Abstract
Dynamic changes of chromatin structure control DNA-dependent events, including DNA replication. Along with DNA, chromatin organization must be replicated to maintain genetic and epigenetic information through cell generations. Chromatin remodelling is important for several steps in replication: determination and activation of origins of replication, replication machinery progression, chromatin assembly and DNA repair. Histone chaperones such as the FACT complex assist DNA replication within chromatin, probably by facilitating both nucleosome disassembly and reassembly. ATP-dependent nucleosome remodelling enzymes of the SWI/SNF family, in particular imitation switch (ISWI)-containing complexes, have been linked to DNA and chromatin replication. They are targeted to replication sites to facilitate DNA replication and subsequent chromatin assembly.
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Akey CW, Luger K (2003) Histone chaperones and nucleosome assembly. Curr Opin Struct Biol 13:6–14
Alexeev A, Mazin A, Kowalczykowski SC (2003) Rad54 protein possesses chromatin-remodeling activity stimulated by the Rad51-ssDNA nucleoprotein filament. Nat Struct Biol 10:182–186
Alexiadis V, Lusser A, Kadonaga JT (2004) A conserved N-terminal motif in Rad54 is important for chromatin remodeling and homologous strand pairing. J Biol Chem 279:27824–27829
Alexiadis V, Varga-Weisz PD, Bonte E, Becker PB, Gruss C (1998) In vitro chromatin remodelling by chromatin accessibility complex (CHRAC) at the SV40 origin of DNA replication. Embo J 17:3428–3438
Aligianni S, Varga-Weisz P (2005) Chromatin-remodelling factors and the maintenance of transcriptional states through DNA replication. Biochem Soc Symp 73:97–108
Anderson LA, Perkins ND (2002) The large subunit of replication factor C interacts with the histone deacetylase, HDAC1. J Biol Chem 277:29550–29554
Annunziato AT (2005) Split decision: what happens to nucleosomes during DNA replication? J Biol Chem 280:12065–12068
Aparicio JG, Viggiani CJ, Gibson DG, Aparicio OM (2004) The Rpd3-Sin3 histone deacetylase regulates replication timing and enables intra-S origin control in Saccharomyces cerevisiae. Mol Cell Biol 24:4769–4780
Baetz KK, Krogan NJ, Emili A, Greenblatt J, Hieter P (2004) The ctf13–30/CTF13 genomic haploinsufficiency modifier screen identifies the yeast chromatin remodeling complex RSC, which is required for the establishment of sister chromatid cohesion. Mol Cell Biol 24:1232–1244
Banting GS, Barak O, Ames TM, Burnham AC, Kardel MD, Cooch NS, Davidson CE, Godbout R, McDermid HE, Shiekhattar R (2005) CECR2, a protein involved in neurulation, forms a novel chromatin remodeling complex with SNF2L. Hum Mol Genet 14:513–524
Barak O, Lazzaro MA, Lane WS, Speicher DW, Picketts DJ, Shiekhattar R (2003) Isolation of human NURF: a regulator of Engrailed gene expression. Embo J 22:6089–6100
Becker PB (2005) Nucleosome remodelers on track. Nat Struct Mol Biol 12:732–733
Becker PB, Horz W (2002) ATP-dependent nucleosome remodeling. Annu Rev Biochem 71:247–273
Bell SP, Dutta A (2002) DNA replication in eukaryotic cells. Annu Rev Biochem 71:333–374
Belotserkovskaya R, Oh S, Bondarenko VA, Orphanides G, Studitsky VM, Reinberg D (2003) FACT facilitates transcription-dependent nucleosome alteration. Science 301:1090–1093
Belotserkovskaya R, Saunders A, Lis JT, Reinberg D (2004) Transcription through chromatin: understanding a complex FACT. Biochim Biophys Acta 1677:87–99
Biswas D, Yu Y, Prall M, Formosa T, Stillman DJ (2005) The yeast FACT complex has a role in transcriptional initiation. Mol Cell Biol 25:5812–5822
Bochar DA, Savard J, Wang W, Lafleur DW, Moore P, Cote J, Shiekhattar R (2000) A family of chromatin remodeling factors related to Williams syndrome transcription factor. Proc Natl Acad Sci USA 97:1038–1043
