celic I, Masumoto H, Griffith WP, Meluh P, Cotter RJ, Boeke JD, Verreault A. The sirtuins Hst3 and Hst4p preserve genome integrity by controlling histone H3 lysine 56 deacetylation. Curr Biol 2006; 16:1280-9.
20. Zhu G, Spellman PT, Volpe T, Brown PO, Botstein D, Davis TN, Futcher B. Two yeast forkhead genes regulate the cell cycle and pseudohyphal growth. Nature 2000; 406:90-4.
21. Sogo JM, Stahl H, Koller T, Knippers R. Structure of replicating simian virus 40 minichromosomes. The replication fork, core histone segregation and terminal structures. J Mol Biol 1986; 189:189-204.
22. Neuwald AF, Landsman D. Gcn5-related histone N-acetyltransferases belong to a diverse superfamily that includes the yeast Spt10 protein. Trends Biochem Sci 1997; 22:154-5.
23. Hess D, Liu B, Roan NR, Sternglanz R, Winston F. Spt10-dependent transcriptional activation in Saccharomyces cerevisiae requires both the Spt10 acetyltransferase domain and Spt21. Mol Cell Biol 2004; 24:135-43.
24. Eriksson PR, Mendiratta G, McLaughlin NB, Wolfsberg TG, Marino-Ramirez L, Pompa TA, Jainerin M, Landsman D, Shen CH, Clark DJ. Global regulation by the yeast Spt10 protein is mediated through chromatin structure and the histone upstream activating sequence elements. Mol Cell Biol 2005; 25:9127-37.
25. Mendiratta G, Eriksson PR, Shen CH, Clark DJ. The DNA-binding domain of the yeast Spt10p activator includes a zinc finger that is homologous to foamy virus integrase. J Biol Chem 2006; 281:7040-8.
26. Parthun MR, Widom J, Gottschling DE. The major cytoplasmic histone acetyltransferase in yeast: Links to chromatin replication and histone metabolism. Cell 1996; 87:85-94.
27. Sklenar AR, Parthun MR. Characterization of yeast histone H3-specific type B histone acetyltransferases identifies an Ada2-independent Gcn5p activity. BMC Biochem 2004; 5:11.
28. Brachmann CB, Sherman JM, Devine SE, Cameron EE, Pillus L, Boeke JD. The SIR2 gene family, conserved from bacteria to humans, functions in silencing, cell cycle progression, and chromosome stability. Genes Dev 1995; 9:2888-902.
29. Budd ME, Tong AH, Polaczek P, Peng X, Boone C, Campbell JL. A network of multi-tasking proteins at the DNA replication fork preserves genome stability. PLoS Genet 2005; 1: e61.
30. Pan X, Ye P, Yuan DS, Wang X, Bader JS, Boeke JD. A DNA integrity network in the yeast Saccharomyces cerevisiae. Cell 2006; 124:1069-81.
31. Tong AH, Lesage G, Bader GD, Ding H, Xu H, Xin X, Young J, Berriz GF, Brost RL, Chang M, Chen Y, Cheng X, Chua G, Friesen H, Goldberg DS, Haynes J, Humphries C, He G, Hussein S, Ke L, Krogan N, Li Z, Levinson JN, Lu H, Menard P, Munyana C, Parsons AB, Ryan O, Tonikian R, Roberts T, Sdicu AM, Shapiro J, Sheikh B, Suter B, Wong SL, Zhang LV, Zhu H, Burd CG, Munro S, Sander C, Rine J, Greenblatt J, Peter M, Bretscher A, Bell G, Roth FP, Brown GW, Andrews B, Bussey H, Boone C. Global mapping of the yeast genetic interaction network. Science 2004; 303:808-13.
32. Lewis LK, Storici F, Van Komen S, Calero S, Sung P, Resnick MA. Role of the nuclease activity of Saccharomyces cerevisiae Mre11 in repair of DNA double-strand breaks in mitotic cells. Genetics 2004; 166:1701-13.
