DOI: 10.1083/jcb.152.1.27. A Novel Role of the Budding Yeast Separin Esp1 in Anaphase Spindle Elongation

A Novel Role of the Budding Yeast Separin Esp1 in Anaphase Spindle Elongation

10.1083/jcb.152.1.27

Crossref journal-article

Rockefeller University Press

The Journal of Cell Biology (291)

Abstract

In Saccharomyces cerevisiae, the metaphase–anaphase transition is initiated by the anaphase-promoting complex–dependent degradation of Pds1, whereby Esp1 is activated to promote sister chromatid separation. Although this is a fundamental step in the cell cycle, little is known about the regulation of Esp1 and how loss of cohesion is coordinated with movement of the anaphase spindle. Here, we show that Esp1 has a novel role in promoting anaphase spindle elongation. The localization of Esp1 to the spindle apparatus, analyzed by live cell imaging, is regulated in a manner consistent with a function during anaphase B. The protein accumulates in the nucleus in G2 and is mobilized onto the spindle pole bodies and spindle midzone at anaphase onset, where it persists into midanaphase. Association with Pds1 occurs during S phase and is required for efficient nuclear targeting of Esp1. Spindle association is not fully restored in pds1 mutants expressing an Esp1-nuclear localization sequence fusion protein, suggesting that Pds1 is also required to promote Esp1 spindle binding. In agreement, Pds1 interacts with the spindle at the metaphase–anaphase transition and a fraction remains at the spindle pole bodies and the spindle midzone in anaphase cells. Finally, mutational analysis reveals that the conserved COOH-terminal region of Esp1 is important for spindle interaction.

Bibliography

Jensen, S., Segal, M., Clarke, D. J., & Reed, S. I. (2001). A Novel Role of the Budding Yeast Separin Esp1 in Anaphase Spindle Elongation. The Journal of Cell Biology, 152(1), 27â40.

Authors 4

Sanne Jensen (first)
Marisa Segal (additional)
Duncan J. Clarke (additional)
Steven I. Reed (additional)