Bozhenok L, Wade PA, Varga-Weisz P (2002) WSTF-ISWI chromatin remodeling complex targets heterochromatic replication foci. Embo J 21:2231–2241
Brewster NK, Johnston GC, Singer RA (1998) Characterization of the CP complex, an abundant dimer of Cdc68 and Pob3 proteins that regulates yeast transcriptional activation and chromatin repression. J Biol Chem 273:21972–21979
Chai B, Huang J, Cairns BR, Laurent BC (2005) Distinct roles for the RSC and Swi/Snf ATP-dependent chromatin remodelers in DNA double-strand break repair. Genes Dev 19:1656–1661
Citterio E, Van Den Boom V, Schnitzler G, Kanaar R, Bonte E, Kingston RE, Hoeijmakers JH, Vermeulen W (2000) ATP-dependent chromatin remodeling by the Cockayne syndrome B DNA repair-transcription-coupling factor. Mol Cell Biol 20:7643–7653
Collins N, Poot RA, Kukimoto I, Garcia-Jimenez C, Dellaire G, Varga-Weisz PD (2002) An ACF1-ISWI chromatin-remodeling complex is required for DNA replication through heterochromatin. Nat Genet 32:627–632
Cosgrove MS, Wolberger C (2005) How does the histone code work? Biochem Cell Biol 83:468–476
Cvetic C, Walter JC (2005) Eukaryotic origins of DNA replication: could you please be more specific? Semin Cell Dev Biol 16:343–353
Dirscherl SS, Krebs JE (2004) Functional diversity of ISWI complexes. Biochem Cell Biol 82:482–489
Donaldson AD (2005) Shaping time: chromatin structure and the DNA replication programme. Trends Genet 21:444–449
Eberharter A, Becker PB (2004) ATP-dependent nucleosome remodelling: factors and functions. J Cell Sci 117:3707–3711
Ehrenhofer-Murray AE (2004) Chromatin dynamics at DNA replication, transcription and repair. Eur J Biochem 271:2335–2349
Eisen JA, Sweder KS, Hanawalt PC (1995) Evolution of the SNF2 family of proteins: subfamilies with distinct sequences and functions. Nucleic Acids Res 23:2715–2723
Flanagan JF, Peterson CL (1999) A role for the yeast SWI/SNF complex in DNA replication. Nucleic Acids Res 27:2022–2028
Formosa T, Eriksson P, Wittmeyer J, Ginn J, Yu Y, Stillman DJ (2001) Spt16-Pob3 and the HMG protein Nhp6 combine to form the nucleosome-binding factor SPN. Embo J 20:3506–3517
Fritsch O, Benvenuto G, Bowler C, Molinier J, Hohn B (2004) The INO80 protein controls homologous recombination in Arabidopsis thaliana. Mol Cell 16:479–485
Fyodorov DV, Blower MD, Karpen GH, Kadonaga JT (2004) Acf1 confers unique activities to ACF/CHRAC and promotes the formation rather than disruption of chromatin in vivo. Genes Dev 18:170–183
Goldmark JP, Fazzio TG, Estep PW, Church GM, Tsukiyama T (2000) The Isw2 chromatin remodeling complex represses early meiotic genes upon recruitment by Ume6p. Cell 103:423–433
Guschin D, Geiman TM, Kikyo N, Tremethick DJ, Wolffe AP, Wade PA (2000) Multiple ISWI ATPase complexes from Xenopus laevis. Functional conservation of an ACF/CHRAC homolog. J Biol Chem 275:35248–35255
Hakimi MA, Bochar DA, Schmiesing JA, Dong Y, Barak OG, Speicher DW, Yokomori K, Shiekhattar R (2002) A chromatin remodelling complex that loads cohesin onto human chromosomes. Nature 418:994–998
Hasan S, Stucki M, Hassa PO, Imhof R, Gehrig P, Hunziker P, Hubscher U, Hottiger MO (2001) Regulation of human flap endonuclease-1 activity by acetylation through the transcriptional coactivator p300. Mol Cell 7:1221–1231
Henikoff S, Ahmad K (2005) Assembly of Variant Histones into Chromatin. Annu Rev Cell Dev Biol 21:133–153
Huang J, Hsu JM, Laurent BC (2004) The RSC nucleosome-remodeling complex is required for Cohesin's association with chromosome arms. Mol Cell 13:739–750
Huang Y (2002) Transcriptional silencing in Saccharomyces cerevisiae and Schizosaccharomyces pombe. Nucleic Acids Res 30:1465–1482
Iida T, Araki H (2004) Noncompetitive counteractions of DNA polymerase epsilon and ISW2/yCHRAC for epigenetic inheritance of telomere position effect in Saccharomyces cerevisiae. Mol Cell Biol 24:217–227
Ito T, Bulger M, Pazin MJ, Kobayashi R, Kadonaga JT (1997) ACF, an ISWI-containing and ATP-utilizing chromatin assembly and remodeling factor. Cell 90:145–155
