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. 2010 Jul 29;1(7):607–612. doi: 10.1007/s13238-010-0086-y

Histones, histone chaperones and nucleosome assembly

Rebecca J Burgess 1, Zhiguo Zhang 1,✉
PMCID: PMC4875279  PMID: 21203931

Abstract

Chromatin structure governs a number of cellular processes including DNA replication, transcription, and DNA repair. During DNA replication, chromatin structure including the basic repeating unit of chromatin, the nucleosome, is temporarily disrupted, and then reformed immediately after the passage of the replication fork. This coordinated process of nucleosome assembly during DNA replication is termed replication—coupled nucleosome assembly. Disruption of this process can lead to genome instability, a hallmark of cancer cells. Therefore, addressing how replication-coupled nucleosome assembly is regulated has been of great interest. Here, we review the current status of this growing field of interest, highlighting recent advances in understanding the regulation of this important process by the dynamic interplay of histone chaperones and histone modifications.

References

  1. Ahmad K., Henikoff S. Histone H3 variants specify modes of chromatin assembly. Proc Natl Acad Sci U S A. 2002;99:16477–16484. doi: 10.1073/pnas.172403699. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Ai X., Parthun M.R. The nuclear Hat1p/Hat2p complex: a molecular link between type B histone acetyltransferases and chromatin assembly. Mol Cell. 2004;14:195–205. doi: 10.1016/S1097-2765(04)00184-4. [DOI] [PubMed] [Google Scholar]
  3. Burgess R.J., Zhou H., Han J., Zhang Z. A role for Gcn5 in replication-coupled nucleosome assembly. Mol Cell. 2010;37:469–480. doi: 10.1016/j.molcel.2010.01.020. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Carrozza M.J., Utley R.T., Workman J.L., Côté J. The diverse functions of histone acetyltransferase complexes. Trends Genet. 2003;19:321–329. doi: 10.1016/S0168-9525(03)00115-X. [DOI] [PubMed] [Google Scholar]
  5. Chen C.C., Carson J.J., Feser J., Tamburini B., Zabaronick S., Linger J., Tyler J.K. Acetylated lysine 56 on histone H3 drives chromatin assembly after repair and signals for the completion of repair. Cell. 2008;134:231–243. doi: 10.1016/j.cell.2008.06.035. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Chodaparambil J.V., Edayathumangalam R.S., Bao Y., Park Y.J., Luger K. Nucleosome structure and function. Ernst Schering Res Found Workshop. 2006;57:29–46. doi: 10.1007/3-540-37633-X_2. [DOI] [PubMed] [Google Scholar]
  7. Das C., Lucia M.S., Hansen K.C., Tyler J.K. CBP/p300-mediated acetylation of histone H3 on lysine 56. Nature. 2009;459:113–117. doi: 10.1038/nature07861. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Drane P., Ouararhni K., Depaux A., Shuaib M., Hamiche A. The death-associated protein DAXX is a novel histone chaperone involved in the replication-independent deposition of H3. Genes Dev. 2010;24:1253–1265. doi: 10.1101/gad.566910. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Driscoll R., Hudson A., Jackson S.P. Yeast Rtt109 promotes genome stability by acetylating histone H3 on lysine 56. Science. 2007;315:649–652. doi: 10.1126/science.1135862. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. English C.M., Adkins M.W., Carson J.J., Churchill M.E., Tyler J.K. Structural basis for the histone chaperone activity of Asf1. Cell. 2006;127:495–508. doi: 10.1016/j.cell.2006.08.047. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Falbo K.B., Shen X. Chromatin remodeling in DNA replication. J Cell Biochem. 2006;97:684–689. doi: 10.1002/jcb.20752. [DOI] [PubMed] [Google Scholar]
