The histone code at DNA breaks: a guide to repair?

Chromatin modifications are important for all cellular processes that involve DNA, including transcription, replication and DNA repair. Chromatin can be modified by the addition of adducts to histone tail residues or by nucleosome remodelling, which requires ATP-dependent chromatin-remodelling complexes. Although the role of these mechanisms in transcription is well studied, their impact on DNA repair has only recently become evident. One crucial chromatin modification, the phosphorylation of histone H2A, links the recruitment of histone modifiers and ATP-dependent chromatin-remodelling complexes to sites of DNA damage.

[1]  E. Rogakou,et al.  Megabase Chromatin Domains Involved in DNA Double-Strand Breaks in Vivo , 1999, The Journal of cell biology.

[2]  S. West,et al.  ATP-dependent branch migration of holliday junctions promoted by the RuvA and RuvB proteins of E. coli , 1992, Cell.

[3]  Kunihiro Matsumoto,et al.  Recruitment of Mec1 and Ddc1 Checkpoint Proteins to Double-Strand Breaks Through Distinct Mechanisms , 2001, Science.

[4]  Barbara Hohn,et al.  Recruitment of the INO80 Complex by H2A Phosphorylation Links ATP-Dependent Chromatin Remodeling with DNA Double-Strand Break Repair , 2004, Cell.

[5]  Andrew J Link,et al.  A Protein Complex Containing the Conserved Swi2/Snf2-Related ATPase Swr1p Deposits Histone Variant H2A.Z into Euchromatin , 2004, PLoS biology.

[6]  B. Cairns,et al.  A Rsc3/Rsc30 zinc cluster dimer reveals novel roles for the chromatin remodeler RSC in gene expression and cell cycle control. , 2001, Molecular cell.

[7]  P. Jeggo,et al.  ATM and DNA-PK Function Redundantly to Phosphorylate H2AX after Exposure to Ionizing Radiation , 2004, Cancer Research.

[8]  K. Nasmyth,et al.  Sister chromatid cohesion is required for postreplicative double-strand break repair in Saccharomyces cerevisiae , 2001, Current Biology.

[9]  Sang Eun Lee,et al.  The Yeast Chromatin Remodeler RSC Complex Facilitates End Joining Repair of DNA Double-Strand Breaks , 2005, Molecular and Cellular Biology.

[10]  R. Glaser,et al.  DNA double-strand break-induced phosphorylation of Drosophila histone variant H2Av helps prevent radiation-induced apoptosis. , 2002, Nucleic acids research.

[11]  E. Rogakou,et al.  Yeast histone 2A serine 129 is essential for the efficient repair of checkpoint‐blind DNA damage , 2003, EMBO reports.

[12]  A. Taylor,et al.  Specific Recruitment of Human Cohesin to Laser-induced DNA Damage* , 2002, The Journal of Biological Chemistry.

[13]  F. Alt,et al.  Increased ionizing radiation sensitivity and genomic instability in the absence of histone H2AX , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[14]  M. Parthun,et al.  Histone H3 and the Histone Acetyltransferase Hat1p Contribute to DNA Double-Strand Break Repair , 2002, Molecular and Cellular Biology.

[15]  Jacques Côté,et al.  The highly conserved and multifunctional NuA4 HAT complex. , 2004, Current opinion in genetics & development.

[16]  Junjie Chen,et al.  Histone H2AX Is Phosphorylated in an ATR-dependent Manner in Response to Replicational Stress* , 2001, The Journal of Biological Chemistry.

[17]  Jonathan Chernoff,et al.  Apoptotic Phosphorylation of Histone H2B Is Mediated by Mammalian Sterile Twenty Kinase , 2003, Cell.

[18]  Sophie G. Martin,et al.  Relocalization of Telomeric Ku and SIR Proteins in Response to DNA Strand Breaks in Yeast , 1999, Cell.

[19]  John Rouse,et al.  Lcd1p recruits Mec1p to DNA lesions in vitro and in vivo. , 2002, Molecular cell.

[20]  James T Kadonaga,et al.  Chromatin remodeling by ATP-dependent molecular machines. , 2003, BioEssays : news and reviews in molecular, cellular and developmental biology.

[21]  Oscar Fernandez-Capetillo,et al.  Phosphorylation of Histone H2B at DNA Double-Strand Breaks , 2004, The Journal of experimental medicine.

[22]  D. Gottschling,et al.  Identification of high-copy disruptors of telomeric silencing in Saccharomyces cerevisiae. , 1998, Genetics.

[23]  Kunihiro Matsumoto,et al.  ATM-related Tel1 associates with double-strand breaks through an Xrs2-dependent mechanism. , 2003, Genes & development.

[24]  T. Ried,et al.  H2AX Haploinsufficiency Modifies Genomic Stability and Tumor Susceptibility , 2003, Cell.

[25]  Paolo Plevani,et al.  The DNA Damage Checkpoint Response Requires Histone H2B Ubiquitination by Rad6-Bre1 and H3 Methylation by Dot1* , 2005, Journal of Biological Chemistry.

[26]  Alexander W. Bird,et al.  Acetylation of histone H4 by Esa1 is required for DNA double-strand break repair , 2002, Nature.

[27]  K. Shirahige,et al.  Postreplicative recruitment of cohesin to double-strand breaks is required for DNA repair. , 2004, Molecular cell.

[28]  R. Marmorstein Protein modules that manipulate histone tails for chromatin regulation , 2001, Nature Reviews Molecular Cell Biology.

