DOI: 10.1139/o05-114. H2AX: tailoring histone H2A for chromatin-dependent genomic integrity

H2AX: tailoring histone H2A for chromatin-dependent genomic integrity

10.1139/o05-114

Crossref journal-article

Canadian Science Publishing

Biochemistry and Cell Biology (155)

Abstract

During the last decade, chromatin research has been focusing on the role of histone variability as a modulator of chromatin structure and function. Histone variability can be the result of either post-translational modifications or intrinsic variation at the primary structure level: histone variants. In this review, we center our attention on one of the most extensively characterized of such histone variants in recent years, histone H2AX. The molecular phylogeny of this variant seems to have run in parallel with that of the major canonical somatic H2A1 in eukaryotes. Functionally, H2AX appears to be mainly associated with maintaining the genome integrity by participating in the repair of the double-stranded DNA breaks exogenously introduced by environmental damage (ionizing radiation, chemicals) or in the process of homologous recombination during meiosis. At the structural level, these processes involve the phosphorylation of serine at the SQE motif, which is present at the very end of the C-terminal domain of H2AX, and possibly other PTMs, some of which have recently started to be defined. We discuss a model to account for how these H2AX PTMs in conjunction with chromatin remodeling complexes (such as INO80 and SWRI) can modify chromatin structure (remodeling) to support the DNA unraveling ultimately required for DNA repair.Key words: H2AX, DNA repair, double-stranded DNA breaks, phosphorylation.

Bibliography

Li, A., EirÃn-LÃ³pez, J. M., & AusiÃ³, J. (2005). H2AX: tailoring histone H2A for chromatin-dependent genomic integrity. Biochemistry and Cell Biology, 83(4), 505â515.

Authors 3

Andra Li (first)
José M Eirín-López (additional)
Juan Ausió (additional)

