DOI: 10.1139/o03-045. A haploid affair: core histone transitions during spermatogenesis

A haploid affair: core histone transitions during spermatogenesis

10.1139/o03-045

Crossref journal-article

Canadian Science Publishing

Biochemistry and Cell Biology (155)

Abstract

The process of meiosis reduces a diploid cell to four haploid gametes and is accompanied by extensive recombination. Thus, the dynamics of chromatin during meiosis are significantly different than in mitotic cells. As spermatogenesis progresses, there is a widespread reorganization of the haploid genome followed by extensive DNA compaction. It has become increasingly clear that the dynamic composition of chromatin plays a critical role in the activities of enzymes and processes that act upon it. Therefore, an analysis of the role of histone variants and modifications in these processes may shed light upon the mechanisms involved and the control of chromatin structure in general. Histone variants such as histone H3.3, H2AX, and macroH2A appear to play key roles in the various stages of spermiogenesis, in addition to the specifically modulated acetylation of histone H4 (acH4), ubiquitination of histones H2A and H2B (uH2A, uH2B), and phosphorylation of histone H3 (H3p). This review will examine recent discoveries concerning the role of histone modifications and variants during meiosis and spermatogenesis.Key words: histone variants, histone modifications, chromatin structure, meiosis.

Bibliography

Lewis, J. D., Abbott, D. W., & AusiÃ³, J. (2003). A haploid affair: core histone transitions during spermatogenesis. Biochemistry and Cell Biology, 81(3), 131â140.

Authors 3

John D Lewis (first)
D Wade Abbott (additional)
Juan Ausió (additional)

