Trends in Cell Biology
Volume 19, Issue 1, January 2009, Pages 29-41
Journal home page for Trends in Cell Biology

Review
Feature Review
Making copies of chromatin: the challenge of nucleosomal organization and epigenetic information

https://doi.org/10.1016/j.tcb.2008.10.002Get rights and content

Understanding the basic mechanisms underlying chromatin dynamics during DNA replication in eukaryotic cells is of fundamental importance. Beyond DNA compaction, chromatin organization represents a means to regulate genome function. Thus, the inheritance and maintenance of the DNA sequence, along with its organization into chromatin, is central for eukaryotic life. To orchestrate DNA replication in the context of chromatin is a challenge, both in terms of accessibility to the compact structures and maintenance of chromatin organization. To meet the challenge of maintenance, cells have evolved efficient nucleosome dynamics involving assembly pathways and chromatin maturation mechanisms that restore chromatin organization in the wake of DNA replication. In this review, we describe our current knowledge concerning how these pathways operate at the nucleosomal level and highlight the key players, such as histone chaperones, chromatin remodelers or modifiers, involved in the process of chromatin duplication. Major advances have been made recently concerning de novo nucleosome assembly and our understanding of its coordination with recycling of parental histones is progressing. Insights into the transmission of chromatin-based information during replication have important implications in the field of epigenetics to fully comprehend how the epigenetic landscape might, or at times might not, be stably maintained in the face of dramatic changes in chromatin structure.

Section snippets

Replication in a chromatin context: the basic issues and principles

Over the past years, numerous biological phenomena ranging from position effect variegation in the fruit fly Drosophila melanogaster, to X chromosome inactivation in mammals, genomic imprinting, centromere function and gene silencing have coalesced into the field of epigenetics. Mechanisms underlying these intriguing phenomena cannot be explained by classical genetics but instead rely on the establishment and faithful maintenance of specific chromatin structures. This raises the issue of how a

De novo deposition of histones

Replicative histones produced during S phase [8] ensure a provision of new histones to fulfill the requirement for nucleosome assembly on the two daughter strands in the wake of the replication fork. The existence of regulatory systems to control histone levels both at the transcriptional or post-transcriptional level 8, 9 is crucial to avoid the deleterious effects of excess histones, such as impaired replication or chromosome loss 10, 11, 12. In addition to the set of canonical ‘replicative’

Factors involved in disruption and recycling of parental nucleosomes

By analogy to transcription, chromatin remodeling factors have been implicated in altering chromatin structure to help progression of the replication fork. Depletion experiments have highlighted their specific contribution to chromatin duplication. ATP-utilizing chromatin assembly and remodeling factor (ACF), comprising the two subunits ACF1 and imitation SWItch (ISWI), is required for efficient replication through heterochromatic dense regions in mouse cells [49]. Furthermore, Williams

How do epigenetic marks get duplicated?

Beyond the genetic information encoded into DNA, histone PTMs and DNA methylation provide an extra layer of information that is termed ‘epigenetic’ when it is stably inherited throughout cell generations. Thus, whether these marks can be considered as epigenetic requires assessment of whether they are perpetuated during DNA and chromatin duplication or whether there are any means to ensure their stable propagation through multiple cell divisions. DNA methylation occurs on cytosine at CpG

Concluding remarks and future perspectives

In eukaryotic cells, chromatin duplication entails a series of complex and coordinated events, including nucleosomal disruption, histone transfer and deposition, along with dynamic histone modifications, that ultimately give rise to particular marks in defined chromatin regions. Here, we have emphasized the possible roles of chromatin remodelers, histone modifiers and histone chaperones in chromatin duplication, both at the level of histone dynamics and during re-establishment of marks that

Acknowledgements

We apologize to authors whose work could not be cited owing to space limitations. We thank A. Cook, E. Dunleavy and J. Show for their input. A.C. is supported by a PhD fellowship from Université Paris 6. G.A. is a recipient of grants from la Ligue Nationale contre le Cancer (Equipe labellisée la Ligue), PIC Programs (‘Retinoblastome and ‘Replication, Instabilite chromosomique et cancer’), the European Commission Network of Excellence Epigenome (LSHG-CT-2004–503433), ACI-2007-Cancéropôle IdF

References (136)

  • R.D. Kornberg

    Chromatin structure: a repeating unit of histones and DNA

    Science

    (1974)
  • K. Luger

    Crystal structure of the nucleosome core particle at 2.8 A resolution

    Nature

    (1997)
  • A. Loyola et al.

