DOI: 10.1083/jcb.200909013. Integrating high-throughput genetic interaction mapping and high-content screening to explore yeast spindle morphogenesis

Integrating high-throughput genetic interaction mapping and high-content screening to explore yeast spindle morphogenesis

10.1083/jcb.200909013

Crossref journal-article

Rockefeller University Press

Journal of Cell Biology (291)

Abstract

We describe the application of a novel screening approach that combines automated yeast genetics, synthetic genetic array (SGA) analysis, and a high-content screening (HCS) system to examine mitotic spindle morphogenesis. We measured numerous spindle and cellular morphological parameters in thousands of single mutants and corresponding sensitized double mutants lacking genes known to be involved in spindle function. We focused on a subset of genes that appear to define a highly conserved mitotic spindle disassembly pathway, which is known to involve Ipl1p, the yeast aurora B kinase, as well as the cell cycle regulatory networks mitotic exit network (MEN) and fourteen early anaphase release (FEAR). We also dissected the function of the kinetochore protein Mcm21p, showing that sumoylation of Mcm21p regulates the enrichment of Ipl1p and other chromosomal passenger proteins to the spindle midzone to mediate spindle disassembly. Although we focused on spindle disassembly in a proof-of-principle study, our integrated HCS-SGA method can be applied to virtually any pathway, making it a powerful means for identifying specific cellular functions.

Bibliography

Vizeacoumar, F. J., van Dyk, N., S.Vizeacoumar, F., Cheung, V., Li, J., Sydorskyy, Y., Case, N., Li, Z., Datti, A., Nislow, C., Raught, B., Zhang, Z., Frey, B., Bloom, K., Boone, C., & Andrews, B. J. (2010). Integrating high-throughput genetic interaction mapping and high-content screening to explore yeast spindle morphogenesis. Journal of Cell Biology, 188(1), 69â81.

Authors 16

Franco J. Vizeacoumar (first)
Nydia van Dyk (additional)
Frederick S.Vizeacoumar (additional)
Vincent Cheung (additional)
Jingjing Li (additional)
Yaroslav Sydorskyy (additional)
Nicolle Case (additional)
Zhijian Li (additional)
Alessandro Datti (additional)
Corey Nislow (additional)
Brian Raught (additional)
Zhaolei Zhang (additional)
Brendan Frey (additional)
Kerry Bloom (additional)
Charles Boone (additional)
Brenda J. Andrews (additional)

