Abstract
Genetic information embedded in DNA sequence and the epigenetic information marked by modifications on DNA and histones are essential for the life of eukaryotes. Cells have evolved mechanisms of DNA duplication and chromatin restoration to ensure the inheritance of genetic and epigenetic information during cell division and development. In this review, we focus on the maintenance of epigenetic landscape during chromatin dynamics which requires the orchestration of histones and their chaperones. We discuss how epigenetic marks are re-established in the assembly of new chromatin after DNA replication and repair, highlighting the roles of CAF-1 in the process of changing chromatin state. The functions of CAF-1 provide a link between chromatin assembly and epigenetic restoration.
Article PDF
Similar content being viewed by others
References
Richmond T J, Finch J T, Rushton B, et al. Structure of the nucleosome core particle at 7 Å resolution. Nature, 1984, 311: 532–537
Kornberg R D, Thomas J O. Chromatin structure: oligomers of the histones. Science, 1974, 184: 865–868
Noll M, Kornberg R D. Action of micrococcal nuclease on chromatin and the location of histone H1. J Mol Biol, 1977, 109: 393–404
Luger K, Mader A W, Richmond R K, et al. Crystal structure of the nucleosome core particle at 2.8 Å resolution. Nature, 1997, 389: 251–260
Robinson P J, Fairall L, Huynh V A, et al. EM measurements define the dimensions of the “30-nm” chromatin fiber: evidence for a compact, interdigitated structure. Proc Natl Acad Sci USA, 2006, 103: 6506–6511
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: 403–427
Finch J T, Klug A. Solenoidal model for superstructure in chromatin. Proc Natl Acad Sci USA, 1976, 73: 1897–1901
Robinson P J, Rhodes D. Structure of the ‘30 nm’ chromatin fibre: a key role for the linker histone. Curr Opin Struct Biol, 2006, 16: 336–343
Mello J A, Sillje H H, Roche D M, et al. Human Asf1 and CAF-1 interact and synergize in a repair-coupled nucleosome assembly pathway. EMBO Rep, 2002, 3: 329–334
Kirov N, Shtilbans A, Rushlow C. Isolation and characterization of a new gene encoding a member of the HIRA family of proteins from Drosophila melanogaster. Gene, 1998, 212: 323–332
Monson E K, de Bruin D, Zakian V A. The yeast Cac1 protein is required for the stable inheritance of transcriptionally repressed chromatin at telomeres. Proc Natl Acad Sci USA, 1997, 94: 13081–13086
Smith S, Stillman B. Purification and characterization of CAF-I, a human cell factor required for chromatin assembly during DNA replication in vitro. Cell, 1989, 58: 15–25
Shibahara K, Stillman B. Replication-dependent marking of DNA by PCNA facilitates CAF-1-coupled inheritance of chromatin. Cell, 1999, 96: 575–585
Krude T. Chromatin assembly during DNA replication in somatic cells. Eur J Biochem, 1999, 263: 1–5
Song Y, He F, Xie G, et al. CAF-1 is essential for Drosophila development and involved in the maintenance of epigenetic memory. Dev Biol, 2007, 311: 213–222
Chen Z, Tan J L, Ingouff M, et al. Chromatin assembly factor 1 regulates the cell cycle but not cell fate during male gametogenesis in Arabidopsis thaliana. Development, 2008, 135: 65–73
Myung K, Pennaneach V, Kats E S, et al. Saccharomyces cerevisiae chromatin-assembly factors that act during DNA replication function in the maintenance of genome stability. Proc Natl Acad Sci USA, 2003, 100: 6640–6645
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
Takami Y, Ono T, Fukagawa T, et al. Essential role of chromatin assembly factor-1-mediated rapid nucleosome assembly for DNA replication and cell division in vertebrate cells. Mol Biol Cell, 2007, 18: 129–141
Worcel A, Han S, Wong M L. Assembly of newly replicated chromatin. Cell, 1978, 15: 969–977
Cremisi C, Yaniv M. Sequential assembly of newly synthesized histones on replicating SV40 DNA. Biochem Biophys Res Commun, 1980, 92: 1117–1123
Gruss C, Wu J, Koller T, et al. Disruption of the nucleosomes at the replication fork. EMBO J, 1993, 12: 4533–4545
Gasser R, Koller T, Sogo J M. The stability of nucleosomes at the replication fork. J Mol Biol, 1996, 258: 224–239
Smith S, Stillman B. Stepwise assembly of chromatin during DNA replication in vitro. EMBO J, 1991, 10: 971–980