Jaskelioff M, Van Komen S, Krebs JE, Sung P, Peterson CL (2003) Rad54p is a chromatin remodeling enzyme required for heteroduplex DNA joint formation with chromatin. J Biol Chem 278:9212–9218
Kornberg RD, Lorch Y (1999) Twenty-five years of the nucleosome, fundamental particle of the eukaryote chromosome. Cell 98:285–294
Krogan NJ, Keogh MC, Datta N, Sawa C, Ryan OW, Ding H, Haw RA, Pootoolal J, Tong A, Canadien V, Richards DP, Wu X, Emili A, Hughes TR, Buratowski S, Greenblatt JF (2003) A Snf2 family ATPase complex required for recruitment of the histone H2A variant Htz1. Mol Cell 12:1565–1576
Krogh BO, Symington LS (2004) Recombination proteins in yeast. Annu Rev Genet 38:233–271
Kusch T, Florens L, Macdonald WH, Swanson SK, Glaser RL, Yates JR III, Abmayr SM, Washburn MP, Workman JL (2004) Acetylation by Tip60 is required for selective histone variant exchange at DNA lesions. Science 306:2084–2087
Kuzminov A (2001) DNA replication meets genetic exchange: chromosomal damage and its repair by homologous recombination. Proc Natl Acad Sci USA 98:8461–8468
Langst G, Becker PB (2001) Nucleosome mobilization and positioning by ISWI-containing chromatin-remodeling factors. J Cell Sci 114:2561–2568
Lazzaro MA, Picketts DJ (2001) Cloning and characterization of the murine Imitation Switch (ISWI) genes: differential expression patterns suggest distinct developmental roles for Snf2h and Snf2l. J Neurochem 77:1145–1156
LeRoy G, Loyola A, Lane WS, Reinberg D (2000) Purification and characterization of a human factor that assembles and remodels chromatin. J Biol Chem 275:14787–14790
LeRoy G, Orphanides G, Lane WS, Reinberg D (1998) Requirement of RSF and FACT for transcription of chromatin templates in vitro. Science 282:1900–1904
Loyola A, Almouzni G (2004) Histone chaperones, a supporting role in the limelight. Biochim Biophys Acta 1677:3–11
Luger K, Hansen JC (2005) Nucleosome and chromatin fiber dynamics. Curr Opin Struct Biol 15:188–196
Lusser A, Kadonaga JT (2003) Chromatin remodeling by ATP-dependent molecular machines. Bioessays 25:1192–1200
MacCallum DE, Losada A, Kobayashi R, Hirano T (2002) ISWI remodeling complexes in Xenopus egg extracts: identification as major chromosomal components that are regulated by INCENP-aurora B. Mol Biol Cell 13:25–39
Maga G, Hubscher U (2003) Proliferating cell nuclear antigen (PCNA): a dancer with many partners. J Cell Sci 116:3051–3060
McConnell AD, Gelbart ME, Tsukiyama T (2004) Histone fold protein Dls1p is required for Isw2-dependent chromatin remodeling in vivo. Mol Cell Biol 24:2605–2613
McNairn AJ, Gilbert DM (2003) Epigenomic replication: linking epigenetics to DNA replication. Bioessays 25:647–656
Meijsing SH, Ehrenhofer-Murray AE (2001) The silencing complex SAS-I links histone acetylation to the assembly of repressed chromatin by CAF-I and Asf1 in Saccharomyces cerevisiae. Genes Dev 15:3169–3182
Milutinovic S, Zhuang Q, Szyf M (2002) Proliferating cell nuclear antigen associates with histone deacetylase activity, integrating DNA replication and chromatin modification. J Biol Chem 277:20974–20978
Mizuguchi G, Shen X, Landry J, Wu WH, Sen S, Wu C (2004) ATP-driven exchange of histone H2AZ variant catalyzed by SWR1 chromatin remodeling complex. Science 303:343–348
Moore JD, Krebs JE (2004) Histone modifications and DNA double-strand break repair. Biochem Cell Biol 82:446–452
Morrison AJ, Highland J, Krogan NJ, Arbel-Eden A, Greenblatt JF, Haber JE, Shen X (2004) INO80 and gamma-H2AX interaction links ATP-dependent chromatin remodeling to DNA damage repair. Cell 119:767–775
Morrison AJ, Shen X (2005) DNA repair in the context of chromatin. Cell Cycle 4:568–571
O'Donnell AF, Brewster NK, Kurniawan J, Minard LV, Johnston GC, Singer RA (2004) Domain organization of the yeast histone chaperone FACT: the conserved N-terminal domain of FACT subunit Spt16 mediates recovery from replication stress. Nucleic Acids Res 32:5894–5906
