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Histone modifications during DNA replication

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Molecules and Cells

Abstract

Faithful and accurate replication of the DNA molecule is essential for eukaryote organisms. Nonetheless, in the last few years it has become evident that inheritance of the chromatin states associated with different regions of the genome is as important as the faithful inheritance of the DNA sequence itself. Such chromatin states are determined by a multitude of factors that act to modify not only the DNA molecule, but also the histone proteins associated with it. For instance, histones can be posttranslationally modified, and it is well established that these posttranslational marks are involved in several essential nuclear processes such as transcription and DNA repair. However, recent evidence indicates that posttranslational modifications of histones might be relevant during DNA replication. Hence, the aim of this review is to describe the most recent publications related to the role of histone posttranslational modifications during DNA replication.

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References

  • Ahmad, K., and Henikoff, S. (2002). The histone variant H3.3 marks active chromatin by replication-independent nucleosome assembly. Mol. Cell 9, 1191–1200.

    Article  PubMed  CAS  Google Scholar 

  • Alexandrow, M.G., and Hamlin, J.L. (2005). Chromatin decondensation in S-phase involves recruitment of Cdk2 by Cdc45 and histone H1 phosphorylation. J. Cell Biol. 168, 875–886.

    Article  PubMed  CAS  Google Scholar 

  • Allis, C.D., Berger, S.L., Cote, J., Dent, S., Jenuwien, T., Kouzarides, T., Pillus, L., Reinberg, D., Shi, Y., Shiekhattar, R., et al. (2007). New nomenclature for chromatin-modifying enzymes. Cell 131, 633–636.

    Article  PubMed  CAS  Google Scholar 

  • Annunziato, A.T., and Seale, R.L. (1983). Histone deacetylation is required for the maturation of newly replicated chromatin. J. Biol. Chem. 258, 12675–12684.

    PubMed  CAS  Google Scholar 

  • Balhorn, R., Chalkley, R., and Granner, D. (1972). Lysine-rich histone phosphorylation. A positive correlation with cell replication. Biochemistry 11, 1094–1098.

    Article  PubMed  CAS  Google Scholar 

  • Barman, H.K., Takami, Y., Ono, T., Nishijima, H., Sanematsu, F., Shibahara, K., and Nakayama, T. (2006). Histone acetyltransferase 1 is dispensable for replication-coupled chromatin assembly but contributes to recover DNA damages created following replication blockage in vertebrate cells. Biochem. Biophys. Res. Commun. 345, 1547–1557.

    Article  PubMed  CAS  Google Scholar 

  • Barman, H.K., Takami, Y., Nishijima, H., Shibahara, K., Sanematsu, F., and Nakayama, T. (2008). Histone acetyltransferase-1 regulates integrity of cytosolic histone H3-H4 containing complex. Biochem. Biophys. Res. Commun. 373, 624–630.

    Article  PubMed  CAS  Google Scholar 

  • Benson, L.J., Gu, Y., Yakovleva, T., Tong, K., Barrows, C., Strack, C.L., Cook, R.G., Mizzen, C.A., and Annunziato, A.T. (2006). Modifications of H3 and H4 during chromatin replication, nucleosome assembly, and histone exchange. J. Biol. Chem. 281, 9287–9296.

    Article  PubMed  CAS  Google Scholar 

  • Bradbury, E.M., Inglis, R.J., and Matthews, H.R. (1974). Control of cell division by very lysine rich histone (F1) phosphorylation. Nature 247, 257–261.

    Article  PubMed  CAS  Google Scholar 

  • Celic, I., Masumoto, H., Griffith, W.P., Meluh, P., Cotter, R.J., Boeke, J.D., and Verreault, A. (2006). The sirtuins hst3 and Hst4p preserve genome integrity by controlling histone h3 lysine 56 deacetylation. Curr. Biol. 16, 1280–1289.

    Article  PubMed  CAS  Google Scholar 

  • Celic, I., Verreault, A., and Boeke, J.D. (2008). Histone H3 K56 hyperacetylation perturbs replisomes and causes DNA damage. Genetics 179, 1769–1784.