References 34 Referenced 109

10.1093/emboj/18.10.2707 / EMBO (Eur. Mol. Biol. Organ.) J / Sister chromatid separation and chromosome re-duplication are regulated by different mechanisms in response to spindle damage by Alexandru (1999)
10.1016/S0092-8674(00)00007-6 / Cell. / A mechanism for coupling exit of mitosis to partitioning of the nucleus by Bardin (2000)
10.1016/S0092-8674(00)81211-8 / Cell. / An ESP1/PDS1 complex regulates loss of sister chromatid cohesion at the metaphase to anaphase transition in yeast by Ciosk (1998)
10.1016/S0960-9822(99)80163-8 / Curr. Biol. / The Pds1 anaphase inhibitor and Mec1 kinase define distinct checkpoints coupling S phase with mitosis in budding yeast by Clarke (1999)
10.1101/gad.13.15.1950 / Genes Dev / Pds1p of budding yeast has dual rolesinhibition of anaphase initiation and regulation of mitotic exit by Cohen-Fix (1999)
10.1101/gad.10.24.3081 / Genes Dev / Anaphase initiation in Saccharomyces cerevisiae is controlled by the APC-dependent degradation of the anaphase inhibitor Pds1p by Cohen-Fix (1996)
10.1002/j.1460-2075.1996.tb01052.x / EMBO (Eur. Mol. Biol. Organ.) J / Fission yeast Cut1 and Cut2 are essential for sister chromatid separation, concentrate along the metaphase spindle and form large complexes by Funabiki (1996)
10.1083/jcb.121.3.503 / J. Cell Biol / NDC10a gene involved in chromosome segregation in Saccharomyces cerevisiae by Goh (1993)
10.1016/S0092-8674(00)80914-9 / Cell. / An anaphase calcium signal controls chromosome disjunction in early sea urchin embryos by Groigno (1998)
{'key': '2023072902512869500_GuthrieandFink1991', 'volume-title': 'Guide to yeast genetics and molecular biology. Vol. 194', 'author': 'Guthrie', 'year': '1991'} / Guide to yeast genetics and molecular biology. Vol. 194 by Guthrie (1991)
10.1126/science.275.5304.1311 / Science. / APC-mediated proteolysis of Ase1 and the morphogenesis of the mitotic spindle by Juang (1997)
10.1101/gad.13.9.1190 / Genes Dev / Cyclin-dependent kinase and Cks/Suc1 interact with the proteosome in yeast to control proteolysis of M-phase targets by Kaiser (1999)
10.1016/S0960-9822(98)70250-7 / Curr. Biol / Cut1 is loaded onto the spindle by binding to Cut2 and promotes anaphase spindle movement upon Cut2 proteolysis by Kumada (1998)
10.1038/71357 / Nat. Cell Biol. / The polarity and dynamics of microtubule assembly in the budding yeast Saccharomyces cerevisiae by Maddox (2000)
10.1016/S0021-9258(19)49597-5 / J. Biol. Chem / The bimB3 mutation of Aspergillus nidulans uncouples DNA replication from the completion of mitosis by May (1992)
10.1091/mbc.3.12.1443 / Mol. Biol. Cell. / Requirement for ESP1 in the nuclear division of Saccharomyces cerevisiae by McGrew (1992)
10.1016/S0092-8674(01)80007-6 / Cell. / Cohesinschromosomal proteins that prevent premature separation of sister chromatids by Michaelis (1997)
10.1093/genetics/147.2.421 / Genetics. / Identification of genes controlling growth polarity of the budding yeast Saccharomyces cerevisiaea possible role of N-glycosylation and involvement of the exocyst complex by Mondesert (1997)
10.1083/jcb.130.6.1373 / J. Cell Biol / Two microtubule-associated proteins required for anaphase spindle movement in Saccharomyces cerevisiae by Pellman (1995)
10.1016/0092-8674(89)90768-X / Cell. / An essential G1 function for cyclin-like proteins in yeast by Richardson (1989)
10.1038/46080 / Nature. / APCCdc20 promotes exit from mitosis by destroying the anaphase inhibitor Pds1 and cyclin Clb5 by Shiramaya (1999)
10.1093/genetics/122.1.19 / Genetics. / A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae by Sikorski (1989)
10.1128/MCB.20.1.286-298.2000 / Mol. Cell. Biol / Essential function of the polo box of Cdc5 in subcellular localization and induction of cytokinetic structures by Song (2000)
10.1126/science.277.5325.574 / Science. / Mitosis in living budding yeastanaphase A but no metaphase plate by Straight (1997)
10.1083/jcb.119.2.379 / J. Cell Biol / Astral microtubules are not required for anaphase B in Saccharomyces cerevisiae by Sullivan (1992)
10.1101/gad.7.5.822 / Genes Dev / The Cdk-associated protein Cks1 functions both in G1 and G2 in Saccharomyces cerevisiae by Tang (1993)
10.1101/gad.13.15.1936 / Genes Dev / Pds1 and Esp1 control both anaphase and mitotic exit in normal cells and after DNA damage by Tinker-Kulberg (1999)
10.1038/21831 / Nature. / Sister-chromatid separation at anaphase onset is promoted by cleavage of the cohesin subunit Scc1 by Uhlmann (1999)
10.1016/0092-8674(90)90266-H / Cell. / The fission yeast cut1+ gene regulates spindle pole body duplication and has homology to the budding yeast ESP1 gene by Uzawa (1990)
10.1002/yea.320101310 / Yeast. / New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae by Wach (1994)
10.1083/jcb.129.6.1601 / J. Cell Biol / Three-dimensional ultrastructural analysis of the Saccharomyces cerevisiae mitotic spindle by Winey (1995)
10.1083/jcb.133.1.85 / J. Cell Biol / Pds1p is required for faithful execution of anaphase in the yeast, Saccharomyces cerevisiae by Yamamoto (1996)
10.1091/mbc.7.5.791 / Mol. Biol. Cell. / TPR proteins required for anaphase progression mediate ubiquitination of mitotic B-type cyclins in yeast by Zachariae (1996)
10.1126/science.285.5426.418 / Science. / Identification of a vertebrate sister-chromatid separation inhibitor involved in transformation and tumorigenesis by Zou (1999)

