Histones, histone chaperones and nucleosome assembly

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.

[1]  R. Marmorstein,et al.  Histone acetyltransferases: function, structure, and catalysis. , 2001, Current opinion in genetics & development.

[2]  Junhong Han,et al.  Rtt109 Acetylates Histone H3 Lysine 56 and Functions in DNA Replication , 2007, Science.

[3]  J. Tyler.  Chromatin assembly. Cooperation between histone chaperones and ATP-dependent nucleosome remodeling machines. , 2002, European journal of biochemistry.

[4]  James A Tarara,et al.  A novel role for histone chaperones CAF‐1 and Rtt106p in heterochromatin silencing , 2007, The EMBO journal.

[5]  Erich A Nigg,et al.  Human Asf1 and CAF‐1 interact and synergize in a repair‐coupled nucleosome assembly pathway , 2002, EMBO reports.

[6]  R. Chalkley,et al.  Modifications to histones immediately after synthesis. , 1976, Journal of molecular biology.

[7]  M. Churchill,et al.  Structural Basis for the Histone Chaperone Activity of Asf1 , 2006, Cell.

[8]  Robert Driscoll,et al.  Yeast Rtt109 Promotes Genome Stability by Acetylating Histone H3 on Lysine 56 , 2007, Science.

[9]  M. Parthun,et al.  The nuclear Hat1p/Hat2p complex: a molecular link between type B histone acetyltransferases and chromatin assembly. , 2004, Molecular cell.

[10]  Kirk C. Hansen,et al.  CBP / p300-mediated acetylation of histone H3 on lysine 56 , 2009, Nature.

[11]  C. Allis,et al.  The language of covalent histone modifications , 2000, Nature.

[12]  S. Jackson,et al.  Screen for DNA-damage-responsive histone modifications identifies H 3 K 9 Ac and H 3 K 56 Ac in human cells , 2009 .

[13]  J. Tyler,et al.  Chaperoning Histones during DNA Replication and Repair , 2010, Cell.

[14]  C. Allis,et al.  Conservation of deposition-related acetylation sites in newly synthesized histones H3 and H4. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[15]  T. Formosa,et al.  The structure of the yFACT Pob3-M domain, its interaction with the DNA replication factor RPA, and a potential role in nucleosome deposition. , 2006, Molecular cell.

[16]  R. Sternglanz,et al.  Two New S‐Phase‐Specific Genes from Saccharomyces cerevisiae , 1997, Yeast.

[17]  C. Allis,et al.  Epigenetics: A Landscape Takes Shape , 2007, Cell.

[18]  A. Hamiche,et al.  The death-associated protein DAXX is a novel histone chaperone involved in the replication-independent deposition of H3.3. , 2010, Genes & development.

[19]  M. Grunstein,et al.  Deposition-related sites K5/K12 in histone H4 are not required for nucleosome deposition in yeast. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[20]  Jeffrey G. Linger,et al.  The Yeast Histone Chaperone Chromatin Assembly Factor 1 Protects Against Double-Strand DNA-Damaging Agents , 2005, Genetics.

[21]  B. Garcia,et al.  Histone chaperone Asf1 is required for histone H3 lysine 56 acetylation, a modification associated with S phase in mitosis and meiosis. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[22]  M. Grunstein,et al.  Functions of site-specific histone acetylation and deacetylation. , 2007, Annual review of biochemistry.

[23]  S. Henikoff,et al.  Histone H3 variants specify modes of chromatin assembly , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[24]  Zhiguo Zhang,et al.  Histone H3-K56 acetylation is important for genomic stability in mammals , 2009, Cell cycle.

[25]  Axel Imhof,et al.  PTMs on H3 variants before chromatin assembly potentiate their final epigenetic state. , 2006, Molecular cell.

[26]  R. Kornberg,et al.  Twenty-Five Years of the Nucleosome, Fundamental Particle of the Eukaryote Chromosome , 1999, Cell.

[27]  G. Almouzni,et al.  Replication stress interferes with histone recycling and predeposition marking of new histones. , 2010, Molecular cell.

[28]  R. Marmorstein.  Structural and chemical basis of histone acetylation. , 2004, Novartis Foundation symposium.

[29]  M. Curcio,et al.  Multiple regulators of Ty1 transposition in Saccharomyces cerevisiae have conserved roles in genome maintenance. , 2001, Genetics.

