DOI: 10.1083/jcb.153.6.1239. Spindle Checkpoint Protein Bub1 Is Required for Kinetochore Localization of Mad1, Mad2, Bub3, and Cenp-E, Independently of Its Kinase Activity

Spindle Checkpoint Protein Bub1 Is Required for Kinetochore Localization of Mad1, Mad2, Bub3, and Cenp-E, Independently of Its Kinase Activity

10.1083/jcb.153.6.1239

Crossref journal-article

Rockefeller University Press

The Journal of Cell Biology (291)

Abstract

The spindle checkpoint inhibits the metaphase to anaphase transition until all the chromosomes are properly attached to the mitotic spindle. We have isolated a Xenopus homologue of the spindle checkpoint component Bub1, and investigated its role in the spindle checkpoint in Xenopus egg extracts. Antibodies raised against Bub1 recognize a 150-kD phosphoprotein at both interphase and mitosis, but the molecular mass is reduced to 140 upon dephosphorylation in vitro. Bub1 is essential for the establishment and maintenance of the checkpoint and is localized to kinetochores, similar to the spindle checkpoint complex Mad1–Mad2. However, Bub1 differs from Mad1–Mad2 in that Bub1 remains on kinetochores that have attached to microtubules; the protein eventually dissociates from the kinetochore during anaphase. Immunodepletion of Bub1 abolishes the spindle checkpoint and the kinetochore binding of the checkpoint proteins Mad1, Mad2, Bub3, and CENP-E. Interestingly, reintroducing either wild-type or kinase-deficient Bub1 protein restores the checkpoint and the kinetochore localization of these proteins. Our studies demonstrate that Bub1 plays a central role in triggering the spindle checkpoint signal from the kinetochore, and that its kinase activity is not necessary for the spindle checkpoint in Xenopus egg extracts.

Bibliography

Sharp-Baker, H., & Chen, R.-H. (2001). Spindle Checkpoint Protein Bub1 Is Required for Kinetochore Localization of Mad1, Mad2, Bub3, and Cenp-E, Independently of Its Kinase Activity. The Journal of Cell Biology, 153(6), 1239â1250.

Authors 2

Hilary Sharp-Baker (first)
Rey-Huei Chen (additional)