Dates

Type	When
Created	23 years, 1 month ago (July 26, 2002, 12:46 p.m.)
Deposited	2 years, 1 month ago (July 28, 2023, 10:53 p.m.)
Indexed	4 months ago (May 2, 2025, 9:30 a.m.)
Issued	24 years, 7 months ago (Jan. 8, 2001)
Published	24 years, 7 months ago (Jan. 8, 2001)
Published Online	24 years, 7 months ago (Jan. 8, 2001)
Published Print	24 years, 7 months ago (Jan. 8, 2001)

Funders 0

None

BibTeX

@article{Jensen_2001, title={A Novel Role of the Budding Yeast Separin Esp1 in Anaphase Spindle Elongation}, volume={152}, ISSN={1540-8140}, url={http://dx.doi.org/10.1083/jcb.152.1.27}, DOI={10.1083/jcb.152.1.27}, number={1}, journal={The Journal of Cell Biology}, publisher={Rockefeller University Press}, author={Jensen, Sanne and Segal, Marisa and Clarke, Duncan J. and Reed, Steven I.}, year={2001}, month=jan, pages={27–40} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        5,
        2
      ]
    ],
    "date-time": "2025-05-02T13:30:15Z",
    "timestamp": 1746192615587
  },
  "reference-count": 34,
  "publisher": "Rockefeller University Press",
  "issue": "1",
  "content-domain": {
    "domain": [
      "rupress.org"
    ],
    "crossmark-restriction": true
  },
  "published-print": {
    "date-parts": [
      [
        2001,
        1,
        8
      ]
    ]
  },
  "abstract": "<jats:p>In Saccharomyces cerevisiae, the metaphase\u2013anaphase transition is initiated by the anaphase-promoting complex\u2013dependent degradation of Pds1, whereby Esp1 is activated to promote sister chromatid separation. Although this is a fundamental step in the cell cycle, little is known about the regulation of Esp1 and how loss of cohesion is coordinated with movement of the anaphase spindle. Here, we show that Esp1 has a novel role in promoting anaphase spindle elongation. The localization of Esp1 to the spindle apparatus, analyzed by live cell imaging, is regulated in a manner consistent with a function during anaphase B. The protein accumulates in the nucleus in G2 and is mobilized onto the spindle pole bodies and spindle midzone at anaphase onset, where it persists into midanaphase. Association with Pds1 occurs during S phase and is required for efficient nuclear targeting of Esp1. Spindle association is not fully restored in pds1 mutants expressing an Esp1-nuclear localization sequence fusion protein, suggesting that Pds1 is also required to promote Esp1 spindle binding. In agreement, Pds1 interacts with the spindle at the metaphase\u2013anaphase transition and a fraction remains at the spindle pole bodies and the spindle midzone in anaphase cells. Finally, mutational analysis reveals that the conserved COOH-terminal region of Esp1 is important for spindle interaction.</jats:p>",
  "DOI": "10.1083/jcb.152.1.27",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2002,
        7,
        26
      ]
    ],
    "date-time": "2002-07-26T16:46:23Z",
    "timestamp": 1027701983000
  },
  "page": "27-40",
  "update-policy": "http://dx.doi.org/10.1083/jcb.crossmarkpolicy",
  "source": "Crossref",
  "is-referenced-by-count": 109,
  "title": "A Novel Role of the Budding Yeast Separin Esp1 in Anaphase Spindle Elongation",
  "prefix": "10.1083",
  "volume": "152",
  "author": [
    {
      "given": "Sanne",
      "family": "Jensen",
      "sequence": "first",
      "affiliation": [
        {
          "name": "aDepartment of Molecular Biology, The Scripps Research Institute, La Jolla, California 92037"
        }
      ]
    },
    {
      "given": "Marisa",
      "family": "Segal",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "aDepartment of Molecular Biology, The Scripps Research Institute, La Jolla, California 92037"
        }
      ]
    },
    {
      "given": "Duncan J.",