    Article  PubMed  CAS  Google Scholar 

  • Chen, C.C., Carson, J.J., Feser, J., Tamburini, B., Zabaronick, S., Linger, J., and Tyler, J.K. (2008). Acetylated lysine 56 on histone H3 drives chromatin assembly after repair and signals for the completion of repair. Cell 134, 231–243.

    Article  PubMed  CAS  Google Scholar 

  • Chiani, F., Di Felice, F., and Camilloni, G. (2006). SIR2 modifies histone H4-K16 acetylation and affects superhelicity in the ARS region of plasmid chromatin in Saccharomyces cerevisiae. Nucleic Acids Res. 34, 5426–5437.

    Article  PubMed  CAS  Google Scholar 

  • Collins, S.R., Miller, K.M., Maas, N.L., Roguev, A., Fillingham, J., Chu, C.S., Schuldiner, M., Gebbia, M., Recht, J., Shales, M., et al. (2007). Functional dissection of protein complexes involved in yeast chromosome biology using a genetic interaction map. Nature 446, 806–810.

    Article  PubMed  CAS  Google Scholar 

  • Davey, C.A., Sargent, D.F., Luger, K., Maeder, A.W., and Richmond, T.J. (2002). Solvent mediated interactions in the structure of the nucleosome core particle at 1.9 a resolution. J. Mol. Biol. 319, 1097–1113.

    Article  PubMed  CAS  Google Scholar 

  • Deterding, L.J., Bunger, M.K., Banks, G.C., Tomer, K.B., and Archer, T.K. (2008). Global changes in and characterization of specific sites of phosphorylation in mouse and human histone H1 Isoforms upon CDK inhibitor treatment using mass spectrometry. J. Proteome Res. 7, 2368–2379.

    Article  PubMed  Google Scholar 

  • Driscoll, R., Hudson, A., and Jackson, S.P. (2007). Yeast Rtt109 promotes genome stability by acetylating histone H3 on lysine 56. Science 315, 649–652.

    Article  PubMed  CAS  Google Scholar 

  • Duro, E., Vaisica, J.A., Brown, G.W., and Rouse, J. (2008). Budding yeast Mms22 and Mms1 regulate homologous recombination induced by replisome blockage. DNA Repair 7, 811–818.

    Article  PubMed  CAS  Google Scholar 

  • Dutnall, R.N., Tafrov, S.T., Sternglanz, R., and Ramakrishnan, V. (1998). Structure of the histone acetyltransferase Hat1: a paradigm for the GCN5-related N-acetyltransferase superfamily. Cell 94, 427–438.

    Article  PubMed  CAS  Google Scholar 

  • English, C.M., Adkins, M.W., Carson, J.J., Churchill, M.E., and Tyler, J.K. (2006). Structural basis for the histone chaperone activity of Asf1. Cell 127, 495–508.

    Article  PubMed  CAS  Google Scholar 

  • Falbo, K.B., and Shen, X. (2006). Chromatin remodeling in DNA replication. J. Cell Biochem. 97, 684–689.

    Article  PubMed  CAS  Google Scholar 

  • Fan, Y., Nikitina, T., Zhao, J., Fleury, T.J., Bhattacharyya, R., Bouhassira, E.E., Stein, A., Woodcock, C.L., and Skoultchi, A.I. (2005). Histone H1 depletion in mammals alters global chromatin structure but causes specific changes in gene regulation. Cell 123, 1199–1212.

    Article  PubMed  CAS  Google Scholar 

  • Fang, J., Feng, Q., Ketel, C.S., Wang, H., Cao, R., Xia, L., Erdjument-Bromage, H., Tempst, P., Simon, J.A., and Zhang, Y. (2002). Purification and functional characterization of SET8, a nucleosomal histone H4-lysine 20-specific methyltransferase. Curr. Biol. 12, 1086–1099.

    Article  PubMed  CAS  Google Scholar 

  • Fisher, D., and Mechali, M. (2003). Vertebrate HoxB gene expression requires DNA replication. EMBO J 22, 3737–3748.

    Article  PubMed  CAS  Google Scholar 

  • Garcia, B.A., Busby, S.A., Barber, C.M., Shabanowitz, J., Allis, C.D., and Hunt, D.F. (2004). Characterization of phosphorylation sites on histone H1 isoforms by tandem mass spectrometry. J. Proteome Res. 3, 1219–1227.