33. Llorente B, Symington LS. The Mre11 nuclease is not required for 5′ to 3′ resection at multiple HO-induced double-strand breaks. Mol Cell Biol 2004; 24:9682-94.
34. Tyler JK, Adams CR, Chen SR, Kobayashi R, Kamakaka RT, Kadonaga JT. The RCAF complex mediates chromatin assembly during DNA replication and repair. Nature 1999; 402:555-60.
35. Franco AA, Lam WM, Burgers PM, Kaufman PD. Histone deposition protein Asf1 maintains DNA replisome integrity and interacts with replication factor C. Genes Dev 2005; 19:1365-75.
36. Green EM, Antczak AJ, Bailey AO, Franco AA, Wu KJ, Yates IIIrd JR, Kaufman PD. Replication-independent histone deposition by the HIR complex and Asf1. Curr Biol 2005; 15:2044-9.
37. Schermer UJ, Korber P, Hörz W. Histones are incorporated in trans during reassembly of the yeast PHO5 promoter. Mol Cell 2005; 19:279-85.
38. Tagami H, Ray-Gallet D, Almouzni G, Nakatani Y. Histone H3.1 and H3.3 complexes mediate nucleosome assembly pathways dependent or independent of DNA synthesis. Cell 2004; 116:51-61.
39. Tyler JK, Collins KA, Prasad-Sinha J, Amiott E, Bulger M, Harte PJ, Kobayashi R, Kadonaga JT. Interaction between the Drosophila CAF-1 and ASF1 chromatin assembly factors. Mol Cell Biol 2001; 21:6574-84.
40. Zabaronick SR, Tyler JK. The histone chaperone anti-silencing function 1 is a global regulator of transcription independent of passage through S phase. Mol Cell Biol 2005; 25:652-60.
41. Linger J, Tyler JK. The yeast histone chaperone chromatin assembly factor 1 protects against double-strand DNA-damaging agents. Genetics 2005; 171:1513-22.
42. Emili A, Schieltz DM, Yates IIIrd JR, Hartwell LH. Dynamic interaction of DNA damage checkpoint protein Rad53 with chromatin assembly factor Asf1. Mol Cell 2001; 7:13-20.
43. Hu F, Alcasabas AA, Elledge SJ. Asf1 links Rad53 to control of chromatin assembly. Genes Dev 2001; 15:1061-6.
44. Sweeney FD, Yang F, Chi A, Shabanowitz J, Hunt DF, Durocher D. Saccharomyces cerevisiae Rad9 acts as a Mec1 adaptor to allow Rad53 activation. Curr Biol 2005; 15:1364-75.
45. Meijsing SH, Ehrenhofer-Murray AE. The silencing complex SAS-I links histone acetylation to the assembly of repressed chromatin by CAF-1 and Asf1 in Saccharomyces cerevisiae. Genes Dev 2001; 15:3169-82.
46. Osada S, Sutton A, Muster N, Brown CE, Yates IIIrd JR, Sternglanz R, Workman JL. The yeast SAS (something about silencing) protein complex contains a MYST-type putative acetyltransferase and functions with chromatin assembly factor Asf1. Genes Dev 2001; 15:3155-68.
47. Mousson F, Lautrette A, Thuret JY, Agez M, Courbeyrette R, Amigues B, Becker E, Neumann JM, Guerois R, Mann C, Ochsenbein F. Structural basis for the interaction of Asf1 with histone H3 and its functional implications. Proc Natl Acad Sci USA 2005; 102:5975-80.
48. Sutton A, Shia WJ, Band D, Kaufman PD, Osada S, Workman JL, Sternglanz R. Sas4 and Sas5 are required for the histone acetyltransferase activity of Sas2 in the SAS complex. J Biol Chem 2003; 278:16887-92.
49. Symington LS. Role of RAD52 epistasis group genes in homologous recombination and double-strand break repair. Microbiol Mol Biol Rev 2002; 66:630-70.
