Chaperoning Histones during DNA Replication and Repair

Nuclear DNA is tightly packaged into chromatin, which profoundly influences DNA replication, transcription, repair, and recombination. The extensive interactions between the basic histone proteins and acidic DNA make the nucleosomal unit of chromatin a highly stable entity. For the cellular machinery to access the DNA, the chromatin must be unwound and the DNA cleared of histone proteins. Conversely, the DNA has to be repackaged into chromatin afterward. This review focuses on the roles of the histone chaperones in assembling and disassembling chromatin during the processes of DNA replication and repair.

[1]  S. Jentsch,et al.  Chromosome-wide Rad51 spreading and SUMO-H2A.Z-dependent chromosome fixation in response to a persistent DNA double-strand break. , 2009, Molecular cell.

[2]  B. Stillman,et al.  Purification and characterization of CAF-I, a human cell factor required for chromatin assembly during DNA replication in vitro , 1989, Cell.

[3]  J. Tyler,et al.  The histone chaperone ASF1 localizes to active DNA replication forks to mediate efficient DNA replication , 2006, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[4]  B. Maier-Davis,et al.  Chromatin remodeling by nucleosome disassembly in vitro. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[5]  Virgil L. Woods,et al.  An epigenetic mark generated by the incorporation of CENP-A into centromeric nucleosomes , 2007, Proceedings of the National Academy of Sciences.

[6]  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.

[7]  T. Krude Chromatin assembly factor 1 (CAF-1) colocalizes with replication foci in HeLa cell nuclei. , 1995, Experimental cell research.

[8]  S. Jackson,et al.  DNA helicases Sgs1 and BLM promote DNA double-strand break resection. , 2008, Genes & development.

[9]  C. Akey,et al.  The crystal structure of nucleoplasmin-core: implications for histone binding and nucleosome assembly. , 2001, Molecular cell.

[10]  J. Yates,et al.  Centromere-Specific Assembly of CENP-A Nucleosomes Is Mediated by HJURP , 2009, Cell.

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

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

[13]  S. Diekmann,et al.  Functional Complementation of Human Centromere Protein A (CENP-A) by Cse4p from Saccharomyces cerevisiae , 2004, Molecular and Cellular Biology.

[14]  Wei-Hua Wu,et al.  Chz1, a nuclear chaperone for histone H2AZ. , 2007, Molecular cell.

[15]  Michael A. Freitas,et al.  Histone H3-K56 acetylation is catalyzed by histone chaperone-dependent complexes. , 2007, Molecular cell.

[16]  A. Houtsmuller,et al.  Chromatin structure and DNA damage repair , 2008, Epigenetics & Chromatin.

[17]  C. Lehner,et al.  Incorporation of Drosophila CID/CENP-A and CENP-C into Centromeres during Early Embryonic Anaphase , 2007, Current Biology.

[18]  J. Tyler,et al.  Localized Histone Acetylation and Deacetylation Triggered by the Homologous Recombination Pathway of Double-Strand DNA Repair , 2005, Molecular and Cellular Biology.

[19]  Michael Lichten,et al.  Distribution and Dynamics of Chromatin Modification Induced by a Defined DNA Double-Strand Break , 2004, Current Biology.

[20]  G. Almouzni,et al.  The histone chaperone Asf1 is dispensable for direct de novo histone deposition in Xenopus egg extracts , 2007, Chromosoma.

[21]  J. Ausió,et al.  sNASP, a histone H1-specific eukaryotic chaperone dimer that facilitates chromatin assembly. , 2008, Biophysical journal.

[22]  Yusuke Nakamura,et al.  HJURP Is a Cell-Cycle-Dependent Maintenance and Deposition Factor of CENP-A at Centromeres , 2009, Cell.

[23]  G. Almouzni,et al.  New Histone Incorporation Marks Sites of UV Repair in Human Cells , 2006, Cell.

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

[25]  J. Sogo,et al.  The stability of nucleosomes at the replication fork. , 1996, Journal of molecular biology.

[26]  Yawen Bai,et al.  NMR structure of chaperone Chz1 complexed with histones H2A.Z-H2B , 2008, Nature Structural &Molecular Biology.

[27]  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.

[28]  M. Lieber,et al.  FACT-mediated exchange of histone variant H2AX regulated by phosphorylation of H2AX and ADP-ribosylation of Spt16. , 2008, Molecular cell.

[29]  T. Formosa,et al.  The Saccharomyces cerevisiae DNA polymerase alpha catalytic subunit interacts with Cdc68/Spt16 and with Pob3, a protein similar to an HMG1-like protein , 1997, Molecular and cellular biology.

[30]  William A. Richardson,et al.  Fission Yeast Scm3: A CENP-A Receptor Required for Integrity of Subkinetochore Chromatin , 2009, Molecular cell.

[31]  M. Osley,et al.  Chromatin remodelling at a DNA double-strand break site in Saccharomyces cerevisiae , 2005, Nature.