      "family": "Clarke",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "aDepartment of Molecular Biology, The Scripps Research Institute, La Jolla, California 92037"
        }
      ]
    },
    {
      "given": "Steven I.",
      "family": "Reed",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "aDepartment of Molecular Biology, The Scripps Research Institute, La Jolla, California 92037"
        }
      ]
    }
  ],
  "member": "291",
  "published-online": {
    "date-parts": [
      [
        2001,
        1,
        8
      ]
    ]
  },
  "reference": [
    {
      "key": "2023072902512869500_Alexandruetal1999",
      "doi-asserted-by": "crossref",
      "first-page": "2707",
      "DOI": "10.1093/emboj/18.10.2707",
      "article-title": "Sister chromatid separation and chromosome re-duplication are regulated by different mechanisms in response to spindle damage",
      "volume": "18",
      "author": "Alexandru",
      "year": "1999",
      "journal-title": "EMBO (Eur. Mol. Biol. Organ.) J"
    },
    {
      "key": "2023072902512869500_Bardinetal2000",
      "doi-asserted-by": "crossref",
      "first-page": "21",
      "DOI": "10.1016/S0092-8674(00)00007-6",
      "article-title": "A mechanism for coupling exit of mitosis to partitioning of the nucleus",
      "volume": "102",
      "author": "Bardin",
      "year": "2000",
      "journal-title": "Cell."
    },
    {
      "key": "2023072902512869500_Ciosketal1998",
      "doi-asserted-by": "crossref",
      "first-page": "1067",
      "DOI": "10.1016/S0092-8674(00)81211-8",
      "article-title": "An ESP1/PDS1 complex regulates loss of sister chromatid cohesion at the metaphase to anaphase transition in yeast",
      "volume": "93",
      "author": "Ciosk",
      "year": "1998",
      "journal-title": "Cell."
    },
    {
      "key": "2023072902512869500_Clarkeetal1999",
      "doi-asserted-by": "crossref",
      "first-page": "365",
      "DOI": "10.1016/S0960-9822(99)80163-8",
      "article-title": "The Pds1 anaphase inhibitor and Mec1 kinase define distinct checkpoints coupling S phase with mitosis in budding yeast",
      "volume": "9",
      "author": "Clarke",
      "year": "1999",
      "journal-title": "Curr. Biol."
    },
    {
      "key": "2023072902512869500_Cohen-FixandKoshland1999",
      "doi-asserted-by": "crossref",
      "first-page": "1950",
      "DOI": "10.1101/gad.13.15.1950",
      "article-title": "Pds1p of budding yeast has dual rolesinhibition of anaphase initiation and regulation of mitotic exit",
      "volume": "13",
      "author": "Cohen-Fix",
      "year": "1999",
      "journal-title": "Genes Dev"
    },
    {
      "key": "2023072902512869500_Cohen-Fixetal1996",
      "doi-asserted-by": "crossref",
      "first-page": "3081",
      "DOI": "10.1101/gad.10.24.3081",
      "article-title": "Anaphase initiation in Saccharomyces cerevisiae is controlled by the APC-dependent degradation of the anaphase inhibitor Pds1p",
      "volume": "10",
      "author": "Cohen-Fix",
      "year": "1996",
      "journal-title": "Genes Dev"
    },
    {
      "key": "2023072902512869500_Funabikietal1996",
      "doi-asserted-by": "crossref",
      "first-page": "6617",
      "DOI": "10.1002/j.1460-2075.1996.tb01052.x",
      "article-title": "Fission yeast Cut1 and Cut2 are essential for sister chromatid separation, concentrate along the metaphase spindle and form large complexes",
      "volume": "15",
      "author": "Funabiki",
      "year": "1996",
      "journal-title": "EMBO (Eur. Mol. Biol. Organ.) J"
    },
    {
      "key": "2023072902512869500_GohandKilmartin1993",
      "doi-asserted-by": "crossref",
      "first-page": "503",
      "DOI": "10.1083/jcb.121.3.503",
      "article-title": "NDC10a gene involved in chromosome segregation in Saccharomyces cerevisiae",
      "volume": "121",