References 66 Referenced 44

10.1023/A:1007156629024 / Mol. Biol. Rep. by Alvelo-Ceron D. (2000)
10.1073/pnas.92.24.11170 / Proc. Natl. Acad. Sci. U.S.A. by Arents G. (1995)
10.1006/jmbi.2001.4564 / J. Mol. Biol. by Arnaudeau C. (2001)
10.1021/bi020059d / Biochemistry by Ausió J. (2002)
Ausió, J., and Abbott, D.W. 2004. The role of histone variability in chromatin stability and folding. In Chromatin structure and dynamics: state-of-the-art. Edited by J. Zlatanova and S.H. Leuba. Elsevier B.V. pp. 241-290. (10.1016/S0167-7306(03)39010-6)
10.1139/o01-147 / Biochem. Cell Biol. by Ausió J. (2001)
10.1038/nature01368 / Nature (London) by Bakkenist C.J. (2003)
10.1016/j.yexcr.2004.07.022 / Exp. Cell Res. by Balajee A.S. (2004)
10.1073/pnas.122228699 / Proc. Natl. Acad. Sci. U.S.A. by Bassing C.H. (2002)
10.1038/nature01035 / Nature (London) by Bird A.W. (2002)
10.1101/gad.1056603 / Genes Dev. by Boudreault A.A. (2003)
10.1074/jbc.C100466200 / J. Biol. Chem. by Burma S. (2001)
10.1016/j.cell.2004.12.005 / Cell by Cairns B.R. (2004)
10.1126/science.1069398 / Science (Wash. D.C.) by Celeste A. (2002)
10.1038/ncb1004 / Nat. Cell Biol. by Celeste A. (2003)
10.1126/science.290.5498.1962 / Science (Wash. D.C.) by Chen H.T. (2000)
10.1074/jbc.M407886200 / J. Biol. Chem. by Daniel R. (2004)
10.1038/35050000 / Nature (London) by Downs J.A. (2000)
10.1016/S1097-2765(03)00197-7 / Mol. Cell by Downs J.A. (2003)
10.1016/j.molcel.2004.12.003 / Mol. Cell by Downs J.A. (2004)
10.1128/MCB.24.5.1884-1896.2004 / Mol. Cell Biol. by Doyon Y. (2004)
10.1074/jbc.M410746200 / J.Biol. Chem. by Drouet J. (2005)
10.1038/ncb884 / Nat. Cell Biol. by Fernandez-Capetillo O. (2002)
10.1083/jcb.200305124 / J. Cell Biol. by Fernandez-Capetillo O. (2003)
10.1016/S1534-5807(03)00093-5 / Dev. Cell by Fernandez-Capetillo O. (2003)
10.1084/jem.20032247 / J. Exp. Med. by Fernandez-Capetillo O. (2004)
10.1016/j.dnarep.2004.03.024 / DNA Repair by Fernandez-Capetillo O. (2004)
10.1095/biolreprod.102.008672 / Biol. Reprod. by Hamer G. (2003)
10.1074/jbc.M403924200 / J. Biol. Chem. by Hao L. (2004)
10.1111/j.1365-2958.2004.04195.x / Mol. Microbiol. by Harvey A.C. (2004)
10.1038/85781 / Nat. Genet. by Hunter N. (2001)
10.1038/nature03114 / Nature (London) by Huyen Y. (2004)
10.1093/nar/28.19.3811 / Nucleic Acids Res. by Jackson J.D. (2000)
10.1083/jcb.200209065 / J. Cell Biol. by Kao G.D. (2003)
10.1146/annurev.genet.38.072902.091500 / Rev. Genet. by Krogh B.O. (2004)
10.1073/pnas.96.4.1403 / Proc. Natl. Acad. Sci. U.S.A. by Kurimasa A. (1999)
10.1126/science.1103455 / Science (Wash. D.C.) by Kusch T. (2004)
10.1139/o03-045 / Biochem. Cell Biol. by Lewis J.D. (2003)
10.1038/38444 / Nature (London) by Luger K. (1997)
10.1038/85830 / Nat. Genet. by Mahadevaiah S.K. (2001)
10.1038/nsb996 / Nat. Struct. Biol. by Malik H.S. (2003)
10.1093/nar/17.22.9113 / Nucleic Acids Res. by Mannironi C. (1989)
10.1139/o04-034 / Biochem. Cell Biol. by Moore J.D. (2004)
10.1016/j.cell.2004.11.037 / Cell by Morrison A.J. (2004)
10.1667/RR3043 / Radiat. Res. by Nazarov I.B. (2003)
10.1093/nar/gkg921 / Nucleic Acids Res. by Park E. (2003)
10.1016/S0960-9822(00)00610-2 / Curr. Biol. by Paull T.T. (2000)
10.1139/o03-042 / Biochem. Cell Biol. by Pilch D.R. (2003)
10.1016/S0959-437X(02)00282-4 / Curr. Opin. Genet. Dev. by Redon C. (2002)
10.1074/jbc.273.10.5858 / J. Biol. Chem. by Rogakou E.P. (1998)
10.1083/jcb.146.5.905 / J. Cell Biol. by Rogakou E.P. (1999)
10.1074/jbc.275.13.9390 / J. Biol. Chem. by Rogakou E.P. (2000)
10.1016/j.cell.2004.11.009 / Cell by Sanders S.L. (2004)
10.1159/000076809 / Cytogenet. Genome Res. by Scherthan H. (2003)
10.1093/nar/18.20.6097 / Nucleic Acids Res. by Schneider T.D. (1990)
10.1016/S0006-291X(02)02383-5 / Biochem. Biophys. Res. Commun. by Siino J.S. (2002)
10.1038/nature01446 / Nature (London) by Stewart G.S. (2004)
10.1158/0008-5472.CAN-03-3207 / Cancer Res. by Stiff T. (2004)
10.1016/j.dnarep.2004.04.009 / DNA Repair by Taylor A.M.R. (2004)
10.1007/s10254-004-0030-8 / Rev. Physiol. Biochem. Pharmacol. by Thelestam M. (2004)
10.1016/j.cell.2004.11.033 / Cell by van Attikum H. (2004)
10.1074/jbc.C100569200 / J. Biol. Chem. by Ward I.M. (2001)
10.1074/jbc.C300117200 / J. Biol. Chem. by Ward I.M. (2003)
10.1093/genetics/164.1.47 / Genetics by Wyatt H.R. (2003)
10.1101/gad.10.19.2411 / Genes Dev. by Xu Y. (1996)
10.1128/MCB.24.21.9286-9294.2004 / Formation. Mol. Cell. Biol. by Zimmerman E.S. (2004)

Dates

Type	When
Created	20 years ago (Aug. 11, 2005, 10:16 a.m.)
Deposited	2 months ago (July 2, 2025, 2:44 p.m.)
Indexed	2 months ago (July 3, 2025, 12:17 a.m.)
Issued	20 years, 1 month ago (Aug. 1, 2005)
Published	20 years, 1 month ago (Aug. 1, 2005)
Published Print	20 years, 1 month ago (Aug. 1, 2005)