[32]  Wei-Hua Wu,et al.  ATP-Driven Exchange of Histone H2AZ Variant Catalyzed by SWR1 Chromatin Remodeling Complex , 2004, Science.

[33]  A. Escargueil,et al.  What histone code for DNA repair? , 2008, Mutation research.

[34]  S. Henikoff,et al.  Centromeric Nucleosomes Induce Positive DNA Supercoils , 2009, Cell.

[35]  P. Adams,et al.  Defective S phase chromatin assembly causes DNA damage, activation of the S phase checkpoint, and S phase arrest. , 2003, Molecular cell.

[36]  K. Luger,et al.  The structure of nucleosome assembly protein 1 , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[37]  P. Sung,et al.  DNA double-strand break processing: the beginning of the end. , 2008, Genes & development.

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

[39]  D. Egli,et al.  Physical and Functional Interaction between the Bloom's Syndrome Gene Product and the Largest Subunit of Chromatin Assembly Factor 1 , 2004, Molecular and Cellular Biology.

[40]  B. E. Black,et al.  Propagation of centromeric chromatin requires exit from mitosis , 2007, The Journal of cell biology.

[41]  P. Kaufman,et al.  Histone deposition protein Asf1 maintains DNA replisome integrity and interacts with replication factor C. , 2005, Genes & development.

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

[43]  T. Formosa,et al.  POB 3 Is Required for Both Transcription and Replication in the Yeast Saccharomyces cerevisiae , 2000 .

[44]  J. Finch,et al.  Nucleosomes are assembled by an acidic protein which binds histones and transfers them to DNA , 1978, Nature.

[45]  Wei-Hua Wu,et al.  Supplemental Data Chz 1 , a Nuclear Chaperone for Histone H 2 AZ , 2007 .

[46]  G. Almouzni,et al.  Local action of the chromatin assembly factor CAF‐1 at sites of nucleotide excision repair in vivo , 2003, The EMBO journal.

[47]  R. Kobayashi,et al.  Drosophila NAP-1 is a core histone chaperone that functions in ATP-facilitated assembly of regularly spaced nucleosomal arrays , 1996, Molecular and cellular biology.

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

[49]  Yusuke Toyoda,et al.  Priming of Centromere for CENP-A Recruitment by Human hMis18α, hMis18β, and M18BP1 , 2007 .

[50]  T. Shibata,et al.  A DNA unwinding factor involved in DNA replication in cell-free extracts of Xenopus eggs , 1999, Current Biology.

[51]  Jiri Bartek,et al.  Human Asf1 regulates the flow of S phase histones during replicational stress. , 2005, Molecular cell.

[52]  Yusuke Toyoda,et al.  Priming of centromere for CENP-A recruitment by human hMis18alpha, hMis18beta, and M18BP1. , 2007, Developmental cell.

[53]  G. Bellomo,et al.  The HMG protein T160 colocalizes with DNA replication foci and is down-regulated during cell differentiation. , 1999, Experimental cell research.

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

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

[56]  T. Krude,et al.  Induction of CAF-1 Expression in Response to DNA Strand Breaks in Quiescent Human Cells , 2006, Molecular and Cellular Biology.

[57]  T. Formosa,et al.  POB3 is required for both transcription and replication in the yeast Saccharomyces cerevisiae. , 2000, Genetics.

[58]  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.

[59]  J. T. Kadonaga,et al.  Chromatin Assembly by Dna-translocating Motors , 2022 .

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

[61]  D. Stillman,et al.  Structural and Functional Analysis of the Spt16p N-terminal Domain Reveals Overlapping Roles of yFACT Subunits* , 2008, Journal of Biological Chemistry.

[62]  T. Fukagawa,et al.  Asf1 Is Required for Viability and Chromatin Assembly during DNA Replication in Vertebrate Cells* , 2006, Journal of Biological Chemistry.

[63]  G. Orphanides,et al.  FACT Facilitates Transcription-Dependent Nucleosome Alteration , 2003, Science.

[64]  John R Yates,et al.  Acetylation by Tip60 Is Required for Selective Histone Variant Exchange at DNA Lesions , 2004, Science.

[65]  M. Smerdon,et al.  DNA repair and the role of chromatin structure. , 1991, Current opinion in cell biology.

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

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

[68]  C. Ban,et al.  Structure and function of the histone chaperone CIA / ASF 1 complexed with histones H 3 and H 4 , 2008 .

[69]  F. Ochsenbein,et al.  In Vivo Study of the Nucleosome Assembly Functions of ASF1 Histone Chaperones in Human Cells , 2008, Molecular and Cellular Biology.

[70]  Jeffrey G. Linger,et al.  Activation of the DNA Damage Checkpoint in Yeast Lacking the Histone Chaperone Anti-Silencing Function 1 , 2004, Molecular and Cellular Biology.

[71]  B. Stillman,et al.  Chromatin Assembly Coupled to DNA Repair: A New Role for Chromatin Assembly Factor I , 1996, Cell.

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

[73]  M. Smerdon,et al.  Nucleosome rearrangement in human chromatin during UV-induced DNA- reapir synthesis. , 1978, Proceedings of the National Academy of Sciences of the United States of America.

