DOI: 10.1083/jcb.153.1.101. Centromeres Are Specialized Replication Domains in Heterochromatin

Centromeres Are Specialized Replication Domains in Heterochromatin

10.1083/jcb.153.1.101

Crossref journal-article

Rockefeller University Press

The Journal of Cell Biology (291)

Abstract

The properties that define centromeres in complex eukaryotes are poorly understood because the underlying DNA is normally repetitive and indistinguishable from surrounding noncentromeric sequences. However, centromeric chromatin contains variant H3-like histones that may specify centromeric regions. Nucleosomes are normally assembled during DNA replication; therefore, we examined replication and chromatin assembly at centromeres in Drosophila cells. DNA in pericentric heterochromatin replicates late in S phase, and so centromeres are also thought to replicate late. In contrast to expectation, we show that centromeres replicate as isolated domains early in S phase. These domains do not appear to assemble conventional H3-containing nucleosomes, and deposition of the Cid centromeric H3-like variant proceeds by a replication-independent pathway. We suggest that late-replicating pericentric heterochromatin helps to maintain embedded centromeres by blocking conventional nucleosome assembly early in S phase, thereby allowing the deposition of centromeric histones.

Bibliography

Ahmad, K., & Henikoff, S. (2001). Centromeres Are Specialized Replication Domains in Heterochromatin. The Journal of Cell Biology, 153(1), 101â110.

Authors 2

Kami Ahmad (first)
Steven Henikoff (additional)