Enomoto S, Berman J. Chromatin assembly factor I contributes to the maintenance, but not the re-establishment, of silencing at the yeast silent mating loci. Genes Dev, 1998, 12: 219–232
Taddei A, Roche D, Sibarita J B, et al. Duplication and maintenance of heterochromatin domains. J Cell Biol, 1999, 147: 1153–1166
Verreault A, Kaufman P D, Kobayashi R, et al. Nucleosome assembly by a complex of CAF-1 and acetylated histones H3/H4. Cell, 1996, 87: 95–104
Sobel R E, Cook R G, Perry C A, et al. Conservation of deposition-related acetylation sites in newly synthesized histones H3 and H4. Proc Natl Acad Sci USA, 1995, 92: 1237–1241
Das C, Lucia M S, Hansen K C, et al. CBP/p300-mediated acetylation of histone H3 on lysine 56. Nature, 2009, 459: 113–117
Zhang Z, Shibahara K, Stillman B. PCNA connects DNA replication to epigenetic inheritance in yeast. Nature, 2000, 408: 221–225
Tyler J K, Adams C R, Chen S R, et al. The RCAF complex mediates chromatin assembly during DNA replication and repair. Nature, 1999, 402: 555–560
Tyler J K, Collins K A, Prasad-Sinha J, et al. Interaction between the Drosophila CAF-1 and ASF1 chromatin assembly factors. Mol Cell Biol, 2001, 21: 6574–6584
Krawitz D C, Kama T, Kaufman P D. Chromatin assembly factor I mutants defective for PCNA binding require Asf1/Hir proteins for silencing. Mol Cell Biol, 2002, 22: 614–625
Xu M, Long C, Chen X, et al. Partitioning of histone H3-H4 tetramers during DNA replication-dependent chromatin assembly. Science, 2010, 328: 94–98
Ahmad K, Henikoff S. The histone variant H3.3 marks active chromatin by replication-independent nucleosome assembly. Mol Cell, 2002, 9: 1191–1200
Hake S B, Garcia B A, Duncan E M, et al. Expression patterns and post-translational modifications associated with mammalian histone H3 variants. J Biol Chem, 2006, 281: 559–568
Mito Y, Henikoff J G, Henikoff S. Genome-scale profiling of histone H3.3 replacement patterns. Nat Genet, 2005, 37: 1090–1097
Loyola A, Bonaldi T, Roche D, et al. PTMs on H3 variants before chromatin assembly potentiate their final epigenetic state. Mol Cell, 2006, 24: 309–316
Quivy J P, Roche D, Kirschner D, et al. A CAF-1 dependent pool of HP1 during heterochromatin duplication. EMBO J, 2004, 23: 3516–3526
Tagami H, Ray-Gallet D, Almouzni G, et al. Histone H3.1 and H3.3 complexes mediate nucleosome assembly pathways dependent or independent of DNA synthesis. Cell, 2004, 116: 51–61
Dohke K, Miyazaki S, Tanaka K, et al. Fission yeast chromatin assembly factor 1 assists in the replication-coupled maintenance of heterochromatin. Genes Cells, 2008, 13: 1027–1043
Houlard M, Berlivet S, Probst A V, et al. CAF-1 is essential for heterochromatin organization in pluripotent embryonic cells. PLoS Genet, 2006, 2: e181
Huang H, Yu Z, Zhang S, et al. Drosophila CAF-1 regulates HP1-mediated epigenetic silencing and pericentric heterochromatin stability. J Cell Sci, 2010, 123: 2853–2861
Clark R F, Elgin S C. Heterochromatin protein 1, a known suppressor of position-effect variegation, is highly conserved in Drosophila. Nucleic Acids Res, 1992, 20: 6067–6074
Schotta G, Lachner M, Sarma K, et al. A silencing pathway to induce H3-K9 and H4-K20 trimethylation at constitutive heterochromatin. Genes Dev, 2004, 18: 1251–1262
Murzina N, Verreault A, Laue E, et al. Heterochromatin dynamics in mouse cells: interaction between chromatin assembly factor 1 and HP1 proteins. Mol Cell, 1999, 4: 529–540
Anderson A E, Karandikar U C, Pepple K L, et al. The enhancer of trithorax and polycomb gene Caf1/p55 is essential for cell survival and patterning in Drosophila development. Development, 2011, 138: 1957–1966
Nabatiyan A, Szuts D, Krude T. Induction of CAF-1 expression in response to DNA strand breaks in quiescent human cells. Mol Cell Biol, 2006, 26: 1839–1849
Polo S E, Roche D, Almouzni G. New histone incorporation marks sites of UV repair in human cells. Cell, 2006, 127: 481–493
Chen C C, Carson J J, Feser J, et al. Acetylated lysine 56 on histone H3 drives chromatin assembly after repair and signals for the completion of repair. Cell, 2008, 134: 231–243
Li Q, Zhou H, Wurtele H, et al. Acetylation of histone H3 lysine 56 regulates replication-coupled nucleosome assembly. Cell, 2008, 134: 244–255