References 70 Referenced 90

10.1371/journal.pcbi.1000065 / PLOS Comput. Biol. / Functional maps of protein complexes from quantitative genetic interaction data by Bandyopadhyay (2008)
{'key': '2023072916301348600_bib2', 'first-page': '738', 'article-title': 'Pattern Recognition and Machine Learning', 'author': 'Bishop', 'year': '2006'} / Pattern Recognition and Machine Learning by Bishop (2006)
10.1016/j.cell.2005.02.016 / Cell. / A Rae1-containing ribonucleoprotein complex is required for mitotic spindle assembly by Blower (2005)
10.1038/nrg2085 / Nat. Rev. Genet. / Exploring genetic interactions and networks with yeast by Boone (2007)
10.1016/S1534-5807(03)00129-1 / Dev. Cell. / Division of the nucleolus and its release of CDC14 during anaphase of meiosis I depends on separase, SPO12, and SLK19 by Buonomo (2003)
10.1083/jcb.200209018 / J. Cell Biol. / The budding yeast Ipl1/Aurora protein kinase regulates mitotic spindle disassembly by Buvelot (2003)
10.1128/jb.124.1.511-523.1975 / J. Bacteriol. / Behavior of spindles and spindle plaques in the cell cycle and conjugation of Saccharomyces cerevisiae by Byers (1975)
10.1074/jbc.274.34.24378 / J. Biol. Chem. / The tumor suppressor protein Fhit. A novel interaction with tubulin by Chaudhuri (1999)
10.1101/gad.1247304 / Genes Dev. / At the interface between signaling and executing anaphase—Cdc14 and the FEAR network by D’Amours (2004)
10.1074/mcp.M400154-MCP200 / Mol. Cell. Proteomics. / A proteomic strategy for gaining insights into protein sumoylation in yeast by Denison (2005)
10.1093/genetics/163.1.47 / Genetics. / Large-scale functional genomic analysis of sporulation and meiosis in Saccharomyces cerevisiae by Enyenihi (2003)
10.1093/emboj/18.9.2424 / EMBO J. / A Bub2p-dependent spindle checkpoint pathway regulates the Dbf2p kinase in budding yeast by Fesquet (1999)
10.1083/jcb.200404001 / J. Cell Biol. / Borealin: a novel chromosomal passenger required for stability of the bipolar mitotic spindle by Gassmann (2004)
10.1074/jbc.M202540200 / J. Biol. Chem. / Control of mitotic exit in budding yeast. In vitro regulation of Tem1 GTPase by Bub2 and Bfa1 by Geymonat (2002)
10.1038/nature00935 / Nature. / Functional profiling of the Saccharomyces cerevisiae genome by Giaever (2002)
10.1074/mcp.M300099-MCP200 / Mol. Cell. Proteomics. / Applicability of tandem affinity purification MudPIT to pathway proteomics in yeast by Graumann (2004)
10.1038/ncb1457 / Nat. Cell Biol. / Plus end-specific depolymerase activity of Kip3, a kinesin-8 protein, explains its role in positioning the yeast mitotic spindle by Gupta (2006)
10.1074/jbc.M413209200 / J. Biol. Chem. / Defining the SUMO-modified proteome by multiple approaches in Saccharomyces cerevisiae by Hannich (2005)
10.1021/nl015521e / Nano Lett. / Light-controlled molecular shuttles made from motor proteins carrying cargo on engineered surfaces by Hess (2001)
10.4161/cc.3.6.950 / Cell Cycle. / Temporal coupling of spindle disassembly and cytokinesis is disrupted by deletion of LTE1 in budding yeast by Jensen (2004)
10.1002/pmic.200800666 / Proteomics. / Using mass spectrometry to identify ubiquitin and ubiquitin-like protein conjugation sites by Jeram (2009)
10.1016/S0168-9525(98)01637-0 / Trends Genet. / Feasting, fasting and fermenting. Glucose sensing in yeast and other cells by Johnston (1999)
10.1002/cm.970250203 / Cell Motil. Cytoskeleton. / Video microscopy of organelle inheritance and motility in budding yeast by Jones (1993)
{'key': '2023072916301348600_bib24', 'first-page': '342', 'article-title': 'Finding groups in data: an introduction to cluster analysis', 'author': 'Kaufman', 'year': '1990'} / Finding groups in data: an introduction to cluster analysis by Kaufman (1990)
10.4161/cc.7.3.5349 / Cell Cycle. / Assembling the spindle midzone in the right place at the right time by Khmelinskii (2008)
10.1083/jcb.200702145 / J. Cell Biol. / Cdc14-regulated midzone assembly controls anaphase B by Khmelinskii (2007)
10.1083/jcb.98.3.922 / J. Cell Biol. / Structural rearrangements of tubulin and actin during the cell cycle of the yeast Saccharomyces by Kilmartin (1984)
10.1038/nature03159 / Nature. / An endoribonuclease-prepared siRNA screen in human cells identifies genes essential for cell division by Kittler (2004)
10.4161/cc.8.16.9267 / Cell Cycle. / The COMA complex is required for Sli15/INCENP-mediated correction of defective kinetochore attachments by Knockleby (2009)
10.1128/MCB.18.4.2100 / Mol. Cell. Biol. / DBF2 protein kinase binds to and acts through the cell cycle-regulated MOB1 protein by Komarnitsky (1998)
10.1083/jcb.144.5.947 / J. Cell Biol. / Control of mitotic spindle position by the Saccharomyces cerevisiae formin Bni1p by Lee (1999)
10.1016/j.molcel.2008.12.025 / Mol. Cell. / Global map of SUMO function revealed by protein-protein interaction and genetic networks by Makhnevych (2009)
10.1016/S1534-5807(03)00130-8 / Dev. Cell. / The Cdc14 phosphatase and the FEAR network control meiotic spindle disassembly and chromosome segregation by Marston (2003)
10.1146/annurev.cellbio.16.1.591 / Annu. Rev. Cell Dev. Biol. / SUMO—nonclassical ubiquitin by Melchior (2000)