References 53 Referenced 114

10.1016/S0959-437X(99)80028-8 / Curr. Opin. Genet. Dev. / Chromatin assemblybiochemical identities and genetic redundancy by Adams (1999)
10.1126/science.287.5461.2185 / Science. / The genome sequence of Drosophila melanogaster by Adams (2000)
10.1101/gad.9.2.218 / Genes Dev. / Mutations derepressing silent centromeric domains in fission yeast disrupt chromosome segregation by Allshire (1995)
10.1016/0014-4827(66)90399-5 / Exp. Cell. Res. / In vitro study of the DNA replication patterns of somatic chromosomes of Drosophila melanogaster by Barigozzi (1966)
10.1016/S0168-9525(00)89100-3 / Trends Genet. / Centromere activation by Brown (1995)
10.1038/44062 / Nature. / A histone-H3-like protein in C. elegans by Buchwitz (1999)
10.1016/S0962-8924(00)01739-6 / Trends Cell Biol. / Centromerization by Choo (2000)
10.1016/0168-9525(90)90149-Z / Trends Genet. / Centromeres of budding and fission yeast by Clarke (1990)
10.1126/science.286.5449.2468 / Science. / Genetic definition and sequence analysis of Arabidopsis centromeres by Copenhaver (1999)
10.1016/S0168-9525(98)01444-9 / Trends Genet. / Something from nothingthe evolution and utility of satellite repeats by Csink (1998)
10.1007/BF02114171 / Experientia. / The cell cycle of an established line of Drosophila melanogaster cells in vitro by Dolfini (1970)
{'key': '2023072211302755500_Dupraw1968', 'volume-title': 'Cell and Molecular Biology', 'author': 'Dupraw', 'year': '1968'} / Cell and Molecular Biology by Dupraw (1968)
{'key': '2023072211302755500_Echalier1997', 'volume-title': 'Drosophila Cells in Culture', 'author': 'Echalier', 'year': '1997'} / Drosophila Cells in Culture by Echalier (1997)
10.1016/S0959-437X(96)80050-5 / Curr. Opin. Genet. Dev. / Heterochromatin and gene regulation in Drosophila by Elgin (1996)
{'key': '2023072211302755500_Foeetal1993', 'first-page': '149', 'article-title': 'Mitosis and morphogenesis in the Drosophila embryopoint and counterpoint', 'volume-title': 'The Development of Drosophila melanogaster', 'author': 'Foe', 'year': '1993'} / The Development of Drosophila melanogaster / Mitosis and morphogenesis in the Drosophila embryopoint and counterpoint by Foe (1993)
10.1073/pnas.97.2.716 / Proc. Natl. Acad. Sci. USA. / Heterochromatic deposition of centromeric histone H3-like proteins by Henikoff (2000)
10.1083/jcb.120.3.591 / J. Cell Biol. / The onset of homologous chromosome pairing during Drosophila melanogaster embryogenesis by Hiraoka (1993)
10.1016/S0960-9822(98)70156-3 / Curr. Biol. / Histone-GFP fusion protein enables sensitive analysis of chromosome dynamics in living mammalian cells by Kanda (1998)
10.1016/S0168-9525(97)01298-5 / Trends Genet. / The case for epigenetic effects on centromere identity and function by Karpen (1997)
10.1007/s004120050384 / Chromosoma. / Nuclear organization studied with the help of a hypotonic shiftits use permits hydrophilic molecules to enter into living cells by Koberna (1999)
10.1073/pnas.71.1.135 / Proc. Natl. Acad. Sci. USA. / Mechanism of DNA replication in Drosophila chromosomesstructure of replication forks and evidence for bidirectionality by Kriegstein (1974)
10.1006/excr.1995.1320 / Exp. Cell Res. / Chromatin assembly factor 1 (CAF-1) colocalizes with replication foci in HeLa cell nuclei by Krude (1995)
10.1046/j.1432-1327.1999.00508.x / Eur. J. Biochem. / Chromatin assembly during DNA replication in somatic cells by Krude (1999)
10.1038/217138a0 / Nature. / Late DNA synthesis in heterochromatin by Lima-de-Faria (1968)
10.1101/gr.9.10.895 / Genome Res. / Extreme reduction of chromosome-specific alpha-satellite array is unusually common in human chromosome 21 by Lo (1999)
10.1083/jcb.143.6.1415 / J. Cell Biol. / Spatial and temporal dynamics of DNA replication sites in mammalian cells by Ma (1998)
10.1242/jcs.103.3.857 / J. Cell Sci. / Dynamics of three-dimensional replication patterns during the S-phase, analyzed by double labelling of DNA and confocal microscopy by Manders (1992)