Zhang D, Wang D, Sun F. Drosophila melanogaster heterochromatin protein HP1b plays important roles in transcriptional activation and development. Chromosoma, 2011, 120: 97–108
Li Y, Danzer J R, Alvarez P, et al. Effects of tethering HP1 to euchromatic regions of the Drosophila genome. Development, 2003, 130: 1817–1824
Schwaiger M, Kohler H, Oakeley E J, et al. Heterochromatin protein 1 (HP1) modulates replication timing of the Drosophila genome. Genome Res, 2010, 20: 771–780
Hwang K K, Eissenberg J C, Worman H J. Transcriptional repression of euchromatic genes by Drosophila heterochromatin protein 1 and histone modifiers. Proc Natl Acad Sci USA, 2001, 98: 11423–11427
Luijsterburg M S, Dinant C, Lans H, et al. Heterochromatin protein 1 is recruited to various types of DNA damage. J Cell Biol, 2009, 185: 577–586
Baldeyron C, Soria G, Roche D, et al. HP1α recruitment to DNA damage by p150CAF-1 promotes homologous recombination repair. J Cell Biol, 2011, 193: 81–95
Jiao R, Bachrati C Z, Pedrazzi G, et al. Physical and functional interaction between the Bloom’s syndrome gene product and the largest subunit of chromatin assembly factor 1. Mol Cell Biol, 2004, 24: 4710–4719
Jiao R, Harrigan J A, Shevelev I, et al. The Werner syndrome protein is required for recruitment of chromatin assembly factor 1 following DNA damage. Oncogene, 2007, 26: 3811–3822
Moggs J G, Grandi P, Quivy J P, et al. A CAF-1-PCNA-mediated chromatin assembly pathway triggered by sensing DNA damage. Mol Cell Biol, 2000, 20: 1206–1218
Grewal S I, Elgin S C. Transcription and RNA interference in the formation of heterochromatin. Nature, 2007, 447: 399–406
Shermoen A W, McCleland M L, O’Farrell P H. Developmental control of late replication and S phase length. Curr Biol, 2010, 20: 2067–2077
Quivy J P, Gerard A, Cook A J, et al. The HP1-p150/CAF-1 interaction is required for pericentric heterochromatin replication and S-phase progression in mouse cells. Nat Struct Mol Biol, 2008, 15: 972–979
Turner B M. Cellular memory and the histone code. Cell, 2002, 111: 285–291
Lusser A, Kadonaga J T. Chromatin remodeling by ATP-dependent molecular machines. Bioessays, 2003, 25: 1192–1200
Fischle W, Wang Y, Allis C D. Histone and chromatin cross-talk. Curr Opin Cell Biol, 2003, 15: 172–183
Goodfellow H, Krejci A, Moshkin Y, et al. Gene-specific targeting of the histone chaperone asf1 to mediate silencing. Dev Cell, 2007, 13: 593–600
Moshkin Y M, Kan T W, Goodfellow H, et al. Histone chaperones ASF1 and NAP1 differentially modulate removal of active histone marks by LID-RPD3 complexes during NOTCH silencing. Mol Cell, 2009, 35: 782–793
Badenhorst P, Xiao H, Cherbas L, et al. The Drosophila nucleosome remodeling factor NURF is required for Ecdysteroid signaling and metamorphosis. Genes Dev, 2005, 19: 2540–2545
Song H, Spichiger-Haeusermann C, Basler K. The ISWI-containing NURF complex regulates the output of the canonical Wingless pathway. EMBO Rep, 2009, 10: 1140–1146
Kugler S J, Nagel A C. A novel Pzg-NURF complex regulates Notch target gene activity. Mol Biol Cell, 2010, 21: 3443–3448
Kugler S J, Gehring E M, Wallkamm V, et al. The Putzig-NURF nucleosome remodeling complex is required for ecdysone receptor signaling and innate immunity in Drosophila melanogaster. Genetics, 2011, 188: 127–139
Kim H J, Seol J H, Cho E J. Potential role of the histone chaperone, CAF-1, in transcription. BMB Rep, 2009, 42: 227–231
Li G, Margueron R, Hu G, et al. Highly compacted chromatin formed in vitro reflects the dynamics of transcription activation in vivo. Mol Cell, 2010, 38: 41–53
Author information
Authors and Affiliations
Corresponding author
Additional information
This article is published with open access at Springerlink.com
Rights and permissions
Open Access This article is distributed under the terms of the Creative Commons Attribution 2.0 International License (https://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
About this article
Cite this article
Huang, H., Jiao, R. Roles of chromatin assembly factor 1 in the epigenetic control of chromatin plasticity. Sci. China Life Sci. 55, 15–19 (2012). https://doi.org/10.1007/s11427-012-4269-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11427-012-4269-z