      "author": "Goh",
      "year": "1993",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2023072902512869500_GroignoandWhitaker1998",
      "doi-asserted-by": "crossref",
      "first-page": "193",
      "DOI": "10.1016/S0092-8674(00)80914-9",
      "article-title": "An anaphase calcium signal controls chromosome disjunction in early sea urchin embryos",
      "volume": "92",
      "author": "Groigno",
      "year": "1998",
      "journal-title": "Cell."
    },
    {
      "key": "2023072902512869500_GuthrieandFink1991",
      "volume-title": "Guide to yeast genetics and molecular biology. Vol. 194",
      "author": "Guthrie",
      "year": "1991"
    },
    {
      "key": "2023072902512869500_Juangetal1997",
      "doi-asserted-by": "crossref",
      "first-page": "1311",
      "DOI": "10.1126/science.275.5304.1311",
      "article-title": "APC-mediated proteolysis of Ase1 and the morphogenesis of the mitotic spindle",
      "volume": "275",
      "author": "Juang",
      "year": "1997",
      "journal-title": "Science."
    },
    {
      "key": "2023072902512869500_Kaiseretal1999",
      "doi-asserted-by": "crossref",
      "first-page": "1190",
      "DOI": "10.1101/gad.13.9.1190",
      "article-title": "Cyclin-dependent kinase and Cks/Suc1 interact with the proteosome in yeast to control proteolysis of M-phase targets",
      "volume": "13",
      "author": "Kaiser",
      "year": "1999",
      "journal-title": "Genes Dev"
    },
    {
      "key": "2023072902512869500_Kumadaetal1998",
      "doi-asserted-by": "crossref",
      "first-page": "633",
      "DOI": "10.1016/S0960-9822(98)70250-7",
      "article-title": "Cut1 is loaded onto the spindle by binding to Cut2 and promotes anaphase spindle movement upon Cut2 proteolysis",
      "volume": "8",
      "author": "Kumada",
      "year": "1998",
      "journal-title": "Curr. Biol"
    },
    {
      "key": "2023072902512869500_Maddoxetal2000",
      "doi-asserted-by": "crossref",
      "first-page": "36",
      "DOI": "10.1038/71357",
      "article-title": "The polarity and dynamics of microtubule assembly in the budding yeast Saccharomyces cerevisiae",
      "volume": "2",
      "author": "Maddox",
      "year": "2000",
      "journal-title": "Nat. Cell Biol."
    },
    {
      "key": "2023072902512869500_Mayetal1992",
      "doi-asserted-by": "crossref",
      "first-page": "15737",
      "DOI": "10.1016/S0021-9258(19)49597-5",
      "article-title": "The bimB3 mutation of Aspergillus nidulans uncouples DNA replication from the completion of mitosis",
      "volume": "267",
      "author": "May",
      "year": "1992",
      "journal-title": "J. Biol. Chem"
    },
    {
      "key": "2023072902512869500_McGrewetal1992",
      "doi-asserted-by": "crossref",
      "first-page": "1443",
      "DOI": "10.1091/mbc.3.12.1443",
      "article-title": "Requirement for ESP1 in the nuclear division of Saccharomyces cerevisiae",
      "volume": "3",
      "author": "McGrew",
      "year": "1992",
      "journal-title": "Mol. Biol. Cell."
    },
    {
      "key": "2023072902512869500_Michaelisetal1997",
      "doi-asserted-by": "crossref",
      "first-page": "35",
      "DOI": "10.1016/S0092-8674(01)80007-6",
      "article-title": "Cohesinschromosomal proteins that prevent premature separation of sister chromatids",
      "volume": "91",
      "author": "Michaelis",
      "year": "1997",
      "journal-title": "Cell."
    },
    {
      "key": "2023072902512869500_Mondesertetal1997",
      "doi-asserted-by": "crossref",
      "first-page": "421",
      "DOI": "10.1093/genetics/147.2.421",
      "article-title": "Identification of genes controlling growth polarity of the budding yeast Saccharomyces cerevisiaea possible role of N-glycosylation and involvement of the exocyst complex",