    Article  PubMed  CAS  Google Scholar 

  • Garcia, B.A., Hake, S.B., Diaz, R.L., Kauer, M., Morris, S.A., Recht, J., Shabanowitz, J., Mishra, N., Strahl, B.D., Allis, C.D., et al. (2007). Organismal differences in post-translational modifications in histones H3 and H4. J. Biol. Chem. 282, 7641–7655.

    Article  PubMed  CAS  Google Scholar 

  • Glowczewski, L., Waterborg, J.H., and Berman, J.G. (2004). Yeast chromatin assembly complex 1 protein excludes nonacetylatable forms of histone H4 from chromatin and the nucleus. Mol. Cell. Biol. 24, 10180–10192.

    Article  PubMed  CAS  Google Scholar 

  • Groth, A., Ray-Gallet, D., Quivy, J.P., Lukas, J., Bartek, J., and Almouzni, G. (2005). Human Asf1 regulates the flow of S phase histones during replicational stress. Mol. Cell 17, 301–311.

    Article  PubMed  CAS  Google Scholar 

  • Groth, A., Rocha, W., Verreault, A., and Almouzni, G. (2007). Chromatin challenges during DNA replication and repair. Cell 128, 721–733.

    Article  PubMed  CAS  Google Scholar 

  • Gurley, L.R., Walters, R.A., and Tobey, R.A. (1975). Sequential phsophorylation of histone subfractions in the Chinese hamster cell cycle. J. Biol. Chem. 250, 3936–3944.

    PubMed  CAS  Google Scholar 

  • Halmer, L., and Gruss, C. (1996). Effects of cell cycle dependent histone H1 phosphorylation on chromatin structure and chromatin replication. Nucleic Acids Res. 24, 1420–1427.

    Article  PubMed  CAS  Google Scholar 

  • Han, J., Zhou, H., Horazdovsky, B., Zhang, K., Xu, R.M., and Zhang, Z. (2007a). Rtt109 acetylates histone H3 lysine 56 and functions in DNA replication. Science 315, 653–655.

    Article  PubMed  CAS  Google Scholar 

  • Han, J., Zhou, H., Li, Z., Xu, R.M., and Zhang, Z. (2007b). Acetylation of lysine 56 of histone H3 catalyzed by RTT109 and regulated by ASF1 is required for replisome integrity. J. Biol. Chem. 282, 28587–28596.

    Article  PubMed  CAS  Google Scholar 

  • Huang, S., Zhou, H., Katzmann, D., Hochstrasser, M., Atanasova, E., and Zhang, Z. (2005). Rtt106p is a histone chaperone involved in heterochromatin-mediated silencing. Proc. Natl. Acad. Sci. USA 102, 13410–13415.

    Article  PubMed  CAS  Google Scholar 

  • Huen, M.S., Sy, S.M., van Deursen, J.M., and Chen, J. (2008). Direct interaction between SET8 and proliferating cell nuclear antigen couples H4-K20 methylation with DNA replication. J. Biol. Chem. 283, 11073–11077.

    Article  PubMed  CAS  Google Scholar 

  • Hyland, E.M., Cosgrove, M.S., Molina, H., Wang, D., Pandey, A., Cottee, R.J., and Boeke, J.D. (2005). Insights into the role of histone H3 and histone H4 core modifiable residues in Saccharomyces cerevisiae. Mol. Cell Biol. 25, 10060–10070.

    Article  PubMed  CAS  Google Scholar 

  • Jorgensen, S., Elvers, I., Trelle, M.B., Menzel, T., Eskildsen, M., Jensen, O.N., Helleday, T., Helin, K., and Sorensen, C.S. (2007). The histone methyltransferase SET8 is required for S-phase progression. J. Cell Biol. 179, 1337–1345.

    Article  PubMed  CAS  Google Scholar 

  • Karachentsev, D., Sarma, K., Reinberg, D., and Steward, R. (2005). PR-Set7-dependent methylation of histone H4 Lys 20 functions in repression of gene expression and is essential for mitosis. Genes Dev. 19, 431–435.