  12. Fillingham J., Kainth P., Lambert J.P., van Bakel H., Tsui K., Peña-Castillo L., Nislow C., Figeys D., Hughes T.R., Greenblatt J., et al. Two-color cell array screen reveals interdependent roles for histone chaperones and a chromatin boundary regulator in histone gene repression. Mol Cell. 2009;35:340–351. doi: 10.1016/j.molcel.2009.06.023. [DOI] [PubMed] [Google Scholar]
  13. Goldberg A.D., Allis C.D., Bernstein E. Epigenetics: a landscape takes shape. Cell. 2007;128:635–638. doi: 10.1016/j.cell.2007.02.006. [DOI] [PubMed] [Google Scholar]
  14. Groth A., Corpet A., Cook A.J., Roche D., Bartek J., Lukas J., Almouzni G. Regulation of replication fork progression through histone supply and demand. Science. 2007;318:1928–1931. doi: 10.1126/science.1148992. [DOI] [PubMed] [Google Scholar]
  15. Han J., Zhou H., Horazdovsky B., Zhang K., Xu R.M., Zhang Z. Rtt109 acetylates histone H3 lysine 56 and functions in DNA replication. Science. 2007;315:653–655. doi: 10.1126/science.1133234. [DOI] [PubMed] [Google Scholar]
  16. Huang S., Zhou H., Katzmann D., Hochstrasser M., Atanasova E., Zhang Z. Rtt106p is a histone chaperone involved in heterochromatin-mediated silencing. Proc Natl Acad Sci U S A. 2005;102:13410–13415. doi: 10.1073/pnas.0506176102. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Huang S., Zhou H., Tarara J., Zhang Z. A novel role for histone chaperones CAF-1 and Rtt106p in heterochromatin silencing. EMBO J. 2007;26:2274–2283. doi: 10.1038/sj.emboj.7601670. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Imbeault D., Gamar L., Rufiange A., Paquet E., Nourani A. 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. 2008;283:27350–27354. doi: 10.1074/jbc.C800147200. [DOI] [PubMed] [Google Scholar]
  19. Jackson V., Shires A., Tanphaichitr N., Chalkley R. Modifications to histones immediately after synthesis. J Mol Biol. 1976;104:471–483. doi: 10.1016/0022-2836(76)90282-5. [DOI] [PubMed] [Google Scholar]
  20. Jasencakova Z., Scharf A.N., Ask K., Corpet A., Imhof A., Almouzni G., Groth A. Replication stress interferes with histone recycling and predeposition marking of new histones. Mol Cell. 2010;37:736–743. doi: 10.1016/j.molcel.2010.01.033. [DOI] [PubMed] [Google Scholar]
  21. Jenuwein T., Allis C.D. Translating the histone code. Science. 2001;293:1074–1080. doi: 10.1126/science.1063127. [DOI] [PubMed] [Google Scholar]
  22. Kaufman P.D., Kobayashi R., Stillman B. Ultraviolet radiation sensitivity and reduction of telomeric silencing in Saccharomyces cerevisiae cells lacking chromatin assembly factor-I. Genes Dev. 1997;11:345–357. doi: 10.1101/gad.11.3.345. [DOI] [PubMed] [Google Scholar]
  23. Kornberg R.D., Lorch Y. Twenty-five years of the nucleosome, fundamental particle of the eukaryote chromosome. Cell. 1999;98:285–294. doi: 10.1016/S0092-8674(00)81958-3. [DOI] [PubMed] [Google Scholar]
  24. Le S., Davis C., Konopka J.B., Sternglanz R. Two new S-phase-specific genes from Saccharomyces cerevisiae. Yeast. 1997;13:1029–1042. doi: 10.1002/(SICI)1097-0061(19970915)13:11<1029::AID-YEA160>3.0.CO;2-1. [DOI] [PubMed] [Google Scholar]