[74]  Jung-Ae Kim,et al.  Chromatin assembly factors Asf1 and CAF-1 have overlapping roles in deactivating the DNA damage checkpoint when DNA repair is complete , 2009, Proceedings of the National Academy of Sciences.

[75]  Michael A. Freitas,et al.  Histone H4 lysine 91 acetylation a core domain modification associated with chromatin assembly. , 2005, Molecular cell.

[76]  P. Russell,et al.  Fission yeast Scm3 mediates stable assembly of Cnp1/CENP-A into centromeric chromatin. , 2009, Molecular cell.

[77]  P. Grandi,et al.  A CAF-1–PCNA-Mediated Chromatin Assembly Pathway Triggered by Sensing DNA Damage , 2000, Molecular and Cellular Biology.

[78]  V. Jackson Deposition of newly synthesized histones: hybrid nucleosomes are not tandemly arranged on daughter DNA strands. , 1988, Biochemistry.

[79]  Richard E. Baker,et al.  Scm3, an essential Saccharomyces cerevisiae centromere protein required for G2/M progression and Cse4 localization , 2007, Proceedings of the National Academy of Sciences.

[80]  C. Cantor,et al.  Incorporation of exogenous pyrene-labeled histone into Physarum chromatin: a system for studying changes in nucleosomes assembled in vivo , 1980, Cell.

[81]  B. E. Black,et al.  The histone variant CENP-A and centromere specification. , 2008, Current opinion in cell biology.

[82]  D. Stillman,et al.  yFACT induces global accessibility of nucleosomal DNA without H2A-H2B displacement. , 2009, Molecular cell.

[83]  E. Wagner,et al.  Nuclear Autoantigenic Sperm Protein (NASP), a Linker Histone Chaperone That Is Required for Cell Proliferation* , 2006, Journal of Biological Chemistry.

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

[85]  G. Mizuguchi,et al.  Nonhistone Scm3 and Histones CenH3-H4 Assemble the Core of Centromere-Specific Nucleosomes , 2007, Cell.

[86]  M. Horikoshi,et al.  Structure and function of the histone chaperone CIA/ASF1 complexed with histones H3 and H4 , 2007, Nature.

[87]  J. Chin,et al.  A Method for Genetically Installing Site-Specific Acetylation in Recombinant Histones Defines the Effects of H3 K56 Acetylation , 2009, Molecular cell.

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

[89]  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.

[90]  R. Reeves,et al.  Sodium butyrate stimulates DNA repair in UV-irradiated normal and xeroderma pigmentosum human fibroblasts. , 1982, The Journal of biological chemistry.

[91]  V. Rybin,et al.  The FACT Spt16 “peptidase” domain is a histone H3–H4 binding module , 2008, Proceedings of the National Academy of Sciences.

[92]  M. Grunstein,et al.  Yeast histone H3 and H4 amino termini are important for nucleosome assembly in vivo and in vitro: redundant and position-independent functions in assembly but not in gene regulation. , 1996, Genes & development.

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

[94]  X. Pei,et al.  Structural Basis for the Recognition of Histone H4 by the Histone-Chaperone RbAp46 , 2008, Structure.

[95]  S. Gasser,et al.  Distinct roles for SWR1 and INO80 chromatin remodeling complexes at chromosomal double‐strand breaks , 2007, The EMBO journal.

[96]  J. Tyler,et al.  Acetylation in the globular core of histone H3 on lysine-56 promotes chromatin disassembly during transcriptional activation , 2008, Proceedings of the National Academy of Sciences.

[97]  R. Knippers,et al.  Structure of replicating simian virus 40 minichromosomes. The replication fork, core histone segregation and terminal structures. , 1986, Journal of molecular biology.

[98]  Ricky D. Edmondson,et al.  GINS maintains association of Cdc45 with MCM in replisome progression complexes at eukaryotic DNA replication forks , 2006, Nature Cell Biology.

[99]  T. Krude,et al.  Silencing of Chromatin Assembly Factor 1 in Human Cells Leads to Cell Death and Loss of Chromatin Assembly during DNA Synthesis , 2004, Molecular and Cellular Biology.

[100]  I. Stagljar,et al.  The Werner syndrome protein is required for recruitment of chromatin assembly factor 1 following DNA damage , 2007, Oncogene.

[101]  C. Chien,et al.  Functional cooperation between FACT and MCM helicase facilitates initiation of chromatin DNA replication , 2006, The EMBO journal.

[102]  G. Almouzni,et al.  Making copies of chromatin: the challenge of nucleosomal organization and epigenetic information. , 2009, Trends in cell biology.

[103]  K. Dubrana,et al.  The processing of double-strand breaks and binding of single-strand-binding proteins RPA and Rad51 modulate the formation of ATR-kinase foci in yeast , 2007, Journal of Cell Science.

[104]  R. Kingston,et al.  Structural basis of histone H4 recognition by p55. , 2008, Genes & development.