Histone H3 Serine 57 and Lysine 56 Interplay in Transcription Elongation and Recovery from S-Phase Stress

PLoS ONE

Volumn 5, Issue 5, 2010, Pages

  Aslam, Aamir ^a   Logie, Colin ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE H3; LYSINE; SERINE; HISTONE; MESYLIC ACID METHYL ESTER;

ACETYLATION; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; CELL CYCLE ARREST; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL CYCLE S PHASE; CELL PROLIFERATION; CELL STRESS; CONTROLLED STUDY; DNA DAMAGE; GENE MUTATION; NONHUMAN; PHENOTYPE; POINT MUTATION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN QUATERNARY STRUCTURE; TRANSCRIPTION REGULATION; CELL CLONE; CHEMISTRY; CYTOLOGY; DOMINANT GENE; DRUG EFFECT; GENE REPRESSION; GENETIC TRANSCRIPTION; GENETICS; HELA CELL; HUMAN; METABOLISM; MITOSIS; MUTATION; PHOSPHORYLATION; PHYSIOLOGICAL STRESS; SACCHAROMYCES CEREVISIAE;

EUKARYOTA;

AMINO ACID SUBSTITUTION; CLONE CELLS; DNA DAMAGE; G2 PHASE; GENES, DOMINANT; HELA CELLS; HISTONES; HUMANS; LYSINE; METHYL METHANESULFONATE; MITOSIS; MUTATION; PHOSPHORYLATION; S PHASE; SACCHAROMYCES CEREVISIAE; SERINE; STRESS, PHYSIOLOGICAL; SUPPRESSION, GENETIC; TRANSCRIPTION, GENETIC;

EID: 77956275748     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0010851     Document Type: Article

References (54)