  25. Li Q., Fazly A.M., Zhou H., Huang S., Zhang Z., Stillman B., Pearson C.E. The elongator complex interacts with PCNA and modulates transcriptional silencing and sensitivity to DNA damage agents. PLoS Genet. 2009;5:e1000684. doi: 10.1371/journal.pgen.1000684. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Li Q., Zhou H., Wurtele H., Davies B., Horazdovsky B., Verreault A., Zhang Z. Acetylation of histone H3 lysine 56 regulates replication-coupled nucleosome assembly. Cell. 2008;134:244–255. doi: 10.1016/j.cell.2008.06.018. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Linger J., Tyler J.K. The yeast histone chaperone chromatin assembly factor 1 protects against double-strand DNA-damaging agents. Genetics. 2005;171:1513–1522. doi: 10.1534/genetics.105.043000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Loyola A., Bonaldi T., Roche D., Imhof A., Almouzni G. PTMs on H3 variants before chromatin assembly potentiate their final epigenetic state. Mol Cell. 2006;24:309–316. doi: 10.1016/j.molcel.2006.08.019. [DOI] [PubMed] [Google Scholar]
  29. Luger K., Mäder A.W., Richmond R.K., Sargent D.F., Richmond T.J. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature. 1997;389:251–260. doi: 10.1038/38444. [DOI] [PubMed] [Google Scholar]
  30. Ma X.J., Wu J., Altheim B.A., Schultz M.C., Grunstein M. Deposition-related sites K5/K12 in histone H4 are not required for nucleosome deposition in yeast. Proc Natl Acad Sci U S A. 1998;95:6693–6698. doi: 10.1073/pnas.95.12.6693. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Marmorstein R. Structural and chemical basis of histone acetylation. Novartis Found Symp. 2004;259:78–98. doi: 10.1002/0470862637.ch6. [DOI] [PubMed] [Google Scholar]
  32. Marmorstein R., Roth S.Y. Histone acetyltransferases: function, structure, and catalysis. Curr Opin Genet Dev. 2001;11:155–161. doi: 10.1016/S0959-437X(00)00173-8. [DOI] [PubMed] [Google Scholar]
  33. 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;436:294–298. doi: 10.1038/nature03714. [DOI] [PubMed] [Google Scholar]
  34. Mello J.A., Silljé H.H., Roche D.M., Kirschner D.B., Nigg E.A., Almouzni G. Human Asf1 and CAF-1 interact and synergize in a repair-coupled nucleosome assembly pathway. EMBO Rep. 2002;3:329–334. doi: 10.1093/embo-reports/kvf068. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Ransom M., Dennehey B.K., Tyler J.K. Chaperoning histones during DNA replication and repair. Cell. 2010;140:183–195. doi: 10.1016/j.cell.2010.01.004. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Recht J., Tsubota T., Tanny J.C., Diaz R.L., Berger J.M., Zhang X., Garcia B.A., Shabanowitz J., Burlingame A.L., Hunt D.F., et al. 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. 2006;103:6988–6993. doi: 10.1073/pnas.0601676103. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Rocha W., Verreault A. Clothing up DNA for all seasons: Histone chaperones and nucleosome assembly pathways. FEBS Lett. 2008;582:1938–1949. doi: 10.1016/j.febslet.2008.03.006. [DOI] [PubMed] [Google Scholar]
  38. Roth S.Y., Denu J.M., Allis C.D. Histone acetyltransferases. Annu Rev Biochem. 2001;70:81–120. doi: 10.1146/annurev.biochem.70.1.81. [DOI] [PubMed] [Google Scholar]
  39. Ruiz-Carrillo A., Wangh L.J., Allfrey V.G. Processing of newly synthesized histone molecules. Science. 1975;190:117–128. doi: 10.1126/science.1166303. [DOI] [PubMed] [Google Scholar]
  40. Scholes D.T., Banerjee M., Bowen B., Curcio M.J. Multiple regulators of Ty1 transposition in Saccharomyces cerevisiae have conserved roles in genome maintenance. Genetics. 2001;159:1449–1465. doi: 10.1093/genetics/159.4.1449. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Shahbazian M.D., Grunstein M. Functions of sitespecific histone acetylation and deacetylation. Annu Rev Biochem. 2007;76:75–100. doi: 10.1146/annurev.biochem.76.052705.162114. [DOI] [PubMed] [Google Scholar]