Funders 0

None

BibTeX

@article{Li_2005, title={H2AX: tailoring histone H2A for chromatin-dependent genomic integrity}, volume={83}, ISSN={1208-6002}, url={http://dx.doi.org/10.1139/o05-114}, DOI={10.1139/o05-114}, number={4}, journal={Biochemistry and Cell Biology}, publisher={Canadian Science Publishing}, author={Li, Andra and Eirín-López, José M and Ausió, Juan}, year={2005}, month=aug, pages={505–515} }

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      "year": "2001",
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      "first-page": "5945",
      "DOI": "10.1021/bi020059d",
      "volume": "41",
      "author": "Ausi\u00f3 J.",
      "year": "2002",
      "journal-title": "Biochemistry"
    },
    {
      "key": "p_5/p_5_1",
      "doi-asserted-by": "crossref",
      "unstructured": "Ausi\u00f3, J., and Abbott, D.W. 2004. The role of histone variability in chromatin stability and folding. In Chromatin structure and dynamics: state-of-the-art. Edited by J. Zlatanova and S.H. Leuba. Elsevier B.V. pp. 241-290.",
      "DOI": "10.1016/S0167-7306(03)39010-6"
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    {
      "key": "p_6/p_6_1",
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      "first-page": "693",
      "DOI": "10.1139/o01-147",
      "volume": "79",
      "author": "Ausi\u00f3 J.",
      "year": "2001",
      "journal-title": "Biochem. Cell Biol."
    },
    {
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      "doi-asserted-by": "crossref",
      "first-page": "499",
      "DOI": "10.1038/nature01368",
      "volume": "421",
      "author": "Bakkenist C.J.",
      "year": "2003",
      "journal-title": "Nature (London)"
    },
    {
      "key": "p_8/p_8_1",
      "doi-asserted-by": "crossref",
      "first-page": "320",
      "DOI": "10.1016/j.yexcr.2004.07.022",
      "volume": "300",
      "author": "Balajee A.S.",
      "year": "2004",
      "journal-title": "Exp. Cell Res."
    },
    {
      "key": "p_9/p_9_1",
      "doi-asserted-by": "crossref",
      "first-page": "8173",
      "DOI": "10.1073/pnas.122228699",
      "volume": "99",
      "author": "Bassing C.H.",
      "year": "2002",
      "journal-title": "Proc. Natl. Acad. Sci. U.S.A."
    },
    {
      "key": "p_10/p_10_1",
      "doi-asserted-by": "crossref",
      "first-page": "411",
      "DOI": "10.1038/nature01035",
      "volume": "419",
      "author": "Bird A.W.",
      "year": "2002",
      "journal-title": "Nature (London)"
    },
    {
      "key": "p_11/p_11_1",
      "doi-asserted-by": "crossref",
      "first-page": "1415",
      "DOI": "10.1101/gad.1056603",
      "volume": "17",
      "author": "Boudreault A.A.",
      "year": "2003",
      "journal-title": "Genes Dev."
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    {
      "key": "p_12/p_12_1",
      "doi-asserted-by": "crossref",
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      "DOI": "10.1074/jbc.C100466200",
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      "journal-title": "J. Biol. Chem."
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    {
      "key": "p_13/p_13_1",
      "doi-asserted-by": "crossref",
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      "DOI": "10.1016/j.cell.2004.12.005",
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      "year": "2004",
      "journal-title": "Cell"
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    {
      "key": "p_14/p_14_1",
      "doi-asserted-by": "crossref",
      "first-page": "922",
      "DOI": "10.1126/science.1069398",
      "volume": "296",
      "author": "Celeste A.",
      "year": "2002",
      "journal-title": "Science (Wash. D.C.)"
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    {
      "key": "p_15/p_15_1",
      "doi-asserted-by": "crossref",
      "first-page": "675",
      "DOI": "10.1038/ncb1004",
      "volume": "5",
      "author": "Celeste A.",
      "year": "2003",
      "journal-title": "Nat. Cell Biol."
    },
    {
      "key": "p_16/p_16_1",
      "doi-asserted-by": "crossref",
      "first-page": "1962",