References 90 Referenced 64

10.1042/bj2500883 / Biochem. J. by Agell N. (1988)
10.1016/0014-5793(82)80604-2 / FEBS Lett. by Agell N. (1983)
10.1016/S1097-2765(02)00542-7 / Mol. Cell by Ahmad K. (2002)
10.1139/g95-075 / Genome by Akhmanova A.S. (1995)
10.1007/s004120050255 / Chromosoma by Akhmanova A. (1997)
10.1021/bi020059d / Biochemistry by Ausió J. (2002)
10.1139/o01-147 / Biochem. Cell Biol. by Ausió J. (2001)
10.1007/s004120050218 / Chromosoma by Ayoub N. (1997)
10.1006/dbio.1998.9155 / Dev. Biol. by Baarends W.M. (1999)
10.1002/bies.950140103 / Bioessays by Bradbury E.M. (1992)
10.1101/gad.940201 / Genes Dev. by Briggs S.D. (2001)
10.1016/S0968-0004(99)01516-9 / Trends Biochem. Sci. by Brown C.E. (2000)
Celeste, A., Petersen, S., Romanienko, P.J., Fernandez-Capetillo, O., Chen, H.T., Sedelnikova, O.A., Reina-San-Martin, B., Coppola, V., Meffre, E., Difilippantonio, M.J., Redon, C., Pilch, D.R., Olaru, A., Eckhaus, M., Camerini-Otero, R.D., Tessarollo, L., Livak, F., Manova, K., Bonner, W.M., Nussenzweig, M.C., and Nussenzweig, A. 2002. Genomic instability in mice lacking histone H2AX. Science (Washington, D.C.), 296: 922-927. (10.1126/science.1069398)
10.1083/jcb.152.2.375 / J. Cell Biol. by Chadwick B.P. (2001)
10.1083/jcb.200112074 / J. Cell Biol. by Chadwick B.P. (2002)
{'key': 'p_16/p_16_1', 'first-page': '165', 'volume': '273', 'author': 'Chen H.Y.', 'year': '1998', 'journal-title': 'J. Biol. Chem.'} / J. Biol. Chem. by Chen H.Y. (1998)
Chen, H.T., Bhandoola, A., Difilippantonio, M.J., Zhu, J., Brown, M.J., Tai, X., Rogakou, E.P., Brotz, T.M., Bonner, W.M., Ried, T., and Nussenzweig, A. 2000. Response to RAG-mediated VDJ cleavage by NBS1 and gamma-H2AX. Science (Washington, D.C.), 290: 1962-1965. (10.1126/science.290.5498.1962)
10.1016/S1097-2765(00)80256-7 / Mol. Cell by Cheung P. (2000)
10.1038/31275 / Nature (London) by Costanzi C. (1998)
10.1242/dev.127.11.2283 / Development by Costanzi C. (2000)
10.1093/geronj/46.2.B81 / J. Gerontol. by Dell-Orco R.T. (1991)
10.1074/jbc.C200348200 / J. Biol. Chem. by Dover J. (2002)
10.1038/35050000 / Nature by Downs J.A. (2000)
10.1016/S1097-2765(02)00508-7 / Mol. Cell by Forsburg S.L. (2002)
10.1146/annurev.biochem.71.090501.150203 / Rev. Biochem. by Gellert M. (2002)
Goebl, M.G., Yochem, J., Jentsch, S., McGrath, J.P., Varshavsky, A., and Byers, B. 1988. The yeast cell cycle gene CDC34 encodes a ubiquitin-conjugating enzyme. Science (Washington, D.C.), 241: 1331-1335. (10.1126/science.2842867)
10.1016/S0021-9258(19)40926-5 / J. Biol. Chem. by Goldknopf I.L. (1975)
10.1111/j.1432-1033.1978.tb12135.x / Eur. J. Biochem. by Gurley L.R. (1978)
10.1078/0171-9335-00123 / Eur. J. Cell Biol. by Hazzouri M. (2000)
10.1006/dbio.1995.1252 / Dev. Biol. by Hendriksen P.J. (1995)
10.1007/s004120050256 / Chromosoma by Hendzel M.J. (1997)
10.1073/pnas.97.2.716 / Proc. Natl. Acad. Sci. U.S.A. by Henikoff S. (2000)
10.1006/excr.2000.4951 / Exp. Cell Res. by Hoyer-Fender S. (2000)
10.1128/MCB.17.11.6693 / Mol. Cell Biol. by Huang H. (1997)
10.1038/85781 / Nat. Genet. by Hunter N. (2001)
10.1021/bi00455a019 / Biochemistry by Jackson V. (1990)
10.1074/jbc.M011153200 / J. Biol. Chem. by Jason L.J. (2001)
10.1002/bies.10038 / Bioessays by Jason L.J. (2002)
10.1038/329131a0 / Nature by Jentsch S. (1987)
10.1126/science.1063127 / Science by Jenuwein T. (2001)
10.1007/BF00042074 / Plant Mol. Biol. by Kapros T. (1995)