1. Luger K, Mader AW, Richmond RK, Sargent DF, Richmond TJ (1997) Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389: 251-260.
2. White CL, Suto RK, Luger K (2001) Structure of the yeast nucleosome core particle reveals fundamental changes in internucleosome interactions. Embo J 20: 5207-5218.
3. Ozdemir A, Spicuglia S, Lasonder E, Vermeulen M, Campsteijn C, et al. (2005) Characterization of lysine 56 of histone H3 as an acetylation site in Saccharomyces cerevisiae. J Biol Chem 280: 25949-25952.
4. Masumoto H, Hawke D, Kobayashi R, Verreault A (2005) A role for cell-cycle-regulated histone H3 lysine 56 acetylation in the DNA damage response. Nature 436: 294-298.
5. Hyland EM, Cosgrove MS, Molina H, Wang D, Pandey A, et al. (2005) Insights into the role of histone H3 and histone H4 core modifiable residues in Saccharomyces cerevisiae. Mol Cell Biol 25: 10060-10070.
6. Kaplan T, Liu CL, Erkmann JA, Holik J, Grunstein M, et al. (2008) Cell cycle-and chaperone-mediated regulation of H3K56ac incorporation in yeast. PLoS Genet 4: e1000270.
7. Xie W, Song C, Young NL, Sperling AS, Xu F, et al. (2009) Histone h3 lysine 56 acetylation is linked to the core transcriptional network in human embryonic stem cells. Mol Cell 33: 417-427.
8. Värv S, Kristjuhan K, Peil K, Lõoke M, Mahlakõiv T, et al. (2010) Acetylation of H3 K56 is Required for RNA Polymerase II Transcript Elongation through Heterochromatin in Yeast. Mol Cell Biol doi:10.1128/MCB.01151-09.
9. Lin C, Yuan YA (2008) Structural insights into histone H3 lysine 56 acetylation by Rtt109. Structure 16: 1503-1510.
10. Tang Y, Holbert MA, Wurtele H, Meeth K, Rocha W, et al. (2008) Fungal Rtt109 histone acetyltransferase is an unexpected structural homolog of metazoan p300/CBP. Nat Struct Mol Biol 15: 998.
11. Collins SR, Miller KM, Maas NL, Roguev A, Fillingham J, et al. (2007) Functional dissection of protein complexes involved in yeast chromosome biology using a genetic interaction map. Nature 446: 806-810.
12. Driscoll R, Hudson A, Jackson SP (2007) Yeast Rtt109 promotes genome stability by acetylating histone H3 on lysine 56. Science 315: 649-652.
13. Das C, Lucia MS, Hansen KC, Tyler JK (2009) CBP/p300-mediated acetylation of histone H3 on lysine 56. Nature 459: 113-117.
14. Tjeertes JV, Miller KM, Jackson SP (2009) Screen for DNA-damage-responsive histone modifications identifies H3K9Ac and H3K56Ac in human cells. Embo J 28: 1878-1889.
15. Recht J, Tsubota T, Tanny JC, Diaz RL, Berger JM, et al. (2006) 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 U S A 103: 6988-6993.
16. Rufiange A, Jacques PE, Bhat W, Robert F, Nourani A (2007) Genome-wide replication-independent histone H3 exchange occurs predominantly at promoters and implicates H3 K56 acetylation and Asf1. Mol Cell 27: 393-405.
17. Williams SK, Truong D, Tyler JK (2008) Acetylation in the globular core of histone H3 on lysine-56 promotes chromatin disassembly during transcriptional activation. Proc Natl Acad Sci U S A 105: 9000-9005.
18. Miller A, Yang B, Foster T, Kirchmaier AL (2008) Proliferating cell nuclear antigen and ASF1 modulate silent chromatin in Saccharomyces cerevisiae via lysine 56 on histone H3. Genetics 179: 793-809.
19. Michishita E, McCord RA, Boxer LD, Barber MF, Hong T, et al. (2009) Cell cycle-dependent deacetylation of telomeric histone H3 lysine K56 by human SIRT6. Cell Cycle 8: 2664-2666.
20. Yang B, Zwaans BM, Eckersdorff M, Lombard DB (2009) The sirtuin SIRT6 deacetylates H3 K56Ac in vivo to promote genomic stability. Cell Cycle 8: 2662-2663.
21. Yuan J, Pu M, Zhang Z, Lou Z (2009) Histone H3-K56 acetylation is important for genomic stability in mammals. Cell Cycle 8: 1747-1753.
22. Celic I, Masumoto H, Griffith WP, Meluh P, Cotter RJ, et al. (2006) The sirtuins hst3 and Hst4p preserve genome integrity by controlling histone h3 lysine 56 deacetylation. Curr Biol 16: 1280-1289.
23. Maas NL, Miller KM, DeFazio LG, Toczyski DP (2006) Cell cycle and checkpoint regulation of histone H3 K56 acetylation by Hst3 and Hst4. Mol Cell 23: 109-119.
24. Ozdemir A, Masumoto H, Fitzjohn P, Verreault A, Logie C (2006) Histone H3 lysine 56 acetylation: a new twist in the chromosome cycle. Cell Cycle 5: 2602-2608.
25. Celic I, Verreault A, Boeke JD (2008) Histone H3 K56 hyperacetylation perturbs replisomes and causes DNA damage. Genetics 179: 1769-1784.
26. Li Q, Zhou H, Wurtele H, Davies B, Horazdovsky B, et al. (2008) Acetylation of histone H3 lysine 56 regulates replication-coupled nucleosome assembly. Cell 134: 244-255.
27. Neumann H, Hancock SM, Buning R, Routh A, Chapman L, et al. (2009) A method for genetically installing site-specific acetylation in recombinant histones defines the effects of H3 K56 acetylation. Mol Cell 36: 153-163.