References 48 Referenced 186

10.1016/S0092-8674(00)00070-2 / Cell / CENP-E as an essential component of the mitotic checkpoint in vitro by Abrieu (2000)
10.1016/S0959-437X(99)80010-0 / Curr. Opin. Genet. Dev / The spindle checkpoint by Amon (1999)
10.1007/s004120050321 / Chromosoma / Localization of the Drosophila checkpoint control protein Bub3 to the kinetochore requires Bub1 but not Zw10 or Rod by Basu (1998)
10.1083/jcb.146.1.13 / J. Cell Biol / Mutations in the essential spindle checkpoint gene bub1 cause chromosome missegregation and fail to block apoptosis in Drosophila by Basu (1999)
10.1016/S0960-9822(00)00515-7 / Curr. Biol / Complex formation between Mad1p, Bub1p and Bub3p is crucial for spindle checkpoint function by Brady (2000)
10.1038/32688 / Nature / Mutations of mitotic checkpoint genes in human cancers by Cahill (1998)
10.1083/jcb.143.1.49 / J. Cell Biol / Characterization of the kinetochore binding domain of CENP-E reveals interactions with the kinetochore proteins CENP-F and hBUBR1 by Chan (1998)
10.1083/jcb.146.5.941 / J. Cell Biol / Human BUBR1 is a mitotic checkpoint kinase that monitors CENP-E functions at kinetochores and binds the cyclosome/APC by Chan (1999)
10.1126/science.274.5285.242 / Science / Association of spindle assembly checkpoint component XMAD2 with unattached kinetochores by Chen (1996)
10.1083/jcb.143.2.283 / J. Cell Biol / Spindle checkpoint protein xmad1 recruits xmad2 to unattached kinetochores by Chen (1998)
10.1091/mbc.10.8.2607 / Mol. Biol. Cell / The spindle checkpoint of budding yeast depends on a tight complex between the Mad1 and Mad2 proteins by Chen (1999)
10.1016/S0092-8674(00)80875-2 / Cell / Chromosome missegregation and apoptosis in mice lacking the mitotic checkpoint protein Mad2 by Dobles (2000)
10.1101/gad.12.12.1871 / Genes Dev / The checkpoint protein MAD2 and the mitotic regulator CDC20 form a ternary complex with the anaphase-promoting complex to control anaphase initiation by Fang (1998)
10.1128/MCB.18.5.2738 / Mol. Cell. Biol / Bub1p kinase activates the Saccharomyces cerevisiae spindle assembly checkpoint by Farr (1998)
10.1083/jcb.141.5.1193 / J. Cell Biol / Microinjection of antibody to mad2 protein into mammalian cells in mitosis induces premature anaphase by Gorbsky (1998)
10.1089/104454999315448 / DNA Cell Biol / Maternal transcripts of mitotic checkpoint gene, Xbub3, are accumulated in the animal blastomeres of Xenopus early embryo by Goto (1999)
10.1083/jcb.131.3.709 / J. Cell Biol. / Mad1p, a phosphoprotein component of the spindle assembly checkpoint in budding yeast by Hardwick (1995)
10.1126/science.273.5277.953 / Science / Activation of the budding yeast spindle assembly checkpoint without mitotic spindle disruption by Hardwick (1996)
10.1016/0092-8674(81)90014-3 / Cell / S. cerevisiae genes required for cell cycle arrest in response to loss of microtubule function by Hoyt (1991)
10.1126/science.279.5353.1041 / Science / Budding yeast Cdc20a target of the spindle checkpoint by Hwang (1998)
10.1007/s004120050322 / Chromosoma / The hBUB1 and hBUBR1 kinases sequentially assemble onto kinetochores during prophase with hBUBR1 concentrating at the kinetochore plates in mitosis by Jablonski (1998)
10.1016/S0092-8674(00)81148-4 / Cell / Human T cell leukemia virus type 1 oncoprotein Tax targets the human mitotic checkpoint protein MAD1 by Jin (1998)
10.1101/gad.827500 / Genes Dev / Bub3 gene disruption in mice reveals essential mitotic spindle checkpoint function during early embryogenesis by Kalitsis (2000)
10.1038/35070123 / Nat. Cell Biol / A role for the Adenomatous Polyposis Coli protein in chromosome segregation by Kaplan (2001)
10.1126/science.279.5353.1045 / Science / Fission yeast Slp1an effector of the Mad2-dependent spindle checkpoint by Kim (1998)