[30]  J. Bartek,et al.  Regulation of Replication Fork Progression Through Histone Supply and Demand , 2007, Science.

[31]  M. Grunstein,et al.  25 years after the nucleosome model: chromatin modifications. , 2000, Trends in biochemical sciences.

[32]  Jeffrey G. Linger,et al.  Acetylated Lysine 56 on Histone H3 Drives Chromatin Assembly after Repair and Signals for the Completion of Repair , 2008, Cell.

[33]  B M Turner,et al.  Histone acetylation and an epigenetic code. , 2000, BioEssays : news and reviews in molecular, cellular and developmental biology.

[34]  Junhong Han,et al.  A role for Gcn5 in replication-coupled nucleosome assembly. , 2010, Molecular cell.

[35]  David Hawke,et al.  A role for cell-cycle-regulated histone H3 lysine 56 acetylation in the DNA damage response , 2005, Nature.

[36]  V. Allfrey,et al.  Processing of newly synthesized histone molecules , 1975, Science.

[37]  Zhiguo Zhang,et al.  Chromatin assembly factor 1 interacts with histone H3 methylated at lysine 79 in the processes of epigenetic silencing and DNA repair. , 2006, Biochemistry.

[38]  R. Kobayashi,et al.  Interaction between the DrosophilaCAF-1 and ASF1 Chromatin Assembly Factors , 2001, Molecular and Cellular Biology.

[39]  Walter Rocha,et al.  Clothing up DNA for all seasons: Histone chaperones and nucleosome assembly pathways , 2008, FEBS letters.

[40]  T. Hughes,et al.  Two-color cell array screen reveals interdependent roles for histone chaperones and a chromatin boundary regulator in histone gene repression. , 2009, Molecular cell.

[41]  R. Kobayashi,et al.  Ultraviolet radiation sensitivity and reduction of telomeric silencing in Saccharomyces cerevisiae cells lacking chromatin assembly factor-I. , 1997, Genes & development.

[42]  E. Paquet,et al.  The Rtt106 Histone Chaperone Is Functionally Linked to Transcription Elongation and Is Involved in the Regulation of Spurious Transcription from Cryptic Promoters in Yeast*♦ , 2008, Journal of Biological Chemistry.

[43]  Ryuji Kobayashi,et al.  The RCAF complex mediates chromatin assembly during DNA replication and repair , 1999, Nature.

[44]  Zhiguo Zhang,et al.  Rtt106p is a histone chaperone involved in heterochromatin-mediated silencing. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[45]  Xuetong Shen,et al.  Chromatin remodeling in DNA replication , 2006, Journal of cellular biochemistry.

[46]  R. Kobayashi,et al.  Nucleosome Assembly by a Complex of CAF-1 and Acetylated Histones H3/H4 , 1996, Cell.

[47]  Zhiguo Zhang,et al.  Acetylation of Histone H3 Lysine 56 Regulates Replication-Coupled Nucleosome Assembly , 2008, Cell.

[48]  T. Richmond,et al.  Crystal structure of the nucleosome core particle at 2.8 Å resolution , 1997, Nature.

[49]  G. Almouzni,et al.  Histone H3.1 and H3.3 Complexes Mediate Nucleosome Assembly Pathways Dependent or Independent of DNA Synthesis , 2004, Cell.

[50]  C. Allis,et al.  Histone acetyltransferases. , 2001, Annual review of biochemistry.

[51]  Zhiguo Zhang,et al.  The Elongator Complex Interacts with PCNA and Modulates Transcriptional Silencing and Sensitivity to DNA Damage Agents , 2009, PLoS genetics.

[52]  Y. Park,et al.  Nucleosome structure and function. , 2006, Ernst Schering Research Foundation workshop.

[53]  Jacques Côté,et al.  The diverse functions of histone acetyltransferase complexes. , 2003, Trends in genetics : TIG.

[54]  B. Stillman.  Chromatin assembly during SV40 DNA replication in vitro , 1986, Cell.

[55]  David P. Toczyski,et al.  Complicated Tails: Histone Modifications and the DNA Damage Response , 2005, Cell.

[56]  C. Allis,et al.  Translating the Histone Code , 2001, Science.

[57]  B. Stillman,et al.  Replication-Dependent Marking of DNA by PCNA Facilitates CAF-1-Coupled Inheritance of Chromatin , 1999, Cell.