10.1242/jcs.113.18.3217 / J. Cell Sci. by Kaszas E. (2000)
Kistler, W.S. 1989. Histones and other basic nuclear proteins. Edited by Editor. Boca Raton, CRC Press.
10.1093/nar/9.11.2423 / Nucleic Acids Res. by Kleinschmidt A.M. (1981)
10.1073/pnas.082248899 / Proc. Natl. Acad. Sci. U.S.A. by Lahn B.T. (2002)
10.1016/S0167-4781(98)00098-0 / Biochim. Biophys. Acta by Lee Y. (1998)
10.1042/bj2960737 / Biochem. J. by Li W. (1993)
10.1016/S1097-2765(00)80257-9 / Mol. Cell by Lo W.S. (2000)
10.1038/38444 / Nature (London) by Luger K. (1997)
10.1016/0012-1606(82)90130-0 / Dev. Biol. by Mackay S. (1982)
10.1038/85830 / Nat. Genet. by Mahadevaiah S.K. (2001)
10.1007/BF00356023 / Chromosoma by McKee B.D. (1993)
10.1139/o02-081 / Biochem. Cell Biol. by Moore S.C. (2002)
10.1159/000015418 / Cytogenet. Cell Genet. by Motzkus D. (1999)
10.1016/S0021-9258(18)89191-8 / J. Biol. Chem. by Mueller R.D. (1985)
10.1016/0012-1606(82)90311-6 / Dev. Biol. by Newrock K.M. (1982)
10.1016/S0968-0004(00)01551-6 / Trends Biochem. Sci. by Ng H.H. (2000)
10.1021/bi00388a034 / Biochemistry by Nickel B.E. (1987)
10.1038/ng0398-257 / Nat. Genet. by Odorisio T. (1998)
10.1016/S0079-6603(08)60839-9 / Prog. Nucleic Acid Res. Mol. Biol. by Oliva R. (1991)
10.1126/science.1529340 / Science by Pehrson J.R. (1992)
10.1002/(SICI)1097-4644(199704)65:1<107::AID-JCB11>3.0.CO;2-H / J. Cell Biochem. by Pehrson J.R. (1997)
10.1038/414660a / Nature (London) by Petersen S. (2001)
10.1093/mutage/15.4.289 / Mutagenesis by Pfeiffer P. (2000)
10.1016/0012-1606(87)90181-3 / Dev. Biol. by Poccia D.L. (1987)
10.1093/nar/27.18.3685 / Nucleic Acids Res. by Rasmussen T.P. (1999)
10.1083/jcb.150.5.1189 / J. Cell Biol. by Rasmussen T.P. (2000)
10.1159/000015589 / Cytogenet. Cell Genet. by Richler C. (2000)
Robzyk, K., Recht, J., and Osley, M.A. 2000. Rad6-dependent ubiquitination of histone H2B in yeast. Science (Washington, D.C.), 287: 501-504. (10.1126/science.287.5452.501)
10.1016/S0092-8674(00)80154-3 / Cell by Roest H.P. (1996)
10.1016/S0531-5565(99)00046-7 / Exp. Gerontol. by Rogakou E.P. (1999)
Sassone-Corsi, P. 2002. Unique chromatin remodeling and transcriptional regulation in spermatogenesis. Science (Washington, D.C.), 296: 2176-2178. (10.1126/science.1070963)
10.1093/nar/9.13.3151 / Nucleic Acids Res. by Seale R.L. (1981)
10.1128/MCB.21.23.8035-8044.2001 / Mol. Cell. Biol. by Seigneurin-Berny D. (2001)
10.1016/S0378-1119(99)00405-9 / Gene by Spencer V.A. (1999)
10.1038/47412 / Nature (London) by Strahl B.D. (2000)
10.1128/MCB.22.5.1298-1306.2002 / Mol. Cell. Biol. by Strahl B.D. (2002)
10.1038/nature00883 / Nature (London) by Sun Z.W. (2002)
10.1038/81971 / Z. Nat. Struct. Biol. by Suto R.K. (2000)
10.1007/BF00292766 / Chromosoma by Tease C. (1989)
10.1002/j.1460-2075.1987.tb04852.x / EMBO J. by Thorne A.W. (1987)
10.1002/1521-1878(200009)22:9<836::AID-BIES9>3.0.CO;2-X / Bioessays by Turner B.M. (2000)
10.1242/jcs.114.18.3367 / J. Cell Sci. by Turner J.M. (2001)
10.1016/S0968-0004(97)01122-5 / Trends Biochem. Sci. by Varshavsky A. (1997)
10.1073/pnas.95.13.7480 / Proc. Natl. Acad. Sci. U.S.A. by Wei Y. (1998)
10.1016/S0092-8674(00)80718-7 / Cell by Wei Y. (1999)
10.1021/bi00555a022 / Biochemistry by West M.H. (1980)
10.1042/bj3290609 / Biochem. J. by Witt O. (1998)
10.1016/S0968-0004(00)01718-7 / Trends Biochem. Sci. by Wu J. (2000)
10.1016/S0021-9258(19)69296-3 / J. Biol. Chem. by Wu R.S. (1981)