50. Lewis LK, Karthikeyan G, Cassiano J, Resnick MA. Reduction of nucleosome assembly during new DNA synthesis impairs both major pathways of double-strand break repair. Nucleic Acids Res 2005; 33:4928-39.
51. Ramey CJ, Howar S, Adkins M, Linger J, Spicer J, Tyler JK. Activation of the DNA damage checkpoint in yeast lacking the histone chaperone anti-silencing function 1. Mol Cell Biol 2004; 24:10313-27.
52. Bird AW, Yu DY, Pray-Grant MG, Qiu Q, Harmon KE, Megee PC, Grant PA, Smith MM, Christman MF. Acetylation of histone H4 by Esa1 is required for DNA double-strand break repair. Nature 2002; 419:411-5.
53. Downs JA, Allard S, Jobin-Robitaille O, Javaheri A, Auger A, Bouchard N, Kron SJ, Jackson SP, Cote J. Binding of chromatin-modifying activities to phosphorylated histone H2A at DNA damage sites. Mol Cell 2004; 16:979-90.
54. Murr R, Loizou JI, Yang YG, Cuenin C, Li H, Wang ZQ, Herceg Z. Histone acetylation by Trrap-Tip60 modulates loading of repair proteins and repair of DNA double-strand breaks. Nat Cell Biol 2006; 8:91-9.
55. Qin S, Parthun MR. Recruitment of the type B histone acetyltransferase Hat1p to chromatin is linked to DNA double-strand breaks. Mol Cell Biol 2006; 26:3649-58.
56. Tamburini BA, Tyler JK. Localized histone acetylation and deacetylation triggered by the homologous recombination pathway of double-strand DNA repair. Mol Cell Biol 2005; 25:4903-13.
57. Qin S, Parthun MR. Histone H3 and the histone acetyltransferase Hat1p contribute to DNA double-strand break repair. Mol Cell Biol 2002; 22:8353-65.
58. Takahashi TS, Wigley DB, Walter JC. Pumps, paradoxes and ploughshares: Mechanism of the MCM2-7 DNA helicase. Trends Biochem Sci 2005; 30:437-44.
59. Byun TS, Pacek M, Yee MC, Walter JC, Cimprich KA. Functional uncoupling of MCM helicase and DNA polymerase activities activates the ATR-dependent checkpoint. Genes Dev 2005; 19:1040-52.
60. Branzei D, Foiani M. The Rad53 signal transduction pathway: Replication fork stabilization, DNA repair, and adaptation. Exp Cell Res 2006; 312:2654-9.
61. Lou Z, Minter-Dykhouse K, Franco S, Gostissa M, Rivera MA, Celeste A, Manis JP, van Deursen J, Nussenzweig A, Paull TT, Alt FW, Chen J. MDC1 maintains genomic stability by participating in the amplification of ATM-dependent DNA damage signals. Mol Cell 2006; 21:187-200.
62. Nakamura TM, Du LL, Redon C, Russell P. Histone H2A phosphorylation controls Crb2 recruitment at DNA breaks, maintains checkpoint arrest, and influences DNA repair in fission yeast. Mol Cell Biol 2004; 24:6215-30.
63. Rogakou EP, Pilch DR, Orr AH, Ivanova VS, Bonner WM. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem 1998; 273:5858-68.
64. Shroff R, Arbel-Eden A, Pilch D, Ira G, Bonner WM, Petrini JH, Haber JE, Lichten M. Distribution and dynamics of chromatin modification induced by a defined DNA double-strand break. Curr Biol 2004; 14:1703-11.
65. Stucki M, Clapperton JA, Mohammad D, Yaffe MB, Smerdon SJ, Jackson SP. MDC1 directly binds phosphorylated histone H2AX to regulate cellular responses to DNA double-strand breaks. Cell 2006; 123:1213-1226.
66. Boyer LA, Logie C, Bonte E, Becker PB, Wade PA, Wolffe AP, Wu C, Imbalzano AN, Peterson CL. Functional delineation of three groups of the ATP-dependent family of chromatin remodeling enzymes. J Biol Chem 2000; 275:18864-70.