      "volume": "147",
      "author": "Mondesert",
      "year": "1997",
      "journal-title": "Genetics."
    },
    {
      "key": "2023072902512869500_Pellmanetal1995",
      "doi-asserted-by": "crossref",
      "first-page": "1373",
      "DOI": "10.1083/jcb.130.6.1373",
      "article-title": "Two microtubule-associated proteins required for anaphase spindle movement in Saccharomyces cerevisiae",
      "volume": "130",
      "author": "Pellman",
      "year": "1995",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2023072902512869500_Richardsonetal1989",
      "doi-asserted-by": "crossref",
      "first-page": "1127",
      "DOI": "10.1016/0092-8674(89)90768-X",
      "article-title": "An essential G1 function for cyclin-like proteins in yeast",
      "volume": "59",
      "author": "Richardson",
      "year": "1989",
      "journal-title": "Cell."
    },
    {
      "key": "2023072902512869500_Shiramayaetal1999",
      "doi-asserted-by": "crossref",
      "first-page": "203",
      "DOI": "10.1038/46080",
      "article-title": "APCCdc20 promotes exit from mitosis by destroying the anaphase inhibitor Pds1 and cyclin Clb5",
      "volume": "11",
      "author": "Shiramaya",
      "year": "1999",
      "journal-title": "Nature."
    },
    {
      "key": "2023072902512869500_SikorskiandHieter1989",
      "doi-asserted-by": "crossref",
      "first-page": "19",
      "DOI": "10.1093/genetics/122.1.19",
      "article-title": "A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae",
      "volume": "122",
      "author": "Sikorski",
      "year": "1989",
      "journal-title": "Genetics."
    },
    {
      "key": "2023072902512869500_Songetal2000",
      "doi-asserted-by": "crossref",
      "first-page": "286",
      "DOI": "10.1128/MCB.20.1.286-298.2000",
      "article-title": "Essential function of the polo box of Cdc5 in subcellular localization and induction of cytokinetic structures",
      "volume": "20",
      "author": "Song",
      "year": "2000",
      "journal-title": "Mol. Cell. Biol"
    },
    {
      "key": "2023072902512869500_Straightetal1997",
      "doi-asserted-by": "crossref",
      "first-page": "574",
      "DOI": "10.1126/science.277.5325.574",
      "article-title": "Mitosis in living budding yeastanaphase A but no metaphase plate",
      "volume": "277",
      "author": "Straight",
      "year": "1997",
      "journal-title": "Science."
    },
    {
      "key": "2023072902512869500_SullivanandHuffaker1992",
      "doi-asserted-by": "crossref",
      "first-page": "379",
      "DOI": "10.1083/jcb.119.2.379",
      "article-title": "Astral microtubules are not required for anaphase B in Saccharomyces cerevisiae",
      "volume": "119",
      "author": "Sullivan",
      "year": "1992",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2023072902512869500_TangandReed1993",
      "doi-asserted-by": "crossref",
      "first-page": "822",
      "DOI": "10.1101/gad.7.5.822",
      "article-title": "The Cdk-associated protein Cks1 functions both in G1 and G2 in Saccharomyces cerevisiae",
      "volume": "7",
      "author": "Tang",
      "year": "1993",
      "journal-title": "Genes Dev"
    },
    {
      "key": "2023072902512869500_Tinker-KulbergandMorgan1999",
      "doi-asserted-by": "crossref",
      "first-page": "1936",
      "DOI": "10.1101/gad.13.15.1936",
      "article-title": "Pds1 and Esp1 control both anaphase and mitotic exit in normal cells and after DNA damage",
      "volume": "13",
      "author": "Tinker-Kulberg",
      "year": "1999",
      "journal-title": "Genes Dev"
    },
    {
      "key": "2023072902512869500_Uhlmannetal1999",
      "doi-asserted-by": "crossref",
      "first-page": "37",
      "DOI": "10.1038/21831",