Dates

Type	When
Created	22 years, 1 month ago (July 23, 2003, 12:08 p.m.)
Deposited	2 months ago (July 2, 2025, 2:19 p.m.)
Indexed	3 hours, 3 minutes ago (Sept. 6, 2025, 4:22 p.m.)
Issued	22 years, 3 months ago (June 1, 2003)
Published	22 years, 3 months ago (June 1, 2003)
Published Print	22 years, 3 months ago (June 1, 2003)

Funders 0

None

BibTeX

@article{Lewis_2003, title={A haploid affair: core histone transitions during spermatogenesis}, volume={81}, ISSN={1208-6002}, url={http://dx.doi.org/10.1139/o03-045}, DOI={10.1139/o03-045}, number={3}, journal={Biochemistry and Cell Biology}, publisher={Canadian Science Publishing}, author={Lewis, John D and Abbott, D Wade and Ausió, Juan}, year={2003}, month=jun, pages={131–140} }

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      "first-page": "586",
      "DOI": "10.1139/g95-075",
      "volume": "38",
      "author": "Akhmanova A.S.",
      "year": "1995",
      "journal-title": "Genome"
    },
    {
      "key": "p_5/p_5_1",
      "doi-asserted-by": "crossref",
      "first-page": "335",
      "DOI": "10.1007/s004120050255",
      "volume": "106",
      "author": "Akhmanova A.",
      "year": "1997",
      "journal-title": "Chromosoma"
    },
    {
      "key": "p_6/p_6_1",
      "doi-asserted-by": "crossref",
      "first-page": "5945",
      "DOI": "10.1021/bi020059d",
      "volume": "41",
      "author": "Ausi\u00f3 J.",
      "year": "2002",
      "journal-title": "Biochemistry"
    },
    {
      "key": "p_7/p_7_1",
      "doi-asserted-by": "crossref",
      "first-page": "693",
      "DOI": "10.1139/o01-147",
      "volume": "79",
      "author": "Ausi\u00f3 J.",
      "year": "2001",
      "journal-title": "Biochem. Cell Biol."
    },
    {
      "key": "p_8/p_8_1",
      "doi-asserted-by": "crossref",
      "first-page": "1",
      "DOI": "10.1007/s004120050218",
      "volume": "106",
      "author": "Ayoub N.",
      "year": "1997",
      "journal-title": "Chromosoma"
    },
    {
      "key": "p_9/p_9_1",
      "doi-asserted-by": "crossref",
      "first-page": "322",
      "DOI": "10.1006/dbio.1998.9155",
      "volume": "207",
      "author": "Baarends W.M.",
      "year": "1999",
      "journal-title": "Dev. Biol."
    },
    {
      "key": "p_10/p_10_1",
      "doi-asserted-by": "crossref",
      "first-page": "9",
      "DOI": "10.1002/bies.950140103",
      "volume": "14",
      "author": "Bradbury E.M.",
      "year": "1992",
      "journal-title": "Bioessays"
    },
    {
      "key": "p_11/p_11_1",
      "doi-asserted-by": "crossref",
      "first-page": "3286",
      "DOI": "10.1101/gad.940201",
      "volume": "15",
      "author": "Briggs S.D.",
      "year": "2001",
      "journal-title": "Genes Dev."
    },
    {
      "key": "p_12/p_12_1",
      "doi-asserted-by": "crossref",
      "first-page": "15",
      "DOI": "10.1016/S0968-0004(99)01516-9",
      "volume": "25",
      "author": "Brown C.E.",
      "year": "2000",
      "journal-title": "Trends Biochem. Sci."
    },
    {
      "key": "p_13/p_13_1",
      "doi-asserted-by": "crossref",
      "unstructured": "Celeste, A., Petersen, S., Romanienko, P.J., Fernandez-Capetillo, O., Chen, H.T., Sedelnikova, O.A., Reina-San-Martin, B., Coppola, V., Meffre, E., Difilippantonio, M.J., Redon, C., Pilch, D.R., Olaru, A., Eckhaus, M., Camerini-Otero, R.D., Tessarollo, L., Livak, F., Manova, K., Bonner, W.M., Nussenzweig, M.C., and Nussenzweig, A. 2002. Genomic instability in mice lacking histone H2AX. Science (Washington, D.C.), 296: 922-927.",
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    },
    {
      "key": "p_14/p_14_1",
      "doi-asserted-by": "crossref",
      "first-page": "375",
      "DOI": "10.1083/jcb.152.2.375",
      "volume": "152",
      "author": "Chadwick B.P.",
      "year": "2001",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "p_15/p_15_1",
      "doi-asserted-by": "crossref",
      "first-page": "1113",
      "DOI": "10.1083/jcb.200112074",
      "volume": "157",
      "author": "Chadwick B.P.",
      "year": "2002",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "p_16/p_16_1",
      "first-page": "165",
      "volume": "273",
      "author": "Chen H.Y.",
      "year": "1998",
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    },
    {
      "key": "p_17/p_17_1",
      "doi-asserted-by": "crossref",
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      "DOI": "10.1126/science.290.5498.1962"
    },
    {
      "key": "p_18/p_18_1",
      "doi-asserted-by": "crossref",
      "first-page": "905",
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      "author": "Cheung P.",