    Marking histone H3 variants: how, when and why?

    Trends Biochem. Sci.

    (2007)
  • A. Groth

    Chromatin challenges during DNA replication and repair

    Cell

    (2007)
  • A. Saha

    Chromatin remodelling: the industrial revolution of DNA around histones

    Nat. Rev. Mol. Cell Biol.

    (2006)
  • L. De Koning

    Histone chaperones: an escort network regulating histone traffic

    Nat. Struct. Mol. Biol.

    (2007)
  • T. Kouzarides

    Chromatin modifications and their function

    Cell

    (2007)
  • W.F. Marzluff et al.

    Histone mRNA expression: multiple levels of cell cycle regulation and important developmental consequences

    Curr. Opin. Cell Biol.

    (2002)
  • A. Gunjan

    Regulation of histone synthesis and nucleosome assembly

    Biochimie

    (2005)
  • A. Groth

    Regulation of replication fork progression through histone supply and demand

    Science

    (2007)
  • A. Gunjan et al.

    A Rad53 kinase-dependent surveillance mechanism that regulates histone protein levels in S. cerevisiae

    Cell

    (2003)
  • D. Meeks-Wagner et al.

    Normal stoichiometry of histone dimer sets is necessary for high fidelity of mitotic chromosome transmission

    Cell

    (1986)
  • R.A. Laskey

    Assembly of SV40 chromatin in a cell-free system from Xenopus eggs

    Cell

    (1977)
  • B. Stillman

    Chromatin assembly during SV40 DNA replication in vitro

    Cell

    (1986)
  • S. Smith et al.

    Purification and characterization of CAF-I, a human cell factor required for chromatin assembly during DNA replication in vitro

    Cell

    (1989)
  • P.D. Kaufman

    The p150 and p60 subunits of chromatin assembly factor I: a molecular link between newly synthesized histones and DNA replication

    Cell

    (1995)
  • A. Verreault

    Nucleosome assembly by a complex of CAF-1 and acetylated histones H3/H4

    Cell

    (1996)
  • J.J. Song

    Structural basis of histone H4 recognition by p55

    Genes Dev.

    (2008)
  • J.G. Moggs

    A CAF-1-PCNA-mediated chromatin assembly pathway triggered by sensing DNA damage

    Mol. Cell. Biol.

    (2000)
  • K. Shibahara et al.

    Replication-dependent marking of DNA by PCNA facilitates CAF-1-coupled inheritance of chromatin

    Cell

    (1999)
  • A. Gerard

    The replication kinase Cdc7-Dbf4 promotes the interaction of the p150 subunit of chromatin assembly factor 1 with proliferating cell nuclear antigen

    EMBO Rep.

    (2006)
  • M. Houlard

    CAF-1 is essential for heterochromatin organization in pluripotent embryonic cells

    PLoS Genet.

    (2006)
  • J.P. Quivy

    Dimerization of the largest subunit of chromatin assembly factor 1: importance in vitro and during Xenopus early development

    EMBO J.

    (2001)
  • Y. Song

    CAF-1 is essential for Drosophila development and involved in the maintenance of epigenetic memory

    Dev. Biol.

    (2007)
  • M. Hoek et al.

    Chromatin assembly factor 1 is essential and couples chromatin assembly to DNA replication in vivo

    Proc. Natl. Acad. Sci. U. S. A.

    (2003)
  • S. Le

    Two new S-phase-specific genes from Saccharomyces cerevisiae

    Yeast

    (1997)
  • J.K. Tyler

    The RCAF complex mediates chromatin assembly during DNA replication and repair

    Nature

    (1999)
  • J.A. Mello

    Human Asf1 and CAF-1 interact and synergize in a repair-coupled nucleosome assembly pathway

    EMBO Rep.