  42. Shibahara K., Stillman B. Replication-dependent marking of DNA by PCNA facilitates CAF-1-coupled inheritance of chromatin. Cell. 1999;96:575–585. doi: 10.1016/S0092-8674(00)80661-3. [DOI] [PubMed] [Google Scholar]
  43. Sobel R.E., Cook R.G., Perry C.A., Annunziato A.T., Allis C.D. Conservation of deposition-related acetylation sites in newly synthesized histones H3 and H4. Proc Natl Acad Sci U S A. 1995;92:1237–1241. doi: 10.1073/pnas.92.4.1237. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Stillman B. Chromatin assembly during SV40 DNA replication in vitro. Cell. 1986;45:555–565. doi: 10.1016/0092-8674(86)90287-4. [DOI] [PubMed] [Google Scholar]
  45. Strahl B.D., Allis C.D. The language of covalent histone modifications. Nature. 2000;403:41–45. doi: 10.1038/47412. [DOI] [PubMed] [Google Scholar]
  46. 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. doi: 10.1016/S0092-8674(03)01064-X. [DOI] [PubMed] [Google Scholar]
  47. Tjeertes J.V., Miller K.M., Jackson S.P. Screen for DNA-damage-responsive histone modifications identifies H3K9Ac and H3K56Ac in human cells. EMBO J. 2009;28:1878–1889. doi: 10.1038/emboj.2009.119. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Turner B.M. Histone acetylation and an epigenetic code. Bioessays. 2000;22:836–845. doi: 10.1002/1521-1878(200009)22:9<836::AID-BIES9>3.0.CO;2-X. [DOI] [PubMed] [Google Scholar]
  49. Tyler J.K. Chromatin assembly. Cooperation between histone chaperones and ATP-dependent nucleosome remodeling machines. Eur J Biochem. 2002;269:2268–2274. doi: 10.1046/j.1432-1033.2002.02890.x. [DOI] [PubMed] [Google Scholar]
  50. 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. 1999;402:555–560. doi: 10.1038/990147. [DOI] [PubMed] [Google Scholar]
  51. Tyler J.K., Collins K.A., Prasad-Sinha J., Amiott E., Bulger M., Harte P.J., Kobayashi R., Kadonaga J.T. Interaction between the Drosophila CAF-1 and ASF1 chromatin assembly factors. Mol Cell Biol. 2001;21:6574–6584. doi: 10.1128/MCB.21.19.6574-6584.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. VanDemark A.P., Blanksma M., Ferris E., Heroux A., Hill C.P., Formosa T. The structure of the yFACT Pob3-M domain, its interaction with the DNA replication factor RPA, and a potential role in nucleosome deposition. Mol Cell. 2006;22:363–374. doi: 10.1016/j.molcel.2006.03.025. [DOI] [PubMed] [Google Scholar]
  53. Verreault A., Kaufman P.D., Kobayashi R., Stillman B. Nucleosome assembly by a complex of CAF-1 and acetylated histones H3/H4. Cell. 1996;87:95–104. doi: 10.1016/S0092-8674(00)81326-4. [DOI] [PubMed] [Google Scholar]
  54. Vidanes G.M., Bonilla C.Y., Toczyski D.P. Complicated tails: histone modifications and the DNA damage response. Cell. 2005;121:973–976. doi: 10.1016/j.cell.2005.06.013. [DOI] [PubMed] [Google Scholar]
  55. Wu J., Grunstein M. 25 years after the nucleosome model: chromatin modifications. Trends Biochem Sci. 2000;25:619–623. doi: 10.1016/S0968-0004(00)01718-7. [DOI] [PubMed] [Google Scholar]
  56. Yuan J., Pu M., Zhang Z., Lou Z. Histone H3-K56 acetylation is important for genomic stability in mammals. Cell Cycle. 2009;8:1747–1753. doi: 10.4161/cc.8.11.8620. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Zhou H., Madden B.J., Muddiman D.C., 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;45:2852–2861. doi: 10.1021/bi0521083. [DOI] [PubMed] [Google Scholar]

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