10.1016/0092-8674(81)90015-5 / Cell / Feedback control of mitosis in budding yeast by Li (1991)
10.1038/373630a0 / Nature / Mitotic forces control a cell cycle checkpoint by Li (1995)
10.1126/science.274.5285.246 / Science / Identification of a human mitotic checkpoint genehsMAD2 by Li (1996)
10.1016/0092-8674(94)90256-9 / Cell / MAP-kinase dependent mitotic feedback arrest in Xenopus egg extracts by Minshull (1994)
{'key': '2023072211434434400_Murray1991', 'first-page': '573', 'article-title': 'Cell cycle extracts', 'volume': '36', 'author': 'Murray', 'year': '1991', 'journal-title': 'Methods Cell Biol.'} / Methods Cell Biol. / Cell cycle extracts by Murray (1991)
10.1146/annurev.biochem.68.1.583 / Annu. Rev. Biochem / The anaphase-promoting complexnew subunits and regulators by Page (1999)
10.1083/jcb.130.4.941 / J. Cell Biol. / The checkpoint delaying anaphase in response to chromosome monoorientation is mediated by an inhibitory signal produced by unattached kinetochores by Rieder (1995)
{'key': '2023072211434434400_Robertsetal1994', 'first-page': '8282', 'article-title': 'The Saccharomyces cerevisiae checkpoint gene BUB1 encodes a novel protein kinase', 'volume': '14', 'author': 'Roberts', 'year': '1994', 'journal-title': 'Mol. Cell. Biol.'} / Mol. Cell. Biol. / The Saccharomyces cerevisiae checkpoint gene BUB1 encodes a novel protein kinase by Roberts (1994)
10.1083/jcb.139.6.1373 / J. Cell Biol / CENP-E function at kinetochores is essential for chromosome alignment by Schaar (1997)
10.1016/S0960-9822(01)00045-8 / Curr. Biol. / Bub1 is activated by the protein kinase p90Rsk during Xenopus oocyte maturation by Schwab (2001)
10.1006/bbrc.1999.0514 / Biochem. Biophys. Res. Commun / Phosphorylation of human MAD1 by the BUB1 kinase in vitro by Seeley (1999)
10.1083/jcb.142.6.1533 / J. Cell Biol / Activation of the MKK/ERK pathway during somatic cell mitosisdirect interactions of active ERK with kinetochores and regulation of the mitotic 3F3/2 phosphoantigen by Shapiro (1998)
10.1083/jcb.136.5.1091 / J. Cell Biol. / MAP kinase is required for the spindle assembly checkpoint but is dispensable for the normal M phase entry and exit in Xenopus egg cell cycle extracts by Takenaka (1997)
10.1016/S0092-8674(00)80255-X / Cell / Kinetochore localization of murine Bub1 is required for normal mitotic timing and checkpoint response to spindle damage by Taylor (1997)
10.1083/jcb.142.1.1 / J. Cell Biol / The human homologue of bub3 is required for kinetochore localization of bub1 and a Mad3/Bub1-related protein kinase by Taylor (1998)
10.1126/science.278.5337.460 / Science / CDC20 and CDH1a family of substrate-specific activators of APC-dependent proteolysis by Visintin (1997)
10.1083/jcb.137.2.433 / J. Cell Biol / A role for mitogen-activated protein kinase in the spindle assembly checkpoint in XTC cells by Wang (1997)
10.1083/jcb.141.5.1181 / J. Cell Biol / Localization of mad2 to kinetochores depends on microtubule attachment, not tension by Waters (1998)
10.1083/jcb.132.1.111 / J. Cell Biol. / The S. cerevisiae SPB duplication gene MPS1 is part of a mitotic checkpoint by Weiss (1996)
10.1016/S0092-8674(00)80419-5 / Cell / CENP-E is a plus end-directed kinetochore motor required for metaphase chromosome alignment by Wood (1997)
10.1038/sj.onc.1203803 / Oncogene / p55CDC/hCDC20 is associated with BUBR1 and may be a downstream target of the spindle checkpoint kinase by Wu (2000)
10.1038/35019518 / Nat. Cell Biol / CENP-E forms a link between attachment of spindle microtubules to kinetochores and the mitotic checkpoint by Yao (2000)
10.1083/jcb.142.6.1547 / J. Cell Biol / Active MAP kinase in mitosislocalization at kinetochores and association with the motor protein CENP-E by Zecevic (1998)