10.1126/science.270.5239.1213 / Science. / Requirement of Saccharomyces cerevisiae Ras for completion of mitosis by Morishita (1995)
10.1038/35056591 / Nat. Rev. Mol. Cell Biol. / SUMO, ubiquitin’s mysterious cousin by Müller (2001)
10.1073/pnas.0509436102 / Proc. Natl. Acad. Sci. USA. / High-dimensional and large-scale phenotyping of yeast mutants by Ohya (2005)
10.1074/jbc.M407950200 / J. Biol. Chem. / A proteome-wide approach identifies sumoylated substrate proteins in yeast by Panse (2004)
10.1126/science.1091936 / Science. / Separase regulates INCENP-Aurora B anaphase spindle function through Cdc14 by Pereira (2003)
10.1016/S1097-2765(00)00002-2 / Mol. Cell. / The Bub2p spindle checkpoint links nuclear migration with mitotic exit by Pereira (2000)
10.1093/emboj/20.22.6359 / EMBO J. / Modes of spindle pole body inheritance and segregation of the Bfa1p-Bub2p checkpoint protein complex by Pereira (2001)
10.1146/annurev.cellbio.20.010403.103108 / Annu. Rev. Cell Dev. Biol. / Mechanisms of polarized growth and organelle segregation in yeast by Pruyne (2004)
10.1073/pnas.062059999 / Proc. Natl. Acad. Sci. USA. / Bfa1 can regulate Tem1 function independently of Bub2 in the mitotic exit network of Saccharomyces cerevisiae by Ro (2002)
10.1186/1471-2105-3-35 / BMC Bioinformatics. / FunSpec: a web-based cluster interpreter for yeast by Robinson (2002)
10.1016/j.cell.2007.10.002 / Cell. / The chromosomal passenger complex: one for all and all for one by Ruchaud (2007)
10.1038/24550 / Nature. / Hsp90 as a capacitor for morphological evolution by Rutherford (1998)
10.1038/nrm1200 / Nat. Rev. Mol. Cell Biol. / Nuclear and unclear functions of SUMO by Seeler (2003)
10.1002/yea.1130 / Yeast. / Optimized cassettes for fluorescent protein tagging in Saccharomyces cerevisiae by Sheff (2004)
10.1016/j.molcel.2005.12.011 / Mol. Cell. / Mapping pathways and phenotypes by systematic gene overexpression by Sopko (2006)
10.1146/annurev.genet.38.072902.093051 / Annu. Rev. Genet. / Closing mitosis: the functions of the Cdc14 phosphatase and its regulation by Stegmeier (2004)
10.1016/S0092-8674(02)00618-9 / Cell. / Separase, polo kinase, the kinetochore protein Slk19, and Spo12 function in a network that controls Cdc14 localization during early anaphase by Stegmeier (2002)
10.1091/mbc.E05-04-0337 / Mol. Biol. Cell. / The mitotic exit network Mob1p-Dbf2p kinase complex localizes to the nucleus and regulates passenger protein localization by Stoepel (2005)
10.1038/ncb940 / Nat. Cell Biol. / A non-proteolytic function of separase links the onset of anaphase to mitotic exit by Sullivan (2003)
10.1038/ncb0901-771 / Nat. Cell Biol. / Orchestrating anaphase and mitotic exit: separase cleavage and localization of Slk19 by Sullivan (2001)
10.1091/mbc.E07-03-0201 / Mol. Biol. Cell. / A Bir1p Sli15p kinetochore passenger complex regulates septin organization during anaphase by Thomas (2007)
10.1126/science.1065810 / Science. / Systematic genetic analysis with ordered arrays of yeast deletion mutants by Tong (2001)
10.1126/science.1091317 / Science. / Global mapping of the yeast genetic interaction network by Tong (2004)
10.1002/j.1460-2075.1994.tb06359.x / EMBO J. / The Dbf2 and Dbf20 protein kinases of budding yeast are activated after the metaphase to anaphase cell cycle transition by Toyn (1994)
10.1002/neu.10314 / J. Neurobiol. / Dynein: An ancient motor protein involved in multiple modes of transport by Vallee (2004)
10.1101/gad.1601308 / Genes Dev. / APC/C-Cdh1-mediated degradation of the Polo kinase Cdc5 promotes the return of Cdc14 into the nucleolus by Visintin (2008)
10.1016/j.febslet.2009.03.068 / FEBS Lett. / A picture is worth a thousand words: genomics to phenomics in the yeast Saccharomyces cerevisiae by Vizeacoumar (2009)
10.1016/S0014-5793(01)03136-2 / FEBS Lett. / Tubulin and microtubule are potential targets for brain hexokinase binding by Wágner (2001)
10.1074/jbc.M409203200 / J. Biol. Chem. / Global analysis of protein sumoylation in Saccharomyces cerevisiae by Wohlschlegel (2004)
10.1074/mcp.M400166-MCP200 / Mol. Cell. Proteomics. / Identification of sumoylated proteins by systematic immunoprecipitation of the budding yeast proteome by Wykoff (2005)
10.1534/genetics.107.072876 / Genetics. / Genetic dissection of parallel sister-chromatid cohesion pathways by Xu (2007)
10.1083/jcb.130.3.687 / J. Cell Biol. / Spindle dynamics and cell cycle regulation of dynein in the budding yeast, Saccharomyces cerevisiae by Yeh (1995)
10.1083/jcb.200301128 / J. Cell Biol. / Ras recruits mitotic exit regulator Lte1 to the bud cortex in budding yeast by Yoshida (2003)
10.1083/jcb.146.2.415 / J. Cell Biol. / Slk19p is a centromere protein that functions to stabilize mitotic spindles by Zeng (1999)
10.1073/pnas.0500537102 / Proc. Natl. Acad. Sci. USA. / A SUMO ligase is part of a nuclear multiprotein complex that affects DNA repair and chromosomal organization by Zhao (2005)
10.1074/jbc.M404173200 / J. Biol. Chem. / Global analyses of sumoylated proteins in Saccharomyces cerevisiae. Induction of protein sumoylation by cellular stresses by Zhou (2004)