      "DOI": "10.1126/science.290.5498.1962",
      "volume": "290",
      "author": "Chen H.T.",
      "year": "2000",
      "journal-title": "Science (Wash. D.C.)"
    },
    {
      "key": "p_17/p_17_1",
      "doi-asserted-by": "crossref",
      "first-page": "45810",
      "DOI": "10.1074/jbc.M407886200",
      "volume": "279",
      "author": "Daniel R.",
      "year": "2004",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "p_18/p_18_1",
      "doi-asserted-by": "crossref",
      "first-page": "1001",
      "DOI": "10.1038/35050000",
      "volume": "408",
      "author": "Downs J.A.",
      "year": "2000",
      "journal-title": "Nature (London)"
    },
    {
      "key": "p_19/p_19_1",
      "doi-asserted-by": "crossref",
      "first-page": "1685",
      "DOI": "10.1016/S1097-2765(03)00197-7",
      "volume": "11",
      "author": "Downs J.A.",
      "year": "2003",
      "journal-title": "Mol. Cell"
    },
    {
      "key": "p_20/p_20_1",
      "doi-asserted-by": "crossref",
      "first-page": "979",
      "DOI": "10.1016/j.molcel.2004.12.003",
      "volume": "16",
      "author": "Downs J.A.",
      "year": "2004",
      "journal-title": "Mol. Cell"
    },
    {
      "key": "p_21/p_21_1",
      "doi-asserted-by": "crossref",
      "first-page": "1884",
      "DOI": "10.1128/MCB.24.5.1884-1896.2004",
      "volume": "24",
      "author": "Doyon Y.",
      "year": "2004",
      "journal-title": "Mol. Cell Biol."
    },
    {
      "issue": "8",
      "key": "p_22/p_22_1",
      "doi-asserted-by": "crossref",
      "first-page": "7060",
      "DOI": "10.1074/jbc.M410746200",
      "volume": "280",
      "author": "Drouet J.",
      "year": "2005",
      "journal-title": "J.Biol. Chem."
    },
    {
      "key": "p_23/p_23_1",
      "doi-asserted-by": "crossref",
      "first-page": "993",
      "DOI": "10.1038/ncb884",
      "volume": "4",
      "author": "Fernandez-Capetillo O.",
      "year": "2002",
      "journal-title": "Nat. Cell Biol."
    },
    {
      "key": "p_24/p_24_1",
      "doi-asserted-by": "crossref",
      "first-page": "15",
      "DOI": "10.1083/jcb.200305124",
      "volume": "163",
      "author": "Fernandez-Capetillo O.",
      "year": "2003",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "p_25/p_25_1",
      "doi-asserted-by": "crossref",
      "first-page": "497",
      "DOI": "10.1016/S1534-5807(03)00093-5",
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      "author": "Fernandez-Capetillo O.",
      "year": "2003",
      "journal-title": "Dev. Cell"
    },
    {
      "key": "p_26/p_26_1",
      "doi-asserted-by": "crossref",
      "first-page": "1671",
      "DOI": "10.1084/jem.20032247",
      "volume": "199",
      "author": "Fernandez-Capetillo O.",
      "year": "2004",
      "journal-title": "J. Exp. Med."
    },
    {
      "issue": "8",
      "key": "p_27/p_27_1",
      "doi-asserted-by": "crossref",
      "first-page": "959",
      "DOI": "10.1016/j.dnarep.2004.03.024",
      "volume": "3",
      "author": "Fernandez-Capetillo O.",
      "year": "2004",
      "journal-title": "DNA Repair"
    },
    {
      "key": "p_28/p_28_1",
      "doi-asserted-by": "crossref",
      "first-page": "628",
      "DOI": "10.1095/biolreprod.102.008672",
      "volume": "68",
      "author": "Hamer G.",
      "year": "2003",
      "journal-title": "Biol. Reprod."
    },
    {
      "key": "p_29/p_29_1",
      "doi-asserted-by": "crossref",
      "first-page": "45148",
      "DOI": "10.1074/jbc.M403924200",
      "volume": "279",
      "author": "Hao L.",
      "year": "2004",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "p_30/p_30_1",
      "doi-asserted-by": "crossref",
      "first-page": "771",
      "DOI": "10.1111/j.1365-2958.2004.04195.x",
      "volume": "53",
      "author": "Harvey A.C.",
      "year": "2004",
      "journal-title": "Mol. Microbiol."
    },
    {
      "key": "p_31/p_31_1",
      "doi-asserted-by": "crossref",
      "first-page": "236",
      "DOI": "10.1038/85781",
      "volume": "27",
      "author": "Hunter N.",
      "year": "2001",
      "journal-title": "Nat. Genet."
    },