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, 7:44 a.m.)
Indexed	6 days, 16 hours ago (Aug. 23, 2025, 9:33 p.m.)
Issued	24 years, 2 months ago (June 11, 2001)
Published	24 years, 2 months ago (June 11, 2001)
Published Online	24 years, 2 months ago (June 11, 2001)
Published Print	24 years, 2 months ago (June 11, 2001)

Funders 0

None

BibTeX

@article{Sharp_Baker_2001, title={Spindle Checkpoint Protein Bub1 Is Required for Kinetochore Localization of Mad1, Mad2, Bub3, and Cenp-E, Independently of Its Kinase Activity}, volume={153}, ISSN={1540-8140}, url={http://dx.doi.org/10.1083/jcb.153.6.1239}, DOI={10.1083/jcb.153.6.1239}, number={6}, journal={The Journal of Cell Biology}, publisher={Rockefeller University Press}, author={Sharp-Baker, Hilary and Chen, Rey-Huei}, year={2001}, month=jun, pages={1239–1250} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        8,
        24
      ]
    ],
    "date-time": "2025-08-24T01:33:25Z",
    "timestamp": 1755999205261
  },
  "reference-count": 48,
  "publisher": "Rockefeller University Press",
  "issue": "6",
  "content-domain": {
    "domain": [
      "rupress.org"
    ],
    "crossmark-restriction": true
  },
  "published-print": {
    "date-parts": [
      [
        2001,
        6,
        11
      ]
    ]
  },
  "abstract": "<jats:p>The spindle checkpoint inhibits the metaphase to anaphase transition until all the chromosomes are properly attached to the mitotic spindle. We have isolated a Xenopus homologue of the spindle checkpoint component Bub1, and investigated its role in the spindle checkpoint in Xenopus egg extracts. Antibodies raised against Bub1 recognize a 150-kD phosphoprotein at both interphase and mitosis, but the molecular mass is reduced to 140 upon dephosphorylation in vitro. Bub1 is essential for the establishment and maintenance of the checkpoint and is localized to kinetochores, similar to the spindle checkpoint complex Mad1\u2013Mad2. However, Bub1 differs from Mad1\u2013Mad2 in that Bub1 remains on kinetochores that have attached to microtubules; the protein eventually dissociates from the kinetochore during anaphase. Immunodepletion of Bub1 abolishes the spindle checkpoint and the kinetochore binding of the checkpoint proteins Mad1, Mad2, Bub3, and CENP-E. Interestingly, reintroducing either wild-type or kinase-deficient Bub1 protein restores the checkpoint and the kinetochore localization of these proteins. Our studies demonstrate that Bub1 plays a central role in triggering the spindle checkpoint signal from the kinetochore, and that its kinase activity is not necessary for the spindle checkpoint in Xenopus egg extracts.</jats:p>",
  "DOI": "10.1083/jcb.153.6.1239",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2002,
        7,
        26
      ]
    ],
    "date-time": "2002-07-26T16:46:23Z",
    "timestamp": 1027701983000
  },
  "page": "1239-1250",
  "update-policy": "http://dx.doi.org/10.1083/jcb.crossmarkpolicy",
  "source": "Crossref",
  "is-referenced-by-count": 186,
  "title": "Spindle Checkpoint Protein Bub1 Is Required for Kinetochore Localization of Mad1, Mad2, Bub3, and Cenp-E, Independently of Its Kinase Activity",
  "prefix": "10.1083",
  "volume": "153",
  "author": [
    {
      "given": "Hilary",
      "family": "Sharp-Baker",
      "sequence": "first",
      "affiliation": [
        {
          "name": "aDepartment of Molecular Biology and Genetics, Cornell University, Ithaca, New York 14853"
        }
      ]
    },
    {
      "given": "Rey-Huei",
      "family": "Chen",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "aDepartment of Molecular Biology and Genetics, Cornell University, Ithaca, New York 14853"
        }
      ]
    }
  ],
  "member": "291",
  "published-online": {
    "date-parts": [
      [
        2001,
        6,
        11
      ]
    ]
  },
  "reference": [
    {
      "key": "2023072211434434400_Abrieuetal2000",
      "doi-asserted-by": "crossref",
      "first-page": "817",
      "DOI": "10.1016/S0092-8674(00)00070-2",
      "article-title": "CENP-E as an essential component of the mitotic checkpoint in vitro",
      "volume": "102",
      "author": "Abrieu",
      "year": "2000",
      "journal-title": "Cell"
    },
    {
      "key": "2023072211434434400_Amon1999",
      "doi-asserted-by": "crossref",
      "first-page": "69",
      "DOI": "10.1016/S0959-437X(99)80010-0",
      "article-title": "The spindle checkpoint",
      "volume": "9",
      "author": "Amon",
      "year": "1999",
      "journal-title": "Curr. Opin. Genet. Dev"
    },
    {
      "key": "2023072211434434400_Basuetal1998",
      "doi-asserted-by": "crossref",
      "first-page": "376",
      "DOI": "10.1007/s004120050321",