Okuhara K, Ohta K, Seo H, Shioda M, Yamada T, Tanaka Y, Dohmae N, Seyama Y, Shibata T, Murofushi H (1999) A DNA unwinding factor involved in DNA replication in cell-free extracts of Xenopus eggs. Curr Biol 9:341–350
Orphanides G, LeRoy G, Chang CH, Luse DS, Reinberg D (1998) FACT, a factor that facilitates transcript elongation through nucleosomes. Cell 92:105–116
Orphanides G, Wu WH, Lane WS, Hampsey M, Reinberg D (1999) The chromatin-specific transcription elongation factor FACT comprises human SPT16 and SSRP1 proteins. Nature 400:284–288
Osada S, Sutton A, Muster N, Brown CE, Yates JR 3rd, Sternglanz R, Workman JL (2001) The yeast SAS (something about silencing) protein complex contains a MYST-type putative acetyltransferase and functions with chromatin assembly factor ASF1. Genes Dev 15:3155–3168
Peterson CL, Laniel MA (2004) Histones and histone modifications. Curr Biol 14:R546–R551
Poot RA, Bozhenok L, van den Berg DL, Hawkes N, Varga-Weisz PD (2005) Chromatin remodeling by WSTF-ISWI at the replication site: opening a window of opportunity for epigenetic inheritance? Cell Cycle 4:543–546
Poot RA, Bozhenok L, van den Berg DL, Steffensen S, Ferreira F, Grimaldi M, Gilbert N, Ferreira J, Varga-Weisz PD (2004) The Williams syndrome transcription factor interacts with PCNA to target chromatin remodelling by ISWI to replication foci. Nat Cell Biol 6:1236–1244
Poot RA, Dellaire G, Hulsmann BB, Grimaldi MA, Corona DF, Becker PB, Bickmore WA, Varga-Weisz PD (2000) HuCHRAC, a human ISWI chromatin remodelling complex contains hACF1 and two novel histone-fold proteins. Embo J 19:3377–3387
Rhoades AR, Ruone S, Formosa T (2004) Structural features of nucleosomes reorganized by yeast FACT and its HMG box component, Nhp6. Mol Cell Biol 24:3907–3917
Riedel CG, Gregan J, Gruber S, Nasmyth K (2004) Is chromatin remodeling required to build sister-chromatid cohesion? Trends Biochem Sci 29:389–392
Santoro R, Grummt I (2005) Epigenetic mechanism of rRNA gene silencing: temporal order of NoRC-mediated histone modification, chromatin remodeling, and DNA methylation. Mol Cell Biol 25:2539–2546
Schalch T, Duda S, Sargent DF, Richmond TJ (2005) X-ray structure of a tetranucleosome and its implications for the chromatin fibre. Nature 436:138–141
Schlesinger MB, Formosa T (2000) POB3 is required for both transcription and replication in the yeast Saccharomyces cerevisiae. Genetics 155:1593–1606
Seo H, Okuhara K, Kurumizaka H, Yamada T, Shibata T, Ohta K, Akiyama T, Murofushi H (2003) Incorporation of DUF/FACT into chromatin enhances the accessibility of nucleosomal DNA. Biochem Biophys Res Commun 303:8–13
Smirnova M, Van Komen S, Sung P, Klein HL (2004) Effects of tumor-associated mutations on Rad54 functions. J Biol Chem 279:24081–24088
Stopka T, Skoultchi AI (2003) The ISWI ATPase Snf2h is required for early mouse development. Proc Natl Acad Sci USA 100:14097–14102
Strohner R, Nemeth A, Jansa P, Hofmann-Rohrer U, Santoro R, Langst G, Grummt I (2001) NoRC— a novel member of mammalian ISWI-containing chromatin remodeling machines. Embo J 20:4892–4900
Suter B, Tong A, Chang M, Yu L, Brown GW, Boone C, Rine J (2004) The origin recognition complex links replication, sister chromatid cohesion and transcriptional silencing in Saccharomyces cerevisiae. Genetics 167:579–591
Tackett AJ, Dilworth DJ, Davey MJ, O'Donnell M, Aitchison JD, Rout MP, Chait BT (2005) Proteomic and genomic characterization of chromatin complexes at a boundary. J Cell Biol 169:35–47
Taddei A, Maison C, Roche D, Almouzni G (2001) Reversible disruption of pericentric heterochromatin and centromere function by inhibiting deacetylases. Nat Cell Biol 3:114–120
Taddei A, Roche D, Sibarita JB, Turner BM, Almouzni G (1999) Duplication and maintenance of heterochromatin domains. J Cell Biol 147:1153–1166