    {
      "key": "p_32/p_32_1",
      "doi-asserted-by": "crossref",
      "first-page": "406",
      "DOI": "10.1038/nature03114",
      "volume": "432",
      "author": "Huyen Y.",
      "year": "2004",
      "journal-title": "Nature (London)"
    },
    {
      "key": "p_33/p_33_1",
      "doi-asserted-by": "crossref",
      "first-page": "3811",
      "DOI": "10.1093/nar/28.19.3811",
      "volume": "28",
      "author": "Jackson J.D.",
      "year": "2000",
      "journal-title": "Nucleic Acids Res."
    },
    {
      "key": "p_34/p_34_1",
      "doi-asserted-by": "crossref",
      "first-page": "1017",
      "DOI": "10.1083/jcb.200209065",
      "volume": "160",
      "author": "Kao G.D.",
      "year": "2003",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "p_35/p_35_1",
      "doi-asserted-by": "crossref",
      "first-page": "233",
      "DOI": "10.1146/annurev.genet.38.072902.091500",
      "volume": "38",
      "author": "Krogh B.O.",
      "year": "2004",
      "journal-title": "Rev. Genet."
    },
    {
      "key": "p_36/p_36_1",
      "doi-asserted-by": "crossref",
      "first-page": "1403",
      "DOI": "10.1073/pnas.96.4.1403",
      "volume": "96",
      "author": "Kurimasa A.",
      "year": "1999",
      "journal-title": "Proc. Natl. Acad. Sci. U.S.A."
    },
    {
      "key": "p_37/p_37_1",
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      "first-page": "2084",
      "DOI": "10.1126/science.1103455",
      "volume": "306",
      "author": "Kusch T.",
      "year": "2004",
      "journal-title": "Science (Wash. D.C.)"
    },
    {
      "key": "p_38/p_38_1",
      "doi-asserted-by": "crossref",
      "first-page": "131",
      "DOI": "10.1139/o03-045",
      "volume": "81",
      "author": "Lewis J.D.",
      "year": "2003",
      "journal-title": "Biochem. Cell Biol."
    },
    {
      "key": "p_39/p_39_1",
      "doi-asserted-by": "crossref",
      "first-page": "251",
      "DOI": "10.1038/38444",
      "volume": "6648",
      "author": "Luger K.",
      "year": "1997",
      "journal-title": "Nature (London)"
    },
    {
      "key": "p_40/p_40_1",
      "doi-asserted-by": "crossref",
      "first-page": "271",
      "DOI": "10.1038/85830",
      "volume": "27",
      "author": "Mahadevaiah S.K.",
      "year": "2001",
      "journal-title": "Nat. Genet."
    },
    {
      "key": "p_41/p_41_1",
      "doi-asserted-by": "crossref",
      "first-page": "882",
      "DOI": "10.1038/nsb996",
      "volume": "10",
      "author": "Malik H.S.",
      "year": "2003",
      "journal-title": "Nat. Struct. Biol."
    },
    {
      "key": "p_42/p_42_1",
      "doi-asserted-by": "crossref",
      "first-page": "9113",
      "DOI": "10.1093/nar/17.22.9113",
      "volume": "17",
      "author": "Mannironi C.",
      "year": "1989",
      "journal-title": "Nucleic Acids Res."
    },
    {
      "key": "p_43/p_43_1",
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      "first-page": "446",
      "DOI": "10.1139/o04-034",
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      "author": "Moore J.D.",
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      "journal-title": "Biochem. Cell Biol."
    },
    {
      "key": "p_44/p_44_1",
      "doi-asserted-by": "crossref",
      "first-page": "767",
      "DOI": "10.1016/j.cell.2004.11.037",
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      "author": "Morrison A.J.",
      "year": "2004",
      "journal-title": "Cell"
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    {
      "key": "p_45/p_45_1",
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      "first-page": "309",
      "DOI": "10.1667/RR3043",
      "volume": "160",
      "author": "Nazarov I.B.",
      "year": "2003",
      "journal-title": "Radiat. Res."
    },
    {
      "key": "p_46/p_46_1",
      "doi-asserted-by": "crossref",
      "first-page": "6819",
      "DOI": "10.1093/nar/gkg921",
      "volume": "31",
      "author": "Park E.",
      "year": "2003",
      "journal-title": "Nucleic Acids Res."
    },
    {
      "key": "p_47/p_47_1",
      "doi-asserted-by": "crossref",