Dates

Type	When
Created	15 years, 7 months ago (Jan. 11, 2010, 2:05 p.m.)
Deposited	2 years, 1 month ago (July 29, 2023, 12:33 p.m.)
Indexed	11 months, 3 weeks ago (Sept. 9, 2024, 6:37 a.m.)
Issued	15 years, 7 months ago (Jan. 11, 2010)
Published	15 years, 7 months ago (Jan. 11, 2010)
Published Online	15 years, 7 months ago (Jan. 11, 2010)
Published Print	15 years, 7 months ago (Jan. 11, 2010)

Funders 0

None

BibTeX

@article{Vizeacoumar_2010, title={Integrating high-throughput genetic interaction mapping and high-content screening to explore yeast spindle morphogenesis}, volume={188}, ISSN={0021-9525}, url={http://dx.doi.org/10.1083/jcb.200909013}, DOI={10.1083/jcb.200909013}, number={1}, journal={Journal of Cell Biology}, publisher={Rockefeller University Press}, author={Vizeacoumar, Franco J. and van Dyk, Nydia and S.Vizeacoumar, Frederick and Cheung, Vincent and Li, Jingjing and Sydorskyy, Yaroslav and Case, Nicolle and Li, Zhijian and Datti, Alessandro and Nislow, Corey and Raught, Brian and Zhang, Zhaolei and Frey, Brendan and Bloom, Kerry and Boone, Charles and Andrews, Brenda J.}, year={2010}, month=jan, pages={69–81} }