      "year": "2000",
      "journal-title": "Mol. Cell"
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    {
      "key": "p_19/p_19_1",
      "doi-asserted-by": "crossref",
      "first-page": "599",
      "DOI": "10.1038/31275",
      "volume": "393",
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      "year": "1998",
      "journal-title": "Nature (London)"
    },
    {
      "key": "p_20/p_20_1",
      "doi-asserted-by": "crossref",
      "first-page": "2283",
      "DOI": "10.1242/dev.127.11.2283",
      "volume": "127",
      "author": "Costanzi C.",
      "year": "2000",
      "journal-title": "Development"
    },
    {
      "key": "p_21/p_21_1",
      "doi-asserted-by": "crossref",
      "first-page": "B81",
      "DOI": "10.1093/geronj/46.2.B81",
      "volume": "46",
      "author": "Dell-Orco R.T.",
      "year": "1991",
      "journal-title": "J. Gerontol."
    },
    {
      "key": "p_22/p_22_1",
      "doi-asserted-by": "crossref",
      "first-page": "368",
      "DOI": "10.1074/jbc.C200348200",
      "volume": "277",
      "author": "Dover J.",
      "year": "2002",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "p_23/p_23_1",
      "doi-asserted-by": "crossref",
      "first-page": "1001",
      "DOI": "10.1038/35050000",
      "volume": "408",
      "author": "Downs J.A.",
      "year": "2000",
      "journal-title": "Nature"
    },
    {
      "key": "p_24/p_24_1",
      "doi-asserted-by": "crossref",
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      "author": "Forsburg S.L.",
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    },
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      "key": "p_25/p_25_1",
      "doi-asserted-by": "crossref",
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      "volume": "71",
      "author": "Gellert M.",
      "year": "2002",
      "journal-title": "Rev. Biochem."
    },
    {
      "key": "p_26/p_26_1",
      "doi-asserted-by": "crossref",
      "unstructured": "Goebl, M.G., Yochem, J., Jentsch, S., McGrath, J.P., Varshavsky, A., and Byers, B. 1988. The yeast cell cycle gene CDC34 encodes a ubiquitin-conjugating enzyme. Science (Washington, D.C.), 241: 1331-1335.",
      "DOI": "10.1126/science.2842867"
    },
    {
      "key": "p_27/p_27_1",
      "doi-asserted-by": "crossref",
      "first-page": "7182",
      "DOI": "10.1016/S0021-9258(19)40926-5",
      "volume": "250",
      "author": "Goldknopf I.L.",
      "year": "1975",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "p_28/p_28_1",
      "doi-asserted-by": "crossref",
      "first-page": "1",
      "DOI": "10.1111/j.1432-1033.1978.tb12135.x",
      "volume": "84",
      "author": "Gurley L.R.",
      "year": "1978",
      "journal-title": "Eur. J. Biochem."
    },
    {
      "key": "p_29/p_29_1",
      "doi-asserted-by": "crossref",
      "first-page": "950",
      "DOI": "10.1078/0171-9335-00123",
      "volume": "79",
      "author": "Hazzouri M.",
      "year": "2000",
      "journal-title": "Eur. J. Cell Biol."
    },
    {
      "key": "p_30/p_30_1",
      "doi-asserted-by": "crossref",
      "first-page": "730",
      "DOI": "10.1006/dbio.1995.1252",
      "volume": "170",
      "author": "Hendriksen P.J.",
      "year": "1995",
      "journal-title": "Dev. Biol."
    },
    {
      "key": "p_31/p_31_1",
      "doi-asserted-by": "crossref",
      "first-page": "348",
      "DOI": "10.1007/s004120050256",
      "volume": "106",
      "author": "Hendzel M.J.",
      "year": "1997",
      "journal-title": "Chromosoma"
    },
    {
      "key": "p_32/p_32_1",
      "doi-asserted-by": "crossref",
      "first-page": "716",
      "DOI": "10.1073/pnas.97.2.716",
      "volume": "97",
      "author": "Henikoff S.",
      "year": "2000",
      "journal-title": "Proc. Natl. Acad. Sci. U.S.A."
    },
    {
      "key": "p_33/p_33_1",
      "doi-asserted-by": "crossref",
      "first-page": "254",
      "DOI": "10.1006/excr.2000.4951",
      "volume": "258",
      "author": "Hoyer-Fender S.",
      "year": "2000",
      "journal-title": "Exp. Cell Res."
    },
    {
      "key": "p_34/p_34_1",
      "doi-asserted-by": "crossref",
      "first-page": "6693",
      "DOI": "10.1128/MCB.17.11.6693",
      "volume": "17",
      "author": "Huang H.",
      "year": "1997",
      "journal-title": "Mol. Cell Biol."
    },
    {
      "key": "p_35/p_35_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_36/p_36_1",
      "doi-asserted-by": "crossref",
      "first-page": "719",
      "DOI": "10.1021/bi00455a019",
      "volume": "29",
      "author": "Jackson V.",
      "year": "1990",