      "article-title": "Localization of the Drosophila checkpoint control protein Bub3 to the kinetochore requires Bub1 but not Zw10 or Rod",
      "volume": "107",
      "author": "Basu",
      "year": "1998",
      "journal-title": "Chromosoma"
    },
    {
      "key": "2023072211434434400_Basuetal1999",
      "doi-asserted-by": "crossref",
      "first-page": "13",
      "DOI": "10.1083/jcb.146.1.13",
      "article-title": "Mutations in the essential spindle checkpoint gene bub1 cause chromosome missegregation and fail to block apoptosis in Drosophila",
      "volume": "146",
      "author": "Basu",
      "year": "1999",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2023072211434434400_BradyandHardwick2000",
      "doi-asserted-by": "crossref",
      "first-page": "675",
      "DOI": "10.1016/S0960-9822(00)00515-7",
      "article-title": "Complex formation between Mad1p, Bub1p and Bub3p is crucial for spindle checkpoint function",
      "volume": "10",
      "author": "Brady",
      "year": "2000",
      "journal-title": "Curr. Biol"
    },
    {
      "key": "2023072211434434400_Cahilletal1998",
      "doi-asserted-by": "crossref",
      "first-page": "300",
      "DOI": "10.1038/32688",
      "article-title": "Mutations of mitotic checkpoint genes in human cancers",
      "volume": "392",
      "author": "Cahill",
      "year": "1998",
      "journal-title": "Nature"
    },
    {
      "key": "2023072211434434400_Chanetal1998",
      "doi-asserted-by": "crossref",
      "first-page": "49",
      "DOI": "10.1083/jcb.143.1.49",
      "article-title": "Characterization of the kinetochore binding domain of CENP-E reveals interactions with the kinetochore proteins CENP-F and hBUBR1",
      "volume": "143",
      "author": "Chan",
      "year": "1998",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2023072211434434400_Chanetal1999",
      "doi-asserted-by": "crossref",
      "first-page": "941",
      "DOI": "10.1083/jcb.146.5.941",
      "article-title": "Human BUBR1 is a mitotic checkpoint kinase that monitors CENP-E functions at kinetochores and binds the cyclosome/APC",
      "volume": "146",
      "author": "Chan",
      "year": "1999",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2023072211434434400_Chenetal1996",
      "doi-asserted-by": "crossref",
      "first-page": "242",
      "DOI": "10.1126/science.274.5285.242",
      "article-title": "Association of spindle assembly checkpoint component XMAD2 with unattached kinetochores",
      "volume": "274",
      "author": "Chen",
      "year": "1996",
      "journal-title": "Science"
    },
    {
      "key": "2023072211434434400_Chenetal1998",
      "doi-asserted-by": "crossref",
      "first-page": "283",
      "DOI": "10.1083/jcb.143.2.283",
      "article-title": "Spindle checkpoint protein xmad1 recruits xmad2 to unattached kinetochores",
      "volume": "143",
      "author": "Chen",
      "year": "1998",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2023072211434434400_Chenetal1999",
      "doi-asserted-by": "crossref",
      "first-page": "2607",
      "DOI": "10.1091/mbc.10.8.2607",
      "article-title": "The spindle checkpoint of budding yeast depends on a tight complex between the Mad1 and Mad2 proteins",
      "volume": "10",
      "author": "Chen",
      "year": "1999",
      "journal-title": "Mol. Biol. Cell"
    },
    {
      "key": "2023072211434434400_Doblesetal2000",
      "doi-asserted-by": "crossref",
      "first-page": "635",
      "DOI": "10.1016/S0092-8674(00)80875-2",
      "article-title": "Chromosome missegregation and apoptosis in mice lacking the mitotic checkpoint protein Mad2",
      "volume": "101",
      "author": "Dobles",
      "year": "2000",
      "journal-title": "Cell"
    },
    {
      "key": "2023072211434434400_Fangetal1998",
      "doi-asserted-by": "crossref",
      "first-page": "1871",
      "DOI": "10.1101/gad.12.12.1871",
      "article-title": "The checkpoint protein MAD2 and the mitotic regulator CDC20 form a ternary complex with the anaphase-promoting complex to control anaphase initiation",
      "volume": "12",
      "author": "Fang",
      "year": "1998",
      "journal-title": "Genes Dev"
    },
    {
      "key": "2023072211434434400_FarrandHoyt1998",
      "doi-asserted-by": "crossref",
      "first-page": "2738",
      "DOI": "10.1128/MCB.18.5.2738",
      "article-title": "Bub1p kinase activates the Saccharomyces cerevisiae spindle assembly checkpoint",
      "volume": "18",
      "author": "Farr",
      "year": "1998",
      "journal-title": "Mol. Cell. Biol"
    },
    {
      "key": "2023072211434434400_Gorbskyetal1998",
      "doi-asserted-by": "crossref",
      "first-page": "1193",