    Article  PubMed  CAS  Google Scholar 

  • Kim, H.S., Rhee, D.K., and Jang, Y.K. (2008). Methylations of histone H3 lysine 9 and lysine 36 are functionally linked to DNA replication checkpoint control in fission yeast. Biochem. Biophys. Res. Commun. 368, 419–425.

    Article  PubMed  CAS  Google Scholar 

  • Li, Q., Zhou, H., Wurtele, H., Davies, B., Horazdovsky, B., Verreault, A., and Zhang, Z. (2008). Acetylation of histone H3 lysine 56 regulates replication-coupled nucleosome assembly. Cell 134, 244–255.

    Article  PubMed  CAS  Google Scholar 

  • Lin, C., and Yuan, Y.A. (2008). Structural insights into histone H3 lysine 56 acetylation by Rtt109. Structure 16, 1503–1510.

    Article  PubMed  CAS  Google Scholar 

  • Loyola, A., Bonaldi, T., Roche, D., Imhof, A., and Almouzni, G. (2006). PTMs on H3 variants before chromatin assembly potentiate their final epigenetic state. Mol. Cell 24, 309–316.

    Article  PubMed  CAS  Google Scholar 

  • Lu, Z.H., Sittman, D.B., Brown, D.T., Munshi, R., and Leno, G.H. (1997). Histone H1 modulates DNA replication through multiple pathways in Xenopus egg extract. J. Cell Sci. 110, 2745–2758.

    PubMed  CAS  Google Scholar 

  • Ma, X.J., Wu, J., Altheim, B.A., Schultz, M.C., and Grunstein, M. (1998). Deposition-related sites K5/K12 in histone H4 are not required for nucleosome deposition in yeast. Proc. Natl. Acad. Sci. USA 95, 6693–6698.

    Article  PubMed  CAS  Google Scholar 

  • Maas, N.L., Miller, K.M., DeFazio, L.G., and Toczyski, D.P. (2006). Cell cycle and checkpoint regulation of histone H3 K56 acetylation by Hst3 and Hst4. Mol. Cell 23, 109–119.

    Article  PubMed  CAS  Google Scholar 

  • Makowski, A.M., Dutnall, R.N., and Annunziato, A.T. (2001). Effects of acetylation of histone H4 at lysines 8 and 16 on activity of the Hat1 histone acetyltransferase. J. Biol. Chem. 276, 43499–43502.

    Article  PubMed  CAS  Google Scholar 

  • Masumoto, H., Hawke, D., Kobayashi, R., and Verreault, A. (2005). A role for cell-cycle-regulated histone H3 lysine 56 acetylation in the DNA damage response. Nature 436, 294–298.

    Article  PubMed  CAS  Google Scholar 

  • Miller, A., Yang, B., Foster, T., and Kirchmaier, A.L. (2008). Proliferating cell nuclear antigen and ASF1 modulate silent chromatin in Saccharomyces cerevisiae via lysine 56 on histone H3. Genetics 179, 793–809.

    Article  PubMed  CAS  Google Scholar 

  • Ozdemir, A., Spicuglia, S., Lasonder, E., Vermeulen, M., Campsteijn, C., Stunnenberg, H.G., and Logie, C. (2005). Characterization of lysine 56 of histone H3 as an acetylation site in Saccharomyces cerevisiae. J. Biol. Chem. 280, 25949–25952.

    Article  PubMed  CAS  Google Scholar 

  • 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. (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. USA 103, 6988–6993.

    Article  PubMed  CAS  Google Scholar 

  • Rice, J.C., Nishioka, K., Sarma, K., Steward, R., Reinberg, D., and Allis, C.D. (2002). Mitotic-specific methylation of histone H4 Lys 20 follows increased PR-Set7 expression and its localization to mitotic chromosomes. Genes Dev. 16, 2225–2230.

    Article  PubMed  CAS  Google Scholar 

  • Sarg, B., Helliger, W., Talasz, H., Forg, B., and Lindner, H.H. (2006). Histone H1 phosphorylation occurs site-specifically during interphase and mitosis: identification of a novel phosphorylation site on histone H1. J. Biol. Chem. 281, 6573–6580.