67. Osborn AJ, Elledge SJ, Zou L. Checking on the fork: The DNA replication stress-response pathway. Trends Cell Biol 2002; 12:509-516.
68. Shogren-Knaak M, Ishii H, Sun JM, Pazin MJ, Davie JR, Peterson CL. Histone H4 K16 acetylation controls chromatin structure and protein interactions. Science 2006; 311:844-7.
69. De Piccoli G, Cortes-Ledesma F, Ira G, Torres-Rosell J, Uhle S, Farmer S, Hwang JY, Machin F, Ceschia A, McAleenan A, Cordon-Preciado V, Clemente-Blanco A, Vilella-Mitjana F, Ullal P, Jarmuz A, Leitao B, Bressan D, Dotiwala F, Papusha A, Zhao X, Myung K, Haber JE, Aguilera A, Aragon L. Smc5-Smc6 mediate DNA double-strand-break repair by promoting sister-chromatid recombination. Nat Cell Biol 2006; 8:1032-1034.
70. Pebernard S, Wohlschlegel J, McDonald WH, Yates IIIrd JR, Boddy MN. The Nse5-Nse6 dimer mediates DNA repair roles of the Smc5-Smc6 complex. Mol Cell Biol 2006; 26:1617-30.
71. Strom L, Lindroos HB, Shirahige K, Sjogren C. Postreplicative recruitment of cohesin to double-strand breaks is required for DNA repair. Mol Cell 2004; 16:1003-15.
72. Ali T, Coles P, Stevens TJ, Stott K, Thomas JO. Two homologous domains of similar structure but different stability in the yeast linker histone, Hho1p. J Mol Biol 2004; 338:139-48.
73. Thoma F, Koller T, Klug A. Involvement of histone H1 in the organization of the nucleosome and of the salt-dependent superstructures of chromatin. J Cell Biol 1979; 83:403-27.
74. Downs JA, Kosmidou E, Morgan A, Jackson SP. Suppression of homologous recombination by the Saccharomyces cerevisiae linker histone. Mol Cell 2003; 11:1685-92.
75. Anderson JD, Thastrom A, Widom J. Spontaneous access of proteins to buried nucleosomal DNA target sites occurs via a mechanism that is distinct from nucleosome translocation. Mol Cell Biol 2002; 22:7147-57.
76. Wu C, Travers A. A 'one-pot' assay for the accessibility of DNA in a nucleosome core particle. Nucleic Acids Res 2004; 32:e122.
77. Wurtele H, Verreault A. Histone post-translational modifications and the response to DNA double-strand breaks. Curr Opin Cell Biol 2006; 18:137-44.
78. Kolodner RD, Putnam CD, Myung K. Maintenance of genome stability in Saccharomyces cerevisiae. Science 2002; 297:552-7.
79. Hurley LH. DNA and its associated processes as targets for cancer therapy. Nat Rev Cancer 2002; 2:188-200.
80. Myung K, Pennaneach V, Kats ES, Kolodner RD. Saccharomyces cerevisiae chromatin assembly factors that act during DNA replication function in the maintenance of genome stability. Proc Natl Acad Sci USA 2003; 100:6640-5.
81. Schmidt KH, Wu J, Kolodner RD. Control of translocations between highly diverged genes by Sgs1, the Saccharomyces cerevisiae homolog of the Bloom's syndrome protein. Mol Cell Biol 2006; 26:5406-20.
82. Shibahara K, Stillman B. Replication-dependent marking of DNA by PCNA facilitates CAF-1-coupled inheritance of chromatin. Cell 1999; 96:575-85.
83. Fraga MF, Esteller M. Towards the human cancer epigenome. Cell Cycle 2005; 4:1377-81
84. Haase SB, Reed SI. Improved flow cytometric analysis of the budding yeast cell cycle. Cell Cycle 2002; 1:132-6.
85. English CM, Adkins CW, Carson JJ, Chruchill MEA, Tyler JK. Structural basis for the histone chaperone activity of Asf1. Cell 2006; 127:495-508.