      "DOI": "10.1083/jcb.141.5.1193",
      "article-title": "Microinjection of antibody to mad2 protein into mammalian cells in mitosis induces premature anaphase",
      "volume": "141",
      "author": "Gorbsky",
      "year": "1998",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2023072211434434400_GotoandKinoshita1999",
      "doi-asserted-by": "crossref",
      "first-page": "227",
      "DOI": "10.1089/104454999315448",
      "article-title": "Maternal transcripts of mitotic checkpoint gene, Xbub3, are accumulated in the animal blastomeres of Xenopus early embryo",
      "volume": "18",
      "author": "Goto",
      "year": "1999",
      "journal-title": "DNA Cell Biol"
    },
    {
      "key": "2023072211434434400_HardwickandMurray1995",
      "doi-asserted-by": "crossref",
      "first-page": "709",
      "DOI": "10.1083/jcb.131.3.709",
      "article-title": "Mad1p, a phosphoprotein component of the spindle assembly checkpoint in budding yeast",
      "volume": "131",
      "author": "Hardwick",
      "year": "1995",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072211434434400_Hardwicketal1996",
      "doi-asserted-by": "crossref",
      "first-page": "953",
      "DOI": "10.1126/science.273.5277.953",
      "article-title": "Activation of the budding yeast spindle assembly checkpoint without mitotic spindle disruption",
      "volume": "273",
      "author": "Hardwick",
      "year": "1996",
      "journal-title": "Science"
    },
    {
      "key": "2023072211434434400_Hoytetal1991",
      "doi-asserted-by": "crossref",
      "first-page": "507",
      "DOI": "10.1016/0092-8674(81)90014-3",
      "article-title": "S. cerevisiae genes required for cell cycle arrest in response to loss of microtubule function",
      "volume": "66",
      "author": "Hoyt",
      "year": "1991",
      "journal-title": "Cell"
    },
    {
      "key": "2023072211434434400_Hwangetal1998",
      "doi-asserted-by": "crossref",
      "first-page": "1041",
      "DOI": "10.1126/science.279.5353.1041",
      "article-title": "Budding yeast Cdc20a target of the spindle checkpoint",
      "volume": "279",
      "author": "Hwang",
      "year": "1998",
      "journal-title": "Science"
    },
    {
      "key": "2023072211434434400_Jablonskietal1998",
      "doi-asserted-by": "crossref",
      "first-page": "386",
      "DOI": "10.1007/s004120050322",
      "article-title": "The hBUB1 and hBUBR1 kinases sequentially assemble onto kinetochores during prophase with hBUBR1 concentrating at the kinetochore plates in mitosis",
      "volume": "107",
      "author": "Jablonski",
      "year": "1998",
      "journal-title": "Chromosoma"
    },
    {
      "key": "2023072211434434400_Jinetal1998",
      "doi-asserted-by": "crossref",
      "first-page": "81",
      "DOI": "10.1016/S0092-8674(00)81148-4",
      "article-title": "Human T cell leukemia virus type 1 oncoprotein Tax targets the human mitotic checkpoint protein MAD1",
      "volume": "93",
      "author": "Jin",
      "year": "1998",
      "journal-title": "Cell"
    },
    {
      "key": "2023072211434434400_Kalitsisetal2000",
      "doi-asserted-by": "crossref",
      "first-page": "2277",
      "DOI": "10.1101/gad.827500",
      "article-title": "Bub3 gene disruption in mice reveals essential mitotic spindle checkpoint function during early embryogenesis",
      "volume": "14",
      "author": "Kalitsis",
      "year": "2000",
      "journal-title": "Genes Dev"
    },
    {
      "key": "2023072211434434400_Kaplanetal2001",
      "doi-asserted-by": "crossref",
      "first-page": "429",
      "DOI": "10.1038/35070123",
      "article-title": "A role for the Adenomatous Polyposis Coli protein in chromosome segregation",
      "volume": "3",
      "author": "Kaplan",
      "year": "2001",
      "journal-title": "Nat. Cell Biol"
    },
    {
      "key": "2023072211434434400_Kimetal1998",
      "doi-asserted-by": "crossref",
      "first-page": "1045",
      "DOI": "10.1126/science.279.5353.1045",
      "article-title": "Fission yeast Slp1an effector of the Mad2-dependent spindle checkpoint",
      "volume": "279",
      "author": "Kim",
      "year": "1998",
      "journal-title": "Science"
    },
    {
      "key": "2023072211434434400_LiandMurray1991",
      "doi-asserted-by": "crossref",
      "first-page": "519",
      "DOI": "10.1016/0092-8674(81)90015-5",
      "article-title": "Feedback control of mitosis in budding yeast",
      "volume": "66",
      "author": "Li",
      "year": "1991",
      "journal-title": "Cell"
    },
    {
      "key": "2023072211434434400_LiandNicklas1995",
      "doi-asserted-by": "crossref",
      "first-page": "630",
      "DOI": "10.1038/373630a0",