      "journal-title": "Biochemistry"
    },
    {
      "key": "p_37/p_37_1",
      "doi-asserted-by": "crossref",
      "first-page": "597",
      "DOI": "10.1074/jbc.M011153200",
      "volume": "276",
      "author": "Jason L.J.",
      "year": "2001",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "p_38/p_38_1",
      "doi-asserted-by": "crossref",
      "first-page": "166",
      "DOI": "10.1002/bies.10038",
      "volume": "24",
      "author": "Jason L.J.",
      "year": "2002",
      "journal-title": "Bioessays"
    },
    {
      "key": "p_39/p_39_1",
      "doi-asserted-by": "crossref",
      "first-page": "131",
      "DOI": "10.1038/329131a0",
      "volume": "329",
      "author": "Jentsch S.",
      "year": "1987",
      "journal-title": "Nature"
    },
    {
      "key": "p_40/p_40_1",
      "doi-asserted-by": "crossref",
      "first-page": "1074",
      "DOI": "10.1126/science.1063127",
      "volume": "293",
      "author": "Jenuwein T.",
      "year": "2001",
      "journal-title": "Science"
    },
    {
      "key": "p_41/p_41_1",
      "doi-asserted-by": "crossref",
      "first-page": "901",
      "DOI": "10.1007/BF00042074",
      "volume": "28",
      "author": "Kapros T.",
      "year": "1995",
      "journal-title": "Plant Mol. Biol."
    },
    {
      "key": "p_42/p_42_1",
      "doi-asserted-by": "crossref",
      "first-page": "3217",
      "DOI": "10.1242/jcs.113.18.3217",
      "volume": "113",
      "author": "Kaszas E.",
      "year": "2000",
      "journal-title": "J. Cell Sci."
    },
    {
      "key": "p_43/p_43_1",
      "unstructured": "Kistler, W.S. 1989. Histones and other basic nuclear proteins. Edited by Editor. Boca Raton, CRC Press."
    },
    {
      "key": "p_44/p_44_1",
      "doi-asserted-by": "crossref",
      "first-page": "2423",
      "DOI": "10.1093/nar/9.11.2423",
      "volume": "9",
      "author": "Kleinschmidt A.M.",
      "year": "1981",
      "journal-title": "Nucleic Acids Res."
    },
    {
      "key": "p_45/p_45_1",
      "doi-asserted-by": "crossref",
      "first-page": "8707",
      "DOI": "10.1073/pnas.082248899",
      "volume": "99",
      "author": "Lahn B.T.",
      "year": "2002",
      "journal-title": "Proc. Natl. Acad. Sci. U.S.A."
    },
    {
      "key": "p_46/p_46_1",
      "doi-asserted-by": "crossref",
      "first-page": "73",
      "DOI": "10.1016/S0167-4781(98)00098-0",
      "volume": "1399",
      "author": "Lee Y.",
      "year": "1998",
      "journal-title": "Biochim. Biophys. Acta"
    },
    {
      "key": "p_47/p_47_1",
      "doi-asserted-by": "crossref",
      "first-page": "737",
      "DOI": "10.1042/bj2960737",
      "volume": "296",
      "author": "Li W.",
      "year": "1993",
      "journal-title": "Biochem. J."
    },
    {
      "key": "p_48/p_48_1",
      "doi-asserted-by": "crossref",
      "first-page": "917",
      "DOI": "10.1016/S1097-2765(00)80257-9",
      "volume": "5",
      "author": "Lo W.S.",
      "year": "2000",
      "journal-title": "Mol. Cell"
    },
    {
      "key": "p_49/p_49_1",
      "doi-asserted-by": "crossref",
      "first-page": "251",
      "DOI": "10.1038/38444",
      "volume": "389",
      "author": "Luger K.",
      "year": "1997",
      "journal-title": "Nature (London)"
    },
    {
      "key": "p_50/p_50_1",
      "doi-asserted-by": "crossref",
      "first-page": "430",
      "DOI": "10.1016/0012-1606(82)90130-0",
      "volume": "93",
      "author": "Mackay S.",
      "year": "1982",
      "journal-title": "Dev. Biol."
    },
    {
      "key": "p_51/p_51_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_52/p_52_1",
      "doi-asserted-by": "crossref",
      "first-page": "71",
      "DOI": "10.1007/BF00356023",
      "volume": "102",
      "author": "McKee B.D.",
      "year": "1993",
      "journal-title": "Chromosoma"
    },
    {
      "key": "p_53/p_53_1",
      "doi-asserted-by": "crossref",
      "first-page": "311",
      "DOI": "10.1139/o02-081",
      "volume": "80",
      "author": "Moore S.C.",
      "year": "2002",
      "journal-title": "Biochem. Cell Biol."
    },
    {
      "key": "p_54/p_54_1",
      "doi-asserted-by": "crossref",
      "first-page": "83",
      "DOI": "10.1159/000015418",
      "volume": "86",
      "author": "Motzkus D.",
      "year": "1999",
      "journal-title": "Cytogenet. Cell Genet."
    },
    {
      "key": "p_55/p_55_1",
      "doi-asserted-by": "crossref",
      "first-page": "5147",
      "DOI": "10.1016/S0021-9258(18)89191-8",
      "volume": "260",
      "author": "Mueller R.D.",
      "year": "1985",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "p_56/p_56_1",