10.1016/0092-8674(88)90072-4 / Cell. / Time of replication of yeast centromeres and telomeres by McCarroll (1988)
10.1101/gad.11.24.3401 / Genes Dev. / Budding yeast centromere composition and assembly as revealed by in vivo cross-linking by Meluh (1997)
10.1016/0092-8674(95)90032-2 / Cell. / Localization of centromere function in a Drosophila minichromosome by Murphy (1995)
10.1016/S0092-8674(00)81158-7 / Cell. / Centromeres take flightalpha satellite and the quest for the human centromere by Murphy (1998)
10.1073/pnas.96.20.11434 / Proc. Natl. Acad. Sci. USA. / Position effect of human telomeric repeats on replication timing by Ofir (1999)
10.1083/jcb.116.5.1095 / J. Cell. Biol. / Dynamic organization of DNA replication in mammalian cell nucleispatially and temporally defined replication of chromosome-specific alpha-satellite DNA sequences by O'Keefe (1992)
10.1146/annurev.bi.60.070191.004143 / Annu. Rev. Biochem. / The regulation of histone synthesis in the cell cycle by Osley (1991)
10.1083/jcb.104.4.805 / J. Cell Biol. / A 17-kD centromere protein (CENP-A) copurifies with nucleosome core particles and with histones by Palmer (1987)
10.1007/BF00337600 / Chromosoma. / The centromere specific histone CENP-A is selectively retained in discrete foci in mammalian sperm nuclei by Palmer (1990)
10.1073/pnas.88.9.3734 / Proc. Natl. Acad. Sci. USA. / Purification of the centromere-specific protein CENP-A and demonstration that it is a distinctive histone by Palmer (1991)
10.1093/hmg/9.2.175 / Hum. Mol. Genet. / Human centromeres and neocentromeres show identical distribution patterns of >20 functionally important kinetochore-associated proteins by Saffery (2000)
10.1083/jcb.136.3.501 / J. Cell Biol. / Assembly of CENP-A into centromeric chromatin requires a cooperative array of nucleosomal DNA contact sites by Shelby (1997)
10.1128/MCB.21.7.2555-2569.2001 / Mol. Cell. Biol. / The hinge and chromoshadow domain impart distinct targeting of HP1-like proteins by Smothers (2001)
10.1101/gad.13.2.146 / Genes Dev. / Telomeric chromatin modulates replication timing near chromosome ends by Stevenson (1999)
10.1101/gad.9.5.573 / Genes Dev. / A mutation in CSE4, an essential gene encoding a novel chromatin-associated protein in yeast, causes chromosome nondisjunction and cell cycle arrest at mitosis by Stoler (1995)
10.1016/S0092-8674(00)80491-2 / Cell. / Molecular structure of a functional Drosophila centromere by Sun (1997)
10.1126/science.288.5474.2215 / Science. / Requirement of Mis6 centromere connector for localizing a CENP-A-like protein in fission yeast by Takahashi (2000)
10.1016/S0092-8674(00)00004-0 / Cell / Many paths to the top of the mountaindiverse evolutionary solutions to centromere structure by Tyler-Smith (2000)
10.1096/fasebj.13.9002.S216 / FASEB J. / The mammalian centromerestructural domains and the attenuation of chromatin modelling by van Hooser (1999)
10.1038/74487 / Nat. Biotech. / Identification of in vivo DNA targets of chromatin proteins using tethered dam methyltransferase by van Steensel (2000)
10.1016/S0092-8674(00)81326-4 / Cell. / Nucleosome assembly by a complex of CAF-1 and acetylated histones H3/H4 by Verreault (1996)
10.1086/302924 / Am. J. Hum. Genet. / Molecular cytogenetic analysis of eight inversion duplications of human chromosome 13q that each contain a neocentromere by Warburton (2000)
10.1016/S0959-437X(98)80144-5 / Curr. Opin. Genet. Dev. / Centromeresthe missing link in the development of human artificial chromosomes by Willard (1998)
10.3109/10409238609083735 / CRC Crit. Rev. Biochem. / Histones and their modifications by Wu (1986)
10.1093/hmg/9.12.1891 / Hum. Mol. Genet. / Human mini-chromosomes with minimal centromeres by Yang (2000)
10.1073/pnas.130189697 / Proc. Natl. Acad. Sci. USA. / Human centromere protein A (CENP-A) can replace histone H3 in nucleosome reconstitution in vitro by Yoda (2000)