      "article-title": "Mitotic forces control a cell cycle checkpoint",
      "volume": "373",
      "author": "Li",
      "year": "1995",
      "journal-title": "Nature"
    },
    {
      "key": "2023072211434434400_LiandBenezra1996",
      "doi-asserted-by": "crossref",
      "first-page": "246",
      "DOI": "10.1126/science.274.5285.246",
      "article-title": "Identification of a human mitotic checkpoint genehsMAD2",
      "volume": "274",
      "author": "Li",
      "year": "1996",
      "journal-title": "Science"
    },
    {
      "key": "2023072211434434400_Minshulletal1994",
      "doi-asserted-by": "crossref",
      "first-page": "475",
      "DOI": "10.1016/0092-8674(94)90256-9",
      "article-title": "MAP-kinase dependent mitotic feedback arrest in Xenopus egg extracts",
      "volume": "79",
      "author": "Minshull",
      "year": "1994",
      "journal-title": "Cell"
    },
    {
      "key": "2023072211434434400_Murray1991",
      "first-page": "573",
      "article-title": "Cell cycle extracts",
      "volume": "36",
      "author": "Murray",
      "year": "1991",
      "journal-title": "Methods Cell Biol."
    },
    {
      "key": "2023072211434434400_PageandHieter1999",
      "doi-asserted-by": "crossref",
      "first-page": "583",
      "DOI": "10.1146/annurev.biochem.68.1.583",
      "article-title": "The anaphase-promoting complexnew subunits and regulators",
      "volume": "68",
      "author": "Page",
      "year": "1999",
      "journal-title": "Annu. Rev. Biochem"
    },
    {
      "key": "2023072211434434400_Riederetal1995",
      "doi-asserted-by": "crossref",
      "first-page": "941",
      "DOI": "10.1083/jcb.130.4.941",
      "article-title": "The checkpoint delaying anaphase in response to chromosome monoorientation is mediated by an inhibitory signal produced by unattached kinetochores",
      "volume": "130",
      "author": "Rieder",
      "year": "1995",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072211434434400_Robertsetal1994",
      "first-page": "8282",
      "article-title": "The Saccharomyces cerevisiae checkpoint gene BUB1 encodes a novel protein kinase",
      "volume": "14",
      "author": "Roberts",
      "year": "1994",
      "journal-title": "Mol. Cell. Biol."
    },
    {
      "key": "2023072211434434400_Schaaretal1997",
      "doi-asserted-by": "crossref",
      "first-page": "1373",
      "DOI": "10.1083/jcb.139.6.1373",
      "article-title": "CENP-E function at kinetochores is essential for chromosome alignment",
      "volume": "139",
      "author": "Schaar",
      "year": "1997",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2023072211434434400_Schwabetal2001",
      "doi-asserted-by": "crossref",
      "first-page": "141",
      "DOI": "10.1016/S0960-9822(01)00045-8",
      "article-title": "Bub1 is activated by the protein kinase p90Rsk during Xenopus oocyte maturation",
      "volume": "11",
      "author": "Schwab",
      "year": "2001",
      "journal-title": "Curr. Biol."
    },
    {
      "key": "2023072211434434400_Seeleyetal1999",
      "doi-asserted-by": "crossref",
      "first-page": "589",
      "DOI": "10.1006/bbrc.1999.0514",
      "article-title": "Phosphorylation of human MAD1 by the BUB1 kinase in vitro",
      "volume": "257",
      "author": "Seeley",
      "year": "1999",
      "journal-title": "Biochem. Biophys. Res. Commun"
    },
    {
      "key": "2023072211434434400_Shapiroetal1998",
      "doi-asserted-by": "crossref",
      "first-page": "1533",
      "DOI": "10.1083/jcb.142.6.1533",
      "article-title": "Activation of the MKK/ERK pathway during somatic cell mitosisdirect interactions of active ERK with kinetochores and regulation of the mitotic 3F3/2 phosphoantigen",
      "volume": "142",
      "author": "Shapiro",
      "year": "1998",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2023072211434434400_Takenakaetal1997",
      "doi-asserted-by": "crossref",
      "first-page": "1091",
      "DOI": "10.1083/jcb.136.5.1091",
      "article-title": "MAP kinase is required for the spindle assembly checkpoint but is dispensable for the normal M phase entry and exit in Xenopus egg cell cycle extracts",
      "volume": "136",
      "author": "Takenaka",
      "year": "1997",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072211434434400_TaylorandMcKeon1997",
      "doi-asserted-by": "crossref",
      "first-page": "727",
      "DOI": "10.1016/S0092-8674(00)80255-X",
      "article-title": "Kinetochore localization of murine Bub1 is required for normal mitotic timing and checkpoint response to spindle damage",
      "volume": "89",
      "author": "Taylor",
      "year": "1997",
      "journal-title": "Cell"
    },
    {