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      "journal-title": "Nat. Rev. Genet."
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      "first-page": "727",
      "DOI": "10.1016/S1534-5807(03)00129-1",
      "article-title": "Division of the nucleolus and its release of CDC14 during anaphase of meiosis I depends on separase, SPO12, and SLK19",
      "volume": "4",
      "author": "Buonomo",
      "year": "2003",
      "journal-title": "Dev. Cell."
    },
    {
      "key": "2023072916301348600_bib6",
      "doi-asserted-by": "publisher",
      "first-page": "329",
      "DOI": "10.1083/jcb.200209018",
      "article-title": "The budding yeast Ipl1/Aurora protein kinase regulates mitotic spindle disassembly",
      "volume": "160",
      "author": "Buvelot",
      "year": "2003",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072916301348600_bib7",
      "doi-asserted-by": "crossref",
      "first-page": "511",
      "DOI": "10.1128/jb.124.1.511-523.1975",
      "article-title": "Behavior of spindles and spindle plaques in the cell cycle and conjugation of Saccharomyces cerevisiae",
      "volume": "124",
      "author": "Byers",
      "year": "1975",
      "journal-title": "J. Bacteriol."
    },
    {
      "key": "2023072916301348600_bib8",
      "doi-asserted-by": "publisher",
      "first-page": "24378",
      "DOI": "10.1074/jbc.274.34.24378",
      "article-title": "The tumor suppressor protein Fhit. A novel interaction with tubulin",
      "volume": "274",
      "author": "Chaudhuri",
      "year": "1999",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2023072916301348600_bib9",
      "doi-asserted-by": "publisher",
      "first-page": "2581",
      "DOI": "10.1101/gad.1247304",
      "article-title": "At the interface between signaling and executing anaphase\u2014Cdc14 and the FEAR network",
      "volume": "18",
      "author": "D\u2019Amours",
      "year": "2004",
      "journal-title": "Genes Dev."
    },
    {
      "key": "2023072916301348600_bib10",
      "doi-asserted-by": "publisher",
      "first-page": "246",
      "DOI": "10.1074/mcp.M400154-MCP200",
      "article-title": "A proteomic strategy for gaining insights into protein sumoylation in yeast",
      "volume": "4",
      "author": "Denison",
      "year": "2005",
      "journal-title": "Mol. Cell. Proteomics."
    },
    {
      "key": "2023072916301348600_bib11",
      "doi-asserted-by": "crossref",
      "first-page": "47",
      "DOI": "10.1093/genetics/163.1.47",
      "article-title": "Large-scale functional genomic analysis of sporulation and meiosis in Saccharomyces cerevisiae",
      "volume": "163",
      "author": "Enyenihi",
      "year": "2003",
      "journal-title": "Genetics."
    },
    {
      "key": "2023072916301348600_bib12",
      "doi-asserted-by": "publisher",
      "first-page": "2424",
      "DOI": "10.1093/emboj/18.9.2424",
      "article-title": "A Bub2p-dependent spindle checkpoint pathway regulates the Dbf2p kinase in budding yeast",
      "volume": "18",
      "author": "Fesquet",
      "year": "1999",
      "journal-title": "EMBO J."
    },
    {
      "key": "2023072916301348600_bib13",
      "doi-asserted-by": "publisher",
      "first-page": "179",
      "DOI": "10.1083/jcb.200404001",
      "article-title": "Borealin: a novel chromosomal passenger required for stability of the bipolar mitotic spindle",
      "volume": "166",
      "author": "Gassmann",
      "year": "2004",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072916301348600_bib14",
      "doi-asserted-by": "publisher",
      "first-page": "28439",
      "DOI": "10.1074/jbc.M202540200",
      "article-title": "Control of mitotic exit in budding yeast. In vitro regulation of Tem1 GTPase by Bub