28. Hurd PJ, Bannister AJ, Halls K, Dawson MA, Vermeulen M, et al. (2009) Phosphorylation of histone H3 Thr-45 is linked to apoptosis. J Biol Chem 284: 16575-16583.
29. Olsen JV, Vermeulen M, Santamaria A, Kumar C, Miller ML, et al. (2010) Quantitative phosphoproteomics reveals widespread full phosphorylation site occupancy during mitosis. Sci Signal 3: ra3.
30. Zielinska DF, Gnad F, Jedrusik-Bode M, Wiśniewski JR, Mann M (2009) Caenorhabditis elegans has a phosphoproteome atypical for metazoans that is enriched in developmental and sex determination proteins. J Proteome Res 8: 4039-4049.
31. Knapp AR, Ren C, Su X, Lucas DM, Byrd JC, et al. (2007) Quantitative profiling of histone post-translational modifications by stable isotope labeling. Methods 41: 312-319.
32. Campsteijn C, Wijnands-Collin AM, Logie C (2007) Reverse genetic analysis of the yeast RSC chromatin remodeler reveals a role for RSC3 and SNF5 homolog 1 in ploidy maintenance. PLoS Genet 3: e92.
33. Erkmann JA, Kaufman PD (2009) A negatively charged residue in place of histone H3K56 supports chromatin assembly factor association but not genotoxic stress resistance. DNA Repair 8: 1371-9.
34. Tercero JA, Diffley JF (2001) Regulation of DNA replication fork progression through damaged DNA by the Mec1/Rad53 checkpoint. Nature 412: 553-537.
35. Chen CC, Carson JJ, Feser J, Tamburini B, Zabaronick S, et al. (2008) Acetylated lysine 56 on histone H3 drives chromatin assembly after repair and signals for the completion of repair. Cell 134: 231-243.
36. Davidson MB, Brown GW (2009) Dissecting the DNA damage response using functional genomics approaches in S. cerevisiae. DNA Repair 8: 1110-1117.
37. Schleker T, Nagai S, Gasser SM (2009) Posttranslational modifications of repair factors and histones in the cellular response to stalled replication forks. DNA Repair 8: 1089-1100.
38. Yang JH, Freudenreich CH (2010) The Rtt109 histone acetyltransferase facilitates error-free replication to prevent CAG/CTG repeat contractions. DNA Repair 9: 414-20.
39. Dai J, Hyland EM, Yuan DS, Huang H, Bader JS, et al. (2008) Probing nucleosome function: a highly versatile library of synthetic histone H3 and H4 mutants. Cell 134: 1066-1078.
40. Xu F, Zhang K, Grunstein M (2005) Acetylation in histone H3 globular domain regulates gene expression in yeast. Cell 121: 375-385.
41. Schneider J, Bajwa P, Johnson FC, Bhaumik SR, Shilatifard A (2006) Rtt109 is required for proper H3K56 acetylation: a chromatin mark associated with the elongating RNA polymerase II. J Biol Chem 281: 37270-37274.
42. Eitoku M, Sato L, Senda T, Horikoshi M (2008) Histone chaperones: 30 years from isolation to elucidation of the mechanisms of nucleosome assembly and disassembly. Cell Mol Life Sci 65: 414-444.
43. Ransom M, Dennehey BK, Tyler JK (2010) Chaperoning Histones during DNA Replication and Repair. Cell 140: 183-195.
44. Schwabish MA, Struhl K (2006) Asf1 mediates histone eviction and deposition during elongation by RNA polymerase II. Mol Cell 22: 415-422.
45. Imbeault D, Gamar L, Rufiange A, Paquet E, Nourani A (2008) The Rtt106 histone chaperone is functionally linked to transcription elongation and is involved in the regulation of spurious transcription from cryptic promoters in yeast. J Biol Chem 283: 27350-27354.
46. Carey M, Li B, Workman JL (2006) RSC exploits histone acetylation to abrogate the nucleosomal block to RNA polymerase II elongation. Mol Cell 24: 481-487.
47. Morillon A, Karabetsou N, Nair A, Mellor J (2005) Dynamic lysine methylation on histone H3 defines the regulatory phase of gene transcription. Mol Cell 18: 723-732.
48. Gunjan A, Verreault A (2003) A Rad53 kinase-dependent surveillance mechanism that regulates histone protein levels in S. cerevisiae. Cell 115: 537-549.
49. Park YJ, Luger K (2008) Histone chaperones in nucleosome eviction and histone exchange. Curr Opin Struct Biol 18: 282-289.
50. Fillingham J, Recht J, Silva AC, Suter B, Emili A, et al. (2008) Chaperone control of the activity and specificity of the histone H3 acetyltransferase Rtt109. Mol Cell Biol 28: 4342-4353.
51. Nakanishi S, Sanderson BW, Delventhal KM, Bradford WD, Staehling-Hampton K, et al. (2008) A comprehensive library of histone mutants identifies nucleosomal residues required for H3K4 methylation. Nat Struct Mol Biol 15: 881-888.
52. Murzina NV, Pei XY, Zhang W, Sparkes M, Vicente-Garcia J, et al. (2008) Structural basis for the recognition of histone H4 by the histone-chaperone RbAp46. Structure 16: 1077-1085.
53. Song JJ, Garlick JD, Kingston RE (2008) Structural basis of histone H4 recognition by p55. Genes Dev 22: 1313-1318.
54. Davey CA, Sargent DF, Luger K, Maeder AW, Richmond TJ (2002) Solvent mediated interactions in the structure of the nucleosome core particle at 1.9 a resolution. J Mol Biol 319: 1097-1113.