      "key": "2023072211434434400_Tayloretal1998",
      "doi-asserted-by": "crossref",
      "first-page": "1",
      "DOI": "10.1083/jcb.142.1.1",
      "article-title": "The human homologue of bub3 is required for kinetochore localization of bub1 and a Mad3/Bub1-related protein kinase",
      "volume": "142",
      "author": "Taylor",
      "year": "1998",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2023072211434434400_Visintinetal1997",
      "doi-asserted-by": "crossref",
      "first-page": "460",
      "DOI": "10.1126/science.278.5337.460",
      "article-title": "CDC20 and CDH1a family of substrate-specific activators of APC-dependent proteolysis",
      "volume": "278",
      "author": "Visintin",
      "year": "1997",
      "journal-title": "Science"
    },
    {
      "key": "2023072211434434400_Wangetal1997",
      "doi-asserted-by": "crossref",
      "first-page": "433",
      "DOI": "10.1083/jcb.137.2.433",
      "article-title": "A role for mitogen-activated protein kinase in the spindle assembly checkpoint in XTC cells",
      "volume": "137",
      "author": "Wang",
      "year": "1997",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2023072211434434400_Watersetal1998",
      "doi-asserted-by": "crossref",
      "first-page": "1181",
      "DOI": "10.1083/jcb.141.5.1181",
      "article-title": "Localization of mad2 to kinetochores depends on microtubule attachment, not tension",
      "volume": "141",
      "author": "Waters",
      "year": "1998",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2023072211434434400_WeissandWiney1996",
      "doi-asserted-by": "crossref",
      "first-page": "111",
      "DOI": "10.1083/jcb.132.1.111",
      "article-title": "The S. cerevisiae SPB duplication gene MPS1 is part of a mitotic checkpoint",
      "volume": "132",
      "author": "Weiss",
      "year": "1996",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072211434434400_Woodetal1997",
      "doi-asserted-by": "crossref",
      "first-page": "357",
      "DOI": "10.1016/S0092-8674(00)80419-5",
      "article-title": "CENP-E is a plus end-directed kinetochore motor required for metaphase chromosome alignment",
      "volume": "91",
      "author": "Wood",
      "year": "1997",
      "journal-title": "Cell"
    },
    {
      "key": "2023072211434434400_Wuetal2000",
      "doi-asserted-by": "crossref",
      "first-page": "4557",
      "DOI": "10.1038/sj.onc.1203803",
      "article-title": "p55CDC/hCDC20 is associated with BUBR1 and may be a downstream target of the spindle checkpoint kinase",
      "volume": "19",
      "author": "Wu",
      "year": "2000",
      "journal-title": "Oncogene"
    },
    {
      "key": "2023072211434434400_Yaoetal2000",
      "doi-asserted-by": "crossref",
      "first-page": "484",
      "DOI": "10.1038/35019518",
      "article-title": "CENP-E forms a link between attachment of spindle microtubules to kinetochores and the mitotic checkpoint",
      "volume": "2",
      "author": "Yao",
      "year": "2000",
      "journal-title": "Nat. Cell Biol"
    },
    {
      "key": "2023072211434434400_Zecevicetal1998",
      "doi-asserted-by": "crossref",
      "first-page": "1547",
      "DOI": "10.1083/jcb.142.6.1547",
      "article-title": "Active MAP kinase in mitosislocalization at kinetochores and association with the motor protein CENP-E",
      "volume": "142",
      "author": "Zecevic",
      "year": "1998",
      "journal-title": "J. Cell Biol"
    }
  ],
  "container-title": "The Journal of Cell Biology",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://rupress.org/jcb/article-pdf/153/6/1239/1512221/0012017.pdf",
      "content-type": "application/pdf",
      "content-version": "vor",
      "intended-application": "syndication"
    },
    {
      "URL": "https://rupress.org/jcb/article-pdf/153/6/1239/1512221/0012017.pdf",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2023,
        7,
        22
      ]
    ],
    "date-time": "2023-07-22T11:44:20Z",
    "timestamp": 1690026260000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://rupress.org/jcb/article/153/6/1239/47804/Spindle-Checkpoint-Protein-Bub1-Is-Required-for"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        2001,
        6,
        11
      ]
    ]
  },
  "references-count": 48,
  "journal-issue": {
    "issue": "6",
    "published-print": {
      "date-parts": [
        [
          2001,
          6,
          11
        ]
      ]
    }
  },
  "URL": "http://dx.doi.org/10.1083/jcb.153.6.1239",
  "relation": {},
  "ISSN": [
    "0021-9525",
    "1540-8140"
  ],
  "subject": [],
  "published": {
    "date-parts": [
      [
        2001,
        6,
        11
      ]
    ]
  }
}