Tan BC, Lee SC (2004) Nek9, a novel FACT-associated protein, modulates interphase progression. J Biol Chem 279:9321–9330
Tan TL, Kanaar R, Wyman C (2003) Rad54, a Jack of all trades in homologous recombination. DNA Repair (Amst) 2:787–794
Tsukiyama T, Palmer J, Landel CC, Shiloach J, Wu C (1999) Characterization of the imitation switch subfamily of ATP-dependent chromatin-remodeling factors in Saccharomyces cerevisiae. Genes Dev 13:686–697
Tsukiyama T, Wu C (1995) Purification and properties of an ATP-dependent nucleosome remodeling factor. Cell 83:1011–1020
van Attikum H, Fritsch O, Hohn B, Gasser SM (2004) Recruitment of the INO80 complex by H2A phosphorylation links ATP-dependent chromatin remodeling with DNA double-strand break repair. Cell 119:777–788
van Attikum H, Gasser SM (2005) ATP-dependent chromatin remodeling and dna double-strand break repair. Cell Cycle 4:1011–1014
Varga-Weisz PD, Wilm M, Bonte E, Dumas K, Mann M, Becker PB (1997) Chromatin-remodelling factor CHRAC contains the ATPases ISWI and topoisomerase II. Nature 388:598–602
Vary JC Jr, Gangaraju VK, Qin J, Landel CC, Kooperberg C, Bartholomew B, Tsukiyama T (2003) Yeast Isw1p forms two separable complexes in vivo. Mol Cell Biol 23:80–91
Vogelauer M, Rubbi L, Lucas I, Brewer BJ, Grunstein M (2002) Histone acetylation regulates the time of replication origin firing. Mol Cell 10:1223–1233
Walfridsson J, Bjerling P, Thalen M, Yoo EJ, Park SD, Ekwall K (2005) The CHD remodeling factor Hrp1 stimulates CENP-A loading to centromeres. Nucleic Acids Res 33:2868–2879
Wiren M, Silverstein RA, Sinha I, Walfridsson J, Lee HM, Laurenson P, Pillus L, Robyr D, Grunstein M, Ekwall K (2005) Genomewide analysis of nucleosome density histone acetylation and HDAC function in fission yeast. Embo J 24:2906–2918
Wittmeyer J, Joss L, Formosa T (1999) Spt16 and Pob3 of Saccharomyces cerevisiae form an essential, abundant heterodimer that is nuclear, chromatin-associated, and copurifies with DNA polymerase alpha. Biochemistry 38:8961–8971
Wu R, Terry AV, Singh PB, Gilbert DM (2005) Differential subnuclear localization and replication timing of histone H3 lysine 9 methylation states. Mol Biol Cell 16:2872–2881
Yamada T, Fischle W, Sugiyama T, Allis CD, Grewal SI (2005) The nucleation and maintenance of heterochromatin by a histone deacetylase in fission yeast. Mol Cell 20:173–185
Yamada T, Okuhara K, Iwamatsu A, Seo H, Ohta K, Shibata T, Murofushi H (2000) p97 ATPase, an ATPase involved in membrane fusion, interacts with DNA unwinding factor (DUF) that functions in DNA replication. FEBS Lett 466:287–291
Yasui D, Miyano M, Cai S, Varga-Weisz P, Kohwi-Shigematsu T (2002) SATB1 targets chromatin remodelling to regulate genes over long distances. Nature 419:641–645
Zhou J, Chau CM, Deng Z, Shiekhattar R, Spindler MP, Schepers A, Lieberman PM (2005) Cell cycle regulation of chromatin at an origin of DNA replication. Embo J 24:1406–1417
Zhou Y, Wang TS (2004) A coordinated temporal interplay of nucleosome reorganization factor, sister chromatin cohesion factor, and DNA polymerase alpha facilitates DNA replication. Mol Cell Biol 24:9568–9579
Acknowledgments
We thank Tom Sexton for constructive criticism of this manuscript. ANC is funded by Fundação para a Ciência e Tecnologia. Work in the Varga-Weisz laboratory is funded by the Biotechnology and Biosciences Research Council, the Association for International Cancer Research, St. Andrews (AICR) and the European Network of Excellence (NoE).
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Neves-Costa, A., Varga-Weisz, P. The Roles of Chromatin Remodelling Factors in Replication. In: Laurent, B.C. (eds) Chromatin Dynamics in Cellular Function. Results and Problems in Cell Differentiation, vol 41. Springer, Berlin, Heidelberg. https://doi.org/10.1007/400_007
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