    (2002)
  • A.D. Malay

    Crystal structures of fission yeast histone chaperone Asf1 complexed with the Hip1 B-domain or the Cac2 C terminus

    J. Biol. Chem.

    (2008)
  • F. Sanematsu

    Asf1 is required for viability and chromatin assembly during DNA replication in vertebrate cells

    J. Biol. Chem.

    (2006)
  • Y. Tang

    Structure of a human ASF1a-HIRA complex and insights into specificity of histone chaperone complex assembly

    Nat. Struct. Mol. Biol.

    (2006)
  • J.K. Tyler

    Interaction between the Drosophila CAF-1 and ASF1 chromatin assembly factors

    Mol. Cell. Biol.

    (2001)
  • C.M. English

    Structural basis for the histone chaperone activity of Asf1

    Cell

    (2006)
  • R. Natsume

    Structure and function of the histone chaperone CIA/ASF1 complexed with histones H3 and H4

    Nature

    (2007)
  • A.D. Baxevanis

    Associative behavior of the histone (H3-H4)2 tetramer: dependence on ionic environment

    Biochemistry

    (1991)
  • H. Tagami

    Histone H3, 1 and H3. 3 complexes mediate nucleosome assembly pathways dependent or independent of DNA synthesis

    Cell

    (2004)
  • Y. Dalal

    Tetrameric structure of centromeric nucleosomes in interphase Drosophila cells

    PLoS Biol.

    (2007)
  • C.M. English

    ASF1 binds to a heterodimer of histones H3 and H4: a two-step mechanism for the assembly of the H3-H4 heterotetramer on DNA

    Biochemistry

    (2005)
  • F. Mousson

    The histone chaperone Asf1 at the crossroads of chromatin and DNA checkpoint pathways

    Chromosoma

    (2007)
  • D. Ray-Gallet

    The histone chaperone Asf1 is dispensable for direct de novo histone deposition in Xenopus egg extracts

    Chromosoma

    (2007)
  • J. Zlatanova

    Nap1: taking a closer look at a juggler protein of extraordinary skills

    FASEB J.

    (2007)
  • H. Kimura et al.

    Kinetics of core histones in living human cells: little exchange of H3 and H4 and some rapid exchange of H2B

    J. Cell Biol.

    (2001)
  • R. Gasser

    The stability of nucleosomes at the replication fork

    J. Mol. Biol.

    (1996)
  • J.M. Sogo

    Structure of replicating simian virus 40 minichromosomes. The replication fork, core histone segregation and terminal structures

    J. Mol. Biol.

    (1986)
  • A.T. Annunziato

    Split decision: what happens to nucleosomes during DNA replication?

    J. Biol. Chem.

    (2005)
  • B. Vestner

    Histone octamer dissociation is not required for in vitro replication of simian virus 40 minichromosomes

    J. Biol. Chem.

    (2000)
  • C. Gruss

    Disruption of the nucleosomes at the replication fork

    EMBO J.

    (1993)
  • S.K. Randall et al.

    The fate of parental nucleosomes during SV40 DNA replication

    J. Biol. Chem.

    (1992)
  • N. Collins

    An ACF1-ISWI chromatin-remodeling complex is required for DNA replication through heterochromatin

    Nat. Genet.

    (2002)
  • R.A. Poot

    The Williams syndrome transcription factor interacts with PCNA to target chromatin remodelling by ISWI to replication foci

    Nat. Cell Biol.

    (2004)
  • Cited by (126)

    • Delayed Accumulation of H3K27me3 on Nascent DNA Is Essential for Recruitment of Transcription Factors at Early Stages of Stem Cell Differentiation

      2017, Molecular Cell
      Citation Excerpt :

      How any transcription factor overcomes the barrier of the most condensed chromatin to bind to DNA and to change transcriptional programs during cell differentiation is not well established. However, it is thought that the chromatin structure is disrupted and then re-assembled following DNA replication (Bonasio et al., 2010; Corpet and Almouzni, 2009). Therefore, we examined whether, during the early periods after DNA replication, the structure of chromatin that is formed on nascent DNA may provide an opportunity for newly induced transcription factors to overcome the barrier of condensed chromatin and associate with their target sites on DNA.

    View all citing articles on Scopus
    View full text