    Article  PubMed  CAS  Google Scholar 

  • Schotta, G., Lachner, M., Sarma, K., Ebert, A., Sengupta, R., Reuter, G., Reinberg, D., and Jenuwein, T. (2004). A silencing pathway to induce H3-K9 and H4-K20 trimethylation at constitutive heterochromatin. Genes Dev. 18, 1251–1262.

    Article  PubMed  CAS  Google Scholar 

  • Shogren-Knaak, M., and Peterson, C.L. (2006). Switching on chromatin: mechanistic role of histone H4-K16 acetylation. Cell Cycle 5, 1361–1365.

    PubMed  CAS  Google Scholar 

  • Shogren-Knaak, M., Ishii, H., Sun, J.M., Pazin, M.J., Davie, J.R., and Peterson, C.L. (2006). Histone H4-K16 acetylation controls chromatin structure and protein interactions. Science 311, 844–847.

    Article  PubMed  CAS  Google Scholar 

  • Sobel, R.E., Cook, R.G., Perry, C.A., Annunziato, A.T., and Allis, C.D. (1995). Conservation of deposition-related acetylation sites in newly synthesized histones H3 and H4. Proc. Natl. Acad. Sci. USA 92, 1237–1241.

    Article  PubMed  CAS  Google Scholar 

  • Taddei, A., Roche, D., Sibarita, J.B., Turner, B.M., and Almouzni, G. (1999). Duplication and maintenance of heterochromatin domains. J. Cell Biol. 147, 1153–1166.

    Article  PubMed  CAS  Google Scholar 

  • Tagami, H., Ray-Gallet, D., Almouzni, G., and Nakatani, Y. (2004). Histone H3.1 and H3.3 complexes mediate nucleosome assembly pathways dependent or independent of DNA synthesis. Cell 116, 51–61.

    Article  PubMed  CAS  Google Scholar 

  • Thiriet, C., and Hayes, J.J. (2008). Linker histone phosphorylation regulates global timing of replication origin firing. J. Biol. Chem. 284, 2823–2329

    Article  PubMed  CAS  Google Scholar 

  • Ulrich, H.D. (2007). Conservation of DNA damage tolerance pathways from yeast to humans. Biochem. Soc. Trans. 35, 1334–1337.

    Article  PubMed  CAS  Google Scholar 

  • Volkel, P., and Angrand, P.O. (2007). The control of histone lysine methylation in epigenetic regulation. Biochimie 89, 1–20.

    Article  PubMed  CAS  Google Scholar 

  • Wisniewski, J.R., Zougman, A., and Mann, M. (2008). Nepsilon-formylation of lysine is a widespread post-translational modification of nuclear proteins occurring at residues involved in regulation of chromatin function. Nucleic Acids Res. 36, 570–577.

    Article  PubMed  CAS  Google Scholar 

  • Xu, F., Zhang, K., and Grunstein, M. (2005). Acetylation in histone H3 globular domain regulates gene expression in yeast. Cell 121, 375–385.

    Article  PubMed  CAS  Google Scholar 

  • Yang, B., Miller, A., and Kirchmaier, A.L. (2008). HST3/HST4-dependent deacetylation of lysine 56 of histone H3 in silent chromatin. Mol. Biol. Cell 19, 4993–5005.

    Article  PubMed  CAS  Google Scholar 

  • Yasuda, H., Matsumoto, Y., Mita, S., Marunouchi, T., and Yamada, M. (1981). A mouse temperature-sensitive mutant defective in H1 histone phosphorylation is defective in deoxyribonucleic acid synthesis and chromosome condensation. Biochemistry 20, 4414–4419.

    Article  PubMed  CAS  Google Scholar 

  • Zlatanova, J., and Doenecke, D. (1994). Histone H1 zero: a major player in cell differentiation? FASEB J. 8, 1260–1268.

    PubMed  CAS  Google Scholar 

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Correspondence to Xuetong Shen.

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Falbo, K.B., Shen, X. Histone modifications during DNA replication. Mol Cells 28, 149–154 (2009). https://doi.org/10.1007/s10059-009-0127-7

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