      "doi-asserted-by": "crossref",
      "first-page": "248",
      "DOI": "10.1016/0012-1606(82)90311-6",
      "volume": "89",
      "author": "Newrock K.M.",
      "year": "1982",
      "journal-title": "Dev. Biol."
    },
    {
      "key": "p_57/p_57_1",
      "doi-asserted-by": "crossref",
      "first-page": "121",
      "DOI": "10.1016/S0968-0004(00)01551-6",
      "volume": "25",
      "author": "Ng H.H.",
      "year": "2000",
      "journal-title": "Trends Biochem. Sci."
    },
    {
      "key": "p_58/p_58_1",
      "doi-asserted-by": "crossref",
      "first-page": "4417",
      "DOI": "10.1021/bi00388a034",
      "volume": "26",
      "author": "Nickel B.E.",
      "year": "1987",
      "journal-title": "Biochemistry"
    },
    {
      "key": "p_59/p_59_1",
      "doi-asserted-by": "crossref",
      "first-page": "257",
      "DOI": "10.1038/ng0398-257",
      "volume": "18",
      "author": "Odorisio T.",
      "year": "1998",
      "journal-title": "Nat. Genet."
    },
    {
      "key": "p_60/p_60_1",
      "doi-asserted-by": "crossref",
      "first-page": "25",
      "DOI": "10.1016/S0079-6603(08)60839-9",
      "volume": "40",
      "author": "Oliva R.",
      "year": "1991",
      "journal-title": "Prog. Nucleic Acid Res. Mol. Biol."
    },
    {
      "key": "p_61/p_61_1",
      "doi-asserted-by": "crossref",
      "first-page": "1398",
      "DOI": "10.1126/science.1529340",
      "volume": "257",
      "author": "Pehrson J.R.",
      "year": "1992",
      "journal-title": "Science"
    },
    {
      "key": "p_62/p_62_1",
      "doi-asserted-by": "crossref",
      "first-page": "107",
      "DOI": "10.1002/(SICI)1097-4644(199704)65:1<107::AID-JCB11>3.0.CO;2-H",
      "volume": "65",
      "author": "Pehrson J.R.",
      "year": "1997",
      "journal-title": "J. Cell Biochem."
    },
    {
      "key": "p_63/p_63_1",
      "doi-asserted-by": "crossref",
      "first-page": "660",
      "DOI": "10.1038/414660a",
      "volume": "414",
      "author": "Petersen S.",
      "year": "2001",
      "journal-title": "Nature (London)"
    },
    {
      "key": "p_64/p_64_1",
      "doi-asserted-by": "crossref",
      "first-page": "289",
      "DOI": "10.1093/mutage/15.4.289",
      "volume": "15",
      "author": "Pfeiffer P.",
      "year": "2000",
      "journal-title": "Mutagenesis"
    },
    {
      "key": "p_65/p_65_1",
      "doi-asserted-by": "crossref",
      "first-page": "445",
      "DOI": "10.1016/0012-1606(87)90181-3",
      "volume": "121",
      "author": "Poccia D.L.",
      "year": "1987",
      "journal-title": "Dev. Biol."
    },
    {
      "key": "p_66/p_66_1",
      "doi-asserted-by": "crossref",
      "first-page": "3685",
      "DOI": "10.1093/nar/27.18.3685",
      "volume": "27",
      "author": "Rasmussen T.P.",
      "year": "1999",
      "journal-title": "Nucleic Acids Res."
    },
    {
      "key": "p_67/p_67_1",
      "doi-asserted-by": "crossref",
      "first-page": "1189",
      "DOI": "10.1083/jcb.150.5.1189",
      "volume": "150",
      "author": "Rasmussen T.P.",
      "year": "2000",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "p_68/p_68_1",
      "doi-asserted-by": "crossref",
      "first-page": "118",
      "DOI": "10.1159/000015589",
      "volume": "89",
      "author": "Richler C.",
      "year": "2000",
      "journal-title": "Cytogenet. Cell Genet."
    },
    {
      "key": "p_69/p_69_1",
      "doi-asserted-by": "crossref",
      "unstructured": "Robzyk, K., Recht, J., and Osley, M.A. 2000. Rad6-dependent ubiquitination of histone H2B in yeast. Science (Washington, D.C.), 287: 501-504.",
      "DOI": "10.1126/science.287.5452.501"
    },
    {
      "key": "p_70/p_70_1",
      "doi-asserted-by": "crossref",
      "first-page": "799",
      "DOI": "10.1016/S0092-8674(00)80154-3",
      "volume": "86",
      "author": "Roest H.P.",
      "year": "1996",
      "journal-title": "Cell"
    },
    {
      "key": "p_71/p_71_1",
      "doi-asserted-by": "crossref",
      "first-page": "741",
      "DOI": "10.1016/S0531-5565(99)00046-7",
      "volume": "34",
      "author": "Rogakou E.P.",
      "year": "1999",
      "journal-title": "Exp. Gerontol."
    },
    {
      "key": "p_72/p_72_1",
      "doi-asserted-by": "crossref",
      "unstructured": "Sassone-Corsi, P. 2002. Unique chromatin remodeling and transcriptional regulation in spermatogenesis. Science (Washington, D.C.), 296: 2176-2178.",
      "DOI": "10.1126/science.1070963"
    },
    {
      "key": "p_73/p_73_1",
      "doi-asserted-by": "crossref",
      "first-page": "3151",
      "DOI": "10.1093/nar/9.13.3151",