      "first-page": "886",
      "DOI": "10.1016/S0960-9822(00)00610-2",
      "volume": "10",
      "author": "Paull T.T.",
      "year": "2000",
      "journal-title": "Curr. Biol."
    },
    {
      "key": "p_48/p_48_1",
      "doi-asserted-by": "crossref",
      "first-page": "123",
      "DOI": "10.1139/o03-042",
      "volume": "81",
      "author": "Pilch D.R.",
      "year": "2003",
      "journal-title": "Biochem. Cell Biol."
    },
    {
      "key": "p_49/p_49_1",
      "doi-asserted-by": "crossref",
      "first-page": "162",
      "DOI": "10.1016/S0959-437X(02)00282-4",
      "volume": "12",
      "author": "Redon C.",
      "year": "2002",
      "journal-title": "Curr. Opin. Genet. Dev."
    },
    {
      "key": "p_50/p_50_1",
      "doi-asserted-by": "crossref",
      "first-page": "5858",
      "DOI": "10.1074/jbc.273.10.5858",
      "volume": "273",
      "author": "Rogakou E.P.",
      "year": "1998",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "p_51/p_51_1",
      "doi-asserted-by": "crossref",
      "first-page": "905",
      "DOI": "10.1083/jcb.146.5.905",
      "volume": "146",
      "author": "Rogakou E.P.",
      "year": "1999",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "p_52/p_52_1",
      "doi-asserted-by": "crossref",
      "first-page": "9390",
      "DOI": "10.1074/jbc.275.13.9390",
      "volume": "275",
      "author": "Rogakou E.P.",
      "year": "2000",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "p_53/p_53_1",
      "doi-asserted-by": "crossref",
      "first-page": "603",
      "DOI": "10.1016/j.cell.2004.11.009",
      "volume": "119",
      "author": "Sanders S.L.",
      "year": "2004",
      "journal-title": "Cell"
    },
    {
      "key": "p_54/p_54_1",
      "doi-asserted-by": "crossref",
      "first-page": "235",
      "DOI": "10.1159/000076809",
      "volume": "103",
      "author": "Scherthan H.",
      "year": "2003",
      "journal-title": "Cytogenet. Genome Res."
    },
    {
      "key": "p_55/p_55_1",
      "doi-asserted-by": "crossref",
      "first-page": "6097",
      "DOI": "10.1093/nar/18.20.6097",
      "volume": "18",
      "author": "Schneider T.D.",
      "year": "1990",
      "journal-title": "Nucleic Acids Res."
    },
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      "key": "p_56/p_56_1",
      "doi-asserted-by": "crossref",
      "first-page": "1318",
      "DOI": "10.1016/S0006-291X(02)02383-5",
      "volume": "297",
      "author": "Siino J.S.",
      "year": "2002",
      "journal-title": "Biochem. Biophys. Res. Commun."
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    {
      "key": "p_57/p_57_1",
      "doi-asserted-by": "crossref",
      "first-page": "961",
      "DOI": "10.1038/nature01446",
      "volume": "421",
      "author": "Stewart G.S.",
      "year": "2004",
      "journal-title": "Nature (London)"
    },
    {
      "issue": "7",
      "key": "p_58/p_58_1",
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      "first-page": "2390",
      "DOI": "10.1158/0008-5472.CAN-03-3207",
      "volume": "64",
      "author": "Stiff T.",
      "year": "2004",
      "journal-title": "Cancer Res."
    },
    {
      "key": "p_59/p_59_1",
      "doi-asserted-by": "crossref",
      "first-page": "1219",
      "DOI": "10.1016/j.dnarep.2004.04.009",
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      "author": "Taylor A.M.R.",
      "year": "2004",
      "journal-title": "DNA Repair"
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      "key": "p_60/p_60_1",
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      "DOI": "10.1007/s10254-004-0030-8",
      "volume": "152",
      "author": "Thelestam M.",
      "year": "2004",
      "journal-title": "Rev. Physiol. Biochem. Pharmacol."
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      "key": "p_61/p_61_1",
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      "first-page": "47",
      "DOI": "10.1093/genetics/164.1.47",
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      "author": "Xu Y.",
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