      "article-title": "Sister-chromatid separation at anaphase onset is promoted by cleavage of the cohesin subunit Scc1",
      "volume": "400",
      "author": "Uhlmann",
      "year": "1999",
      "journal-title": "Nature."
    },
    {
      "key": "2023072902512869500_Uzawaetal1990",
      "doi-asserted-by": "crossref",
      "first-page": "913",
      "DOI": "10.1016/0092-8674(90)90266-H",
      "article-title": "The fission yeast cut1+ gene regulates spindle pole body duplication and has homology to the budding yeast ESP1 gene",
      "volume": "62",
      "author": "Uzawa",
      "year": "1990",
      "journal-title": "Cell."
    },
    {
      "key": "2023072902512869500_Wachetal1994",
      "doi-asserted-by": "crossref",
      "first-page": "1793",
      "DOI": "10.1002/yea.320101310",
      "article-title": "New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae",
      "volume": "10",
      "author": "Wach",
      "year": "1994",
      "journal-title": "Yeast."
    },
    {
      "key": "2023072902512869500_Wineyetal1995",
      "doi-asserted-by": "crossref",
      "first-page": "1601",
      "DOI": "10.1083/jcb.129.6.1601",
      "article-title": "Three-dimensional ultrastructural analysis of the Saccharomyces cerevisiae mitotic spindle",
      "volume": "129",
      "author": "Winey",
      "year": "1995",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2023072902512869500_Yamamotoetal1996",
      "doi-asserted-by": "crossref",
      "first-page": "85",
      "DOI": "10.1083/jcb.133.1.85",
      "article-title": "Pds1p is required for faithful execution of anaphase in the yeast, Saccharomyces cerevisiae",
      "volume": "133",
      "author": "Yamamoto",
      "year": "1996",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2023072902512869500_ZachariaeandNasmyth1996",
      "doi-asserted-by": "crossref",
      "first-page": "791",
      "DOI": "10.1091/mbc.7.5.791",
      "article-title": "TPR proteins required for anaphase progression mediate ubiquitination of mitotic B-type cyclins in yeast",
      "volume": "7",
      "author": "Zachariae",
      "year": "1996",
      "journal-title": "Mol. Biol. Cell."
    },
    {
      "key": "2023072902512869500_Zouetal1999",
      "doi-asserted-by": "crossref",
      "first-page": "418",
      "DOI": "10.1126/science.285.5426.418",
      "article-title": "Identification of a vertebrate sister-chromatid separation inhibitor involved in transformation and tumorigenesis",
      "volume": "285",
      "author": "Zou",
      "year": "1999",
      "journal-title": "Science."
    }
  ],
  "container-title": "The Journal of Cell Biology",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://rupress.org/jcb/article-pdf/152/1/27/1862585/0007076.pdf",
      "content-type": "application/pdf",
      "content-version": "vor",
      "intended-application": "syndication"
    },
    {
      "URL": "https://rupress.org/jcb/article-pdf/152/1/27/1862585/0007076.pdf",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2023,
        7,
        29
      ]
    ],
    "date-time": "2023-07-29T02:53:27Z",
    "timestamp": 1690599207000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://rupress.org/jcb/article/152/1/27/32156/A-Novel-Role-of-the-Budding-Yeast-Separin-Esp1-in"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        2001,
        1,
        8
      ]
    ]
  },
  "references-count": 34,
  "journal-issue": {
    "issue": "1",
    "published-print": {
      "date-parts": [
        [
          2001,
          1,
          8
        ]
      ]
    }
  },
  "URL": "http://dx.doi.org/10.1083/jcb.152.1.27",
  "relation": {},
  "ISSN": [
    "0021-9525",
    "1540-8140"
  ],
  "subject": [],
  "published": {
    "date-parts": [
      [
        2001,
        1,
        8
      ]
    ]
  }
}