Dates

Type	When
Created	23 years, 1 month ago (July 26, 2002, 12:46 p.m.)
Deposited	2 years, 1 month ago (July 22, 2023, 7:31 a.m.)
Indexed	4 weeks ago (Aug. 6, 2025, 8:22 a.m.)
Issued	24 years, 5 months ago (April 2, 2001)
Published	24 years, 5 months ago (April 2, 2001)
Published Online	24 years, 5 months ago (April 2, 2001)
Published Print	24 years, 5 months ago (April 2, 2001)

Funders 0

None

BibTeX

@article{Ahmad_2001, title={Centromeres Are Specialized Replication Domains in Heterochromatin}, volume={153}, ISSN={1540-8140}, url={http://dx.doi.org/10.1083/jcb.153.1.101}, DOI={10.1083/jcb.153.1.101}, number={1}, journal={The Journal of Cell Biology}, publisher={Rockefeller University Press}, author={Ahmad, Kami and Henikoff, Steven}, year={2001}, month=apr, pages={101–110} }

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    },
    {
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      "article-title": "The genome sequence of Drosophila melanogaster",
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      "author": "Adams",
      "year": "2000",
      "journal-title": "Science."
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    {
      "key": "2023072211302755500_Allshireetal1995",
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      "first-page": "218",
      "DOI": "10.1101/gad.9.2.218",
      "article-title": "Mutations derepressing silent centromeric domains in fission yeast disrupt chromosome segregation",
      "volume": "9",
      "author": "Allshire",
      "year": "1995",
      "journal-title": "Genes Dev."
    },
    {
      "key": "2023072211302755500_Barigozzietal1966",
      "doi-asserted-by": "crossref",
      "first-page": "231",
      "DOI": "10.1016/0014-4827(66)90399-5",
      "article-title": "In vitro study of the DNA replication patterns of somatic chromosomes of Drosophila melanogaster",
      "volume": "43",
      "author": "Barigozzi",
      "year": "1966",
      "journal-title": "Exp. Cell. Res."
    },
    {
      "key": "2023072211302755500_BrownandTyler-Smith1995",
      "doi-asserted-by": "crossref",
      "first-page": "337",
      "DOI": "10.1016/S0168-9525(00)89100-3",
      "article-title": "Centromere activation",
      "volume": "11",
      "author": "Brown",
      "year": "1995",
      "journal-title": "Trends Genet."
    },
    {
      "key": "2023072211302755500_Buchwitzetal1999",
      "doi-asserted-by": "crossref",
      "first-page": "547",
      "DOI": "10.1038/44062",
      "article-title": "A histone-H3-like protein in C. elegans",
      "volume": "401",
      "author": "Buchwitz",
      "year": "1999",
      "journal-title": "Nature."
    },
    {
      "key": "2023072211302755500_Choo2000",
      "doi-asserted-by": "crossref",
      "first-page": "182",
      "DOI": "10.1016/S0962-8924(00)01739-6",
      "article-title": "Centromerization",
      "volume": "10",
      "author": "Choo",
      "year": "2000",
      "journal-title": "Trends Cell Biol."
    },
    {
      "key": "2023072211302755500_Clarke1990",
      "doi-asserted-by": "crossref",
      "first-page": "150",
      "DOI": "10.1016/0168-9525(90)90149-Z",
      "article-title": "Centromeres of budding and fission yeast",
      "volume": "6",
      "author": "Clarke",
      "year": "1990",
      "journal-title": "Trends Genet."
    },
    {
      "key": "2023072211302755500_Copenhaveretal1999",
      "doi-asserted-by": "crossref",
      "first-page": "2468",
      "DOI": "10.1126/science.286.5449.2468",
      "article-title": "Genetic definition and sequence analysis of Arabidopsis centromeres",
      "volume": "286",
      "author": "Copenhaver",
      "year": "1999",
      "journal-title": "Science."
    },
    {
      "key": "2023072211302755500_CsinkandHenikoff1998",
      "doi-asserted-by": "crossref",
      "first-page": "200",
      "DOI": "10.1016/S0168-9525(98)01444-9",
      "article-title": "Something from nothingthe evolution and utility of satellite repeats",
      "volume": "14",
      "author": "Csink",
      "year": "1998",
      "journal-title": "Trends Genet."
    },
    {
      "key": "2023072211302755500_Dolfinietal1970",
      "doi-asserted-by": "crossref",
      "first-page": "1020",
      "DOI": "10.1007/BF02114171",
      "article-title": "The cell cycle of an established line of Drosophila melanogaster cells in vitro",
      "volume": "26",
      "author": "Dolfini",
      "year": "1970",
      "journal-title": "Experientia."
    },
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      "key": "2023072211302755500_Dupraw1968",
      "volume-title": "Cell and Molecular Biology",
      "author": "Dupraw",
      "year": "1968"
    },
    {
      "key": "2023072211302755500_Echalier1997",
      "volume-title": "Drosophila Cells in Culture",
      "author": "Echalier",
      "year": "1997"
    },
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      "key": "2023072211302755500_Elgin1996",
      "doi-asserted-by": "crossref",
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      "article-title": "Heterochromatin and gene regulation in Drosophila",