      "volume": "9",
      "author": "Seale R.L.",
      "year": "1981",
      "journal-title": "Nucleic Acids Res."
    },
    {
      "key": "p_74/p_74_1",
      "doi-asserted-by": "crossref",
      "first-page": "8035",
      "DOI": "10.1128/MCB.21.23.8035-8044.2001",
      "volume": "21",
      "author": "Seigneurin-Berny D.",
      "year": "2001",
      "journal-title": "Mol. Cell. Biol."
    },
    {
      "key": "p_75/p_75_1",
      "doi-asserted-by": "crossref",
      "first-page": "1",
      "DOI": "10.1016/S0378-1119(99)00405-9",
      "volume": "240",
      "author": "Spencer V.A.",
      "year": "1999",
      "journal-title": "Gene"
    },
    {
      "key": "p_76/p_76_1",
      "doi-asserted-by": "crossref",
      "first-page": "41",
      "DOI": "10.1038/47412",
      "volume": "403",
      "author": "Strahl B.D.",
      "year": "2000",
      "journal-title": "Nature (London)"
    },
    {
      "key": "p_77/p_77_1",
      "doi-asserted-by": "crossref",
      "first-page": "1298",
      "DOI": "10.1128/MCB.22.5.1298-1306.2002",
      "volume": "22",
      "author": "Strahl B.D.",
      "year": "2002",
      "journal-title": "Mol. Cell. Biol."
    },
    {
      "key": "p_78/p_78_1",
      "doi-asserted-by": "crossref",
      "first-page": "104",
      "DOI": "10.1038/nature00883",
      "volume": "418",
      "author": "Sun Z.W.",
      "year": "2002",
      "journal-title": "Nature (London)"
    },
    {
      "key": "p_79/p_79_1",
      "doi-asserted-by": "crossref",
      "first-page": "1121",
      "DOI": "10.1038/81971",
      "volume": "7",
      "author": "Suto R.K.",
      "year": "2000",
      "journal-title": "Z. Nat. Struct. Biol."
    },
    {
      "key": "p_80/p_80_1",
      "doi-asserted-by": "crossref",
      "first-page": "390",
      "DOI": "10.1007/BF00292766",
      "volume": "97",
      "author": "Tease C.",
      "year": "1989",
      "journal-title": "Chromosoma"
    },
    {
      "key": "p_81/p_81_1",
      "doi-asserted-by": "crossref",
      "first-page": "1005",
      "DOI": "10.1002/j.1460-2075.1987.tb04852.x",
      "volume": "6",
      "author": "Thorne A.W.",
      "year": "1987",
      "journal-title": "EMBO J."
    },
    {
      "key": "p_82/p_82_1",
      "doi-asserted-by": "crossref",
      "first-page": "836",
      "DOI": "10.1002/1521-1878(200009)22:9<836::AID-BIES9>3.0.CO;2-X",
      "volume": "22",
      "author": "Turner B.M.",
      "year": "2000",
      "journal-title": "Bioessays"
    },
    {
      "key": "p_83/p_83_1",
      "doi-asserted-by": "crossref",
      "first-page": "3367",
      "DOI": "10.1242/jcs.114.18.3367",
      "volume": "114",
      "author": "Turner J.M.",
      "year": "2001",
      "journal-title": "J. Cell Sci."
    },
    {
      "key": "p_84/p_84_1",
      "doi-asserted-by": "crossref",
      "first-page": "383",
      "DOI": "10.1016/S0968-0004(97)01122-5",
      "volume": "22",
      "author": "Varshavsky A.",
      "year": "1997",
      "journal-title": "Trends Biochem. Sci."
    },
    {
      "key": "p_85/p_85_1",
      "doi-asserted-by": "crossref",
      "first-page": "7480",
      "DOI": "10.1073/pnas.95.13.7480",
      "volume": "95",
      "author": "Wei Y.",
      "year": "1998",
      "journal-title": "Proc. Natl. Acad. Sci. U.S.A."
    },
    {
      "key": "p_86/p_86_1",
      "doi-asserted-by": "crossref",
      "first-page": "99",
      "DOI": "10.1016/S0092-8674(00)80718-7",
      "volume": "97",
      "author": "Wei Y.",
      "year": "1999",
      "journal-title": "Cell"
    },
    {
      "key": "p_87/p_87_1",
      "doi-asserted-by": "crossref",
      "first-page": "3238",
      "DOI": "10.1021/bi00555a022",
      "volume": "19",
      "author": "West M.H.",
      "year": "1980",
      "journal-title": "Biochemistry"
    },
    {
      "key": "p_88/p_88_1",
      "doi-asserted-by": "crossref",
      "first-page": "609",
      "DOI": "10.1042/bj3290609",
      "volume": "329",
      "author": "Witt O.",
      "year": "1998",
      "journal-title": "Biochem. J."
    },
    {
      "key": "p_89/p_89_1",
      "doi-asserted-by": "crossref",
      "first-page": "619",
      "DOI": "10.1016/S0968-0004(00)01718-7",
      "volume": "25",
      "author": "Wu J.",
      "year": "2000",
      "journal-title": "Trends Biochem. Sci."
    },
    {
      "key": "p_90/p_90_1",
      "doi-asserted-by": "crossref",
      "first-page": "5916",
      "DOI": "10.1016/S0021-9258(19)69296-3",
      "volume": "256",
      "author": "Wu R.S.",
      "year": "1981",
      "journal-title": "J. Biol. Chem."
    }
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