[29]  J. Hoeijmakers,et al.  Chromosomal stability and the DNA double-stranded break connection , 2001, Nature Reviews Genetics.

[30]  Michael Lichten,et al.  DNA damage response pathway uses histone modification to assemble a double-strand break-specific cohesin domain. , 2004, Molecular cell.

[31]  Michael Grunstein,et al.  Histone acetylation and deacetylation in yeast , 2003, Nature Reviews Molecular Cell Biology.

[32]  N. Krogan,et al.  INO80 and γ-H2AX Interaction Links ATP-Dependent Chromatin Remodeling to DNA Damage Repair , 2004, Cell.

[33]  S. Kron,et al.  NuA4 Subunit Yng2 Function in Intra-S-Phase DNA Damage Response , 2002, Molecular and Cellular Biology.

[34]  J. Haber,et al.  In vivo roles of Rad52, Rad54, and Rad55 proteins in Rad51-mediated recombination. , 2003, Molecular cell.

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

[36]  P. Brown,et al.  Whole-genome expression analysis of snf/swi mutants of Saccharomyces cerevisiae. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[37]  K. Miyahara,et al.  Abundance of the RSC nucleosome‐remodeling complex is important for the cells to tolerate DNA damage in Saccharomyces cerevisiae , 2002, FEBS letters.

[38]  Jian Huang,et al.  The RSC nucleosome-remodeling complex is required for Cohesin's association with chromosome arms. , 2004, Molecular cell.

[39]  Michel C. Nussenzweig,et al.  Genomic Instability in Mice Lacking Histone H2AX , 2002, Science.

[40]  Sung-Hee Ahn,et al.  Phosphorylation of Histone H4 Serine 1 during DNA Damage Requires Casein Kinase II in S. cerevisiae , 2005, Current Biology.

[41]  Michael M. Murphy,et al.  ATM Phosphorylates Histone H2AX in Response to DNA Double-strand Breaks* , 2001, The Journal of Biological Chemistry.

[42]  P. Sung,et al.  Recruitment of the recombinational repair machinery to a DNA double-strand break in yeast. , 2003, Molecular cell.

[43]  G. Benvenuto,et al.  The INO80 protein controls homologous recombination in Arabidopsis thaliana. , 2004, Molecular cell.

[44]  Ali Jazayeri,et al.  Saccharomyces cerevisiae Sin 3 p facilitates DNA double-strand break repair , 2004 .

[45]  Jun Qin,et al.  Involvement of the TIP60 Histone Acetylase Complex in DNA Repair and Apoptosis , 2000, Cell.

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

[47]  Huiming Ding,et al.  A Snf2 family ATPase complex required for recruitment of the histone H2A variant Htz1. , 2003, Molecular cell.

[48]  S. Jackson,et al.  Binding of chromatin-modifying activities to phosphorylated histone H2A at DNA damage sites. , 2004, Molecular cell.

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

[50]  F. Alt,et al.  Histone H2AX A Dosage-Dependent Suppressor of Oncogenic Translocations and Tumors , 2003, Cell.

[51]  M. Resnick,et al.  Genes required for ionizing radiation resistance in yeast , 2001, Nature Genetics.

[52]  Stephen P. Jackson,et al.  A role for Saccharomyces cerevisiae histone H2A in DNA repair , 2000, Nature.

[53]  B. Cairns,et al.  Distinct roles for the RSC and Swi/Snf ATP-dependent chromatin remodelers in DNA double-strand break repair. , 2005, Genes & development.

[54]  D. Toczyski,et al.  Two checkpoint complexes are independently recruited to sites of DNA damage in vivo. , 2001, Genes & development.

[55]  P. Russell,et al.  Erratum: Histone H2A phosphorylation controls Crb2 recruitment at DNA breaks, maintains checkpoint arrest, and influences DNA repair in fission yeast (Molecular and Cellular Biology (2004) 24, 14 (6215-6230)) , 2004 .

[56]  Tom J. Petty,et al.  Methylated lysine 79 of histone H3 targets 53BP1 to DNA double-strand breaks , 2004, Nature.

[57]  Sung-Hee Ahn,et al.  Sterile 20 Kinase Phosphorylates Histone H2B at Serine 10 during Hydrogen Peroxide-Induced Apoptosis in S. cerevisiae , 2005, Cell.

[58]  R. Bonner,et al.  Histone H2AX phosphorylation is dispensable for the initial recognition of DNA breaks , 2003, Nature Cell Biology.

[59]  A. Lustig,et al.  Multiple roles for Saccharomyces cerevisiae histone H2A in telomere position effect, Spt phenotypes and double-strand-break repair. , 2003, Genetics.

[60]  Jessica A Downs,et al.  Saccharomyces cerevisiae Histone H2A Ser122 Facilitates DNA Repair , 2005, Genetics.

[61]  J. Mata,et al.  Methylation of Histone H4 Lysine 20 Controls Recruitment of Crb2 to Sites of DNA Damage , 2004, Cell.

[62]  Ali Hamiche,et al.  A chromatin remodelling complex involved in transcription and DNA processing , 2000, Nature.

[63]  Brian D. Strahl,et al.  Gene silencing: Trans-histone regulatory pathway in chromatin , 2002, Nature.

[64]  F. Alt,et al.  Control of sister chromatid recombination by histone H2AX. , 2004, Molecular cell.