      "volume": "6",
      "author": "Elgin",
      "year": "1996",
      "journal-title": "Curr. Opin. Genet. Dev."
    },
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      "key": "2023072211302755500_Foeetal1993",
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      "article-title": "Mitosis and morphogenesis in the Drosophila embryopoint and counterpoint",
      "volume-title": "The Development of Drosophila melanogaster",
      "author": "Foe",
      "year": "1993"
    },
    {
      "key": "2023072211302755500_Henikoffetal2000",
      "doi-asserted-by": "crossref",
      "first-page": "716",
      "DOI": "10.1073/pnas.97.2.716",
      "article-title": "Heterochromatic deposition of centromeric histone H3-like proteins",
      "volume": "97",
      "author": "Henikoff",
      "year": "2000",
      "journal-title": "Proc. Natl. Acad. Sci. USA."
    },
    {
      "key": "2023072211302755500_Hiraokaetal1993",
      "doi-asserted-by": "crossref",
      "first-page": "591",
      "DOI": "10.1083/jcb.120.3.591",
      "article-title": "The onset of homologous chromosome pairing during Drosophila melanogaster embryogenesis",
      "volume": "120",
      "author": "Hiraoka",
      "year": "1993",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072211302755500_Kandaetal1998",
      "doi-asserted-by": "crossref",
      "first-page": "377",
      "DOI": "10.1016/S0960-9822(98)70156-3",
      "article-title": "Histone-GFP fusion protein enables sensitive analysis of chromosome dynamics in living mammalian cells",
      "volume": "8",
      "author": "Kanda",
      "year": "1998",
      "journal-title": "Curr. Biol."
    },
    {
      "key": "2023072211302755500_KarpenandAllshire1997",
      "doi-asserted-by": "crossref",
      "first-page": "489",
      "DOI": "10.1016/S0168-9525(97)01298-5",
      "article-title": "The case for epigenetic effects on centromere identity and function",
      "volume": "13",
      "author": "Karpen",
      "year": "1997",
      "journal-title": "Trends Genet."
    },
    {
      "key": "2023072211302755500_Kobernaetal1999",
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      "DOI": "10.1007/s004120050384",
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      "volume": "108",
      "author": "Koberna",
      "year": "1999",
      "journal-title": "Chromosoma."
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      "key": "2023072211302755500_KriegsteinandHogness1974",
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      "first-page": "135",
      "DOI": "10.1073/pnas.71.1.135",
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      "author": "Kriegstein",
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      "key": "2023072211302755500_Krude1995",
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      "DOI": "10.1006/excr.1995.1320",
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      "volume": "220",
      "author": "Krude",
      "year": "1995",
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    {
      "key": "2023072211302755500_Krude1999",
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      "volume": "263",
      "author": "Krude",
      "year": "1999",
      "journal-title": "Eur. J. Biochem."
    },
    {
      "key": "2023072211302755500_Lima-de-FariaandJaworska1968",
      "doi-asserted-by": "crossref",
      "first-page": "138",
      "DOI": "10.1038/217138a0",
      "article-title": "Late DNA synthesis in heterochromatin",
      "volume": "217",
      "author": "Lima-de-Faria",
      "year": "1968",
      "journal-title": "Nature."
    },
    {
      "key": "2023072211302755500_Loetal1999",
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      "first-page": "895",
      "DOI": "10.1101/gr.9.10.895",
      "article-title": "Extreme reduction of chromosome-specific alpha-satellite array is unusually common in human chromosome 21",
      "volume": "8",
      "author": "Lo",
      "year": "1999",
      "journal-title": "Genome Res."
    },
    {
      "key": "2023072211302755500_Maetal1998",
      "doi-asserted-by": "crossref",
      "first-page": "1415",
      "DOI": "10.1083/jcb.143.6.1415",
      "article-title": "Spatial and temporal dynamics of DNA replication sites in mammalian cells",
      "volume": "143",
      "author": "Ma",
      "year": "1998",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072211302755500_Mandersetal1992",
      "doi-asserted-by": "crossref",
      "first-page": "857",
      "DOI": "10.1242/jcs.103.3.857",
      "article-title": "Dynamics of three-dimensional replication patterns during the S-phase, analyzed by double labelling of DNA and confocal microscopy",
      "volume": "103",
      "author": "Manders",
      "year": "1992",
      "journal-title": "J. Cell Sci."
    },
    {
      "key": "2023072211302755500_McCarrollandFangman1988",
      "doi-asserted-by": "crossref",
      "first-page": "505",
      "DOI": "10.1016/0092-8674(88)90072-4",
      "article-title": "Time of replication of yeast centromeres and telomeres",
      "volume": "54",
      "author": "McCarroll",
      "year": "1988",
      "journal-title": "Cell."
    },
    {
      "key": "2023072211302755500_MeluhandKoshland1997",
      "doi-asserted-by": "crossref",
      "first-page": "3401",
      "DOI": "10.1101/gad.11.24.3401",
      "article-title": "Budding yeast centromere composition and assembly as revealed by in vivo cross-linking",
      "volume": "11",
      "author": "Meluh",
      "year": "1997",
      "journal-title": "Genes Dev."
    },
    {
      "key": "2023072211302755500_MurphyandKarpen1995",
      "doi-asserted-by": "crossref",
      "first-page": "599",
      "DOI": "10.1016/0092-8674(95)90032-2",
      "article-title": "Localization of centromere function in a Drosophila minichromosome",
      "volume": "82",
      "author": "Murphy",
      "year": "1995",
      "journal-title": "Cell."
    },
    {
      "key": "2023072211302755500_MurphyandKarpen1998",
      "doi-asserted-by": "crossref",
      "first-page": "317",
      "DOI": "10.1016/S0092-8674(00)81158-7",
      "article-title": "Centromeres take flightalpha satellite and the quest for the human centromere",
      "volume": "93",
      "author": "Murphy",
      "year": "1998",
      "journal-title": "Cell."
    },
    {
      "key": "2023072211302755500_Ofiretal1999",
      "doi-asserted-by": "crossref",
      "first-page": "11434",
      "DOI": "10.1073/pnas.96.20.11434",
      "article-title": "Position effect of human telomeric repeats on replication timing",
      "volume": "96",
      "author": "Ofir",
      "year": "1999",
      "journal-title": "Proc. Natl. Acad. Sci. USA."
    },
    {
      "key": "2023072211302755500_OKeefeetal1992",
      "doi-asserted-by": "crossref",
      "first-page": "1095",
      "DOI": "10.1083/jcb.116.5.1095",
      "article-title": "Dynamic organization of DNA replication in mammalian cell nucleispatially and temporally defined replication of chromosome-specific alpha-satellite DNA sequences",
      "volume": "116",
      "author": "O'Keefe",
      "year": "1992",
      "journal-title": "J. Cell. Biol."
    },
    {
      "key": "2023072211302755500_Osley1991",
      "doi-asserted-by": "crossref",
      "first-page": "827",
      "DOI": "10.1146/annurev.bi.60.070191.004143",
      "article-title": "The regulation of histone synthesis in the cell cycle",
      "volume": "60",
      "author": "Osley",
      "year": "1991",
      "journal-title": "Annu. Rev. Biochem."
    },
    {
      "key": "2023072211302755500_Palmeretal1987",
      "doi-asserted-by": "crossref",
      "first-page": "805",
      "DOI": "10.1083/jcb.104.4.805",
      "article-title": "A 17-kD centromere protein (CENP-A) copurifies with nucleosome core particles and with histones",
      "volume": "104",
      "author": "Palmer",
      "year": "1987",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072211302755500_Palmeretal1990",
      "doi-asserted-by": "crossref",
      "first-page": "32",
      "DOI": "10.1007/BF00337600",
      "article-title": "The centromere specific histone CENP-A is selectively retained in discrete foci in mammalian sperm nuclei",
      "volume": "100",
      "author": "Palmer",
      "year": "1990",
      "journal-title": "Chromosoma."
    },
    {
      "key": "2023072211302755500_Palmeretal1991",
      "doi-asserted-by": "crossref",
      "first-page": "3734",
      "DOI": "10.1073/pnas.88.9.3734",
      "article-title": "Purification of the centromere-specific protein CENP-A and demonstration that it is a distinctive histone",
      "volume": "88",
      "author": "Palmer",
      "year": "1991",
      "journal-title": "Proc. Natl. Acad. Sci. USA."
    },
    {
      "key": "2023072211302755500_Safferyetal2000",
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      "first-page": "175",
      "DOI": "10.1093/hmg/9.2.175",
      "article-title": "Human centromeres and neocentromeres show identical distribution patterns of &gt;20 functionally important kinetochore-associated proteins",
      "volume": "9",
      "author": "Saffery",
      "year": "2000",
      "journal-title": "Hum. Mol. Genet."
    },
    {
      "key": "2023072211302755500_Shelbyetal1997",
      "doi-asserted-by": "crossref",
      "first-page": "501",
      "DOI": "10.1083/jcb.136.3.501",
      "article-title": "Assembly of CENP-A into centromeric chromatin requires a cooperative array of nucleosomal DNA contact sites",
      "volume": "136",
      "author": "Shelby",
      "year": "1997",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072211302755500_SmothersandHenikoff2001",
      "doi-asserted-by": "crossref",
      "first-page": "2555",
      "DOI": "10.1128/MCB.21.7.2555-2569.2001",
      "article-title": "The hinge and chromoshadow domain impart distinct targeting of HP1-like proteins",
      "volume": "21",
      "author": "Smothers",
      "year": "2001",
      "journal-title": "Mol. Cell. Biol."
    },
    {
      "key": "2023072211302755500_StevensonandGottschling1999",
      "doi-asserted-by": "crossref",
      "first-page": "146",
      "DOI": "10.1101/gad.13.2.146",
      "article-title": "Telomeric chromatin modulates replication timing near chromosome ends",
      "volume": "13",
      "author": "Stevenson",
      "year": "1999",
      "journal-title": "Genes Dev."
    },
    {
      "key": "2023072211302755500_Stoleretal1995",
      "doi-asserted-by": "crossref",
      "first-page": "573",
      "DOI": "10.1101/gad.9.5.573",
      "article-title": "A mutation in CSE4, an essential gene encoding a novel chromatin-associated protein in yeast, causes chromosome nondisjunction and cell cycle arrest at mitosis",
      "volume": "9",
      "author": "Stoler",
      "year": "1995",
      "journal-title": "Genes Dev."
    },
    {
      "key": "2023072211302755500_Sunetal1997",
      "doi-asserted-by": "crossref",
      "first-page": "1007",
      "DOI": "10.1016/S0092-8674(00)80491-2",
      "article-title": "Molecular structure of a functional Drosophila centromere",
      "volume": "91",
      "author": "Sun",
      "year": "1997",
      "journal-title": "Cell."
    },
    {
      "key": "2023072211302755500_Takahashietal2000",
      "doi-asserted-by": "crossref",
      "first-page": "2215",
      "DOI": "10.1126/science.288.5474.2215",
      "article-title": "Requirement of Mis6 centromere connector for localizing a CENP-A-like protein in fission yeast",
      "volume": "288",
      "author": "Takahashi",
      "year": "2000",
      "journal-title": "Science."
    },
    {
      "key": "2023072211302755500_Tyler-SmithandFloridia2000",
      "doi-asserted-by": "crossref",
      "first-page": "5",
      "DOI": "10.1016/S0092-8674(00)00004-0",
      "article-title": "Many paths to the top of the mountaindiverse evolutionary solutions to centromere structure",
      "volume": "102",
      "author": "Tyler-Smith",
      "year": "2000",
      "journal-title": "Cell"
    },
    {
      "key": "2023072211302755500_vanHooseretal1999",
      "doi-asserted-by": "crossref",
      "first-page": "S216",
      "DOI": "10.1096/fasebj.13.9002.S216",
      "article-title": "The mammalian centromerestructural domains and the attenuation of chromatin modelling",
      "volume": "13",
      "author": "van Hooser",
      "year": "1999",
      "journal-title": "FASEB J."
    },
    {
      "key": "2023072211302755500_vanSteenselandHenikoff2000",
      "doi-asserted-by": "crossref",
      "first-page": "424",
      "DOI": "10.1038/74487",
      "article-title": "Identification of in vivo DNA targets of chromatin proteins using tethered dam methyltransferase",
      "volume": "18",
      "author": "van Steensel",
      "year": "2000",
      "journal-title": "Nat. Biotech."
    },
    {
      "key": "2023072211302755500_Verreaultetal1996",
      "doi-asserted-by": "crossref",
      "first-page": "95",
      "DOI": "10.1016/S0092-8674(00)81326-4",
      "article-title": "Nucleosome assembly by a complex of CAF-1 and acetylated histones H3/H4",
      "volume": "87",
      "author": "Verreault",
      "year": "1996",
      "journal-title": "Cell."
    },
    {
      "key": "2023072211302755500_Warburtonetal2000",
      "doi-asserted-by": "crossref",
      "first-page": "1794",
      "DOI": "10.1086/302924",
      "article-title": "Molecular cytogenetic analysis of eight inversion duplications of human chromosome 13q that each contain a neocentromere",
      "volume": "66",
      "author": "Warburton",
      "year": "2000",
      "journal-title": "Am. J. Hum. Genet."
    },
    {
      "key": "2023072211302755500_Willard1998",
      "doi-asserted-by": "crossref",
      "first-page": "219",
      "DOI": "10.1016/S0959-437X(98)80144-5",
      "article-title": "Centromeresthe missing link in the development of human artificial chromosomes",
      "volume": "8",
      "author": "Willard",
      "year": "1998",
      "journal-title": "Curr. Opin. Genet. Dev."
    },
    {
      "key": "2023072211302755500_Wuetal1986",
      "doi-asserted-by": "crossref",
      "first-page": "201",
      "DOI": "10.3109/10409238609083735",
      "article-title": "Histones and their modifications",
      "volume": "20",
      "author": "Wu",
      "year": "1986",
      "journal-title": "CRC Crit. Rev. Biochem."
    },
    {
      "key": "2023072211302755500_Yangetal2000",
      "doi-asserted-by": "crossref",
      "first-page": "1891",
      "DOI": "10.1093/hmg/9.12.1891",
      "article-title": "Human mini-chromosomes with minimal centromeres",
      "volume": "9",
      "author": "Yang",
      "year": "2000",
      "journal-title": "Hum. Mol. Genet."
    },
    {
      "key": "2023072211302755500_Yodaetal2000",
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      "first-page": "7266",
      "DOI": "10.1073/pnas.130189697",
      "article-title": "Human centromere protein A (CENP-A) can replace histone H3 in nucleosome reconstitution in vitro",
      "volume": "97",
      "author": "Yoda",
      "year": "2000",
      "journal-title": "Proc. Natl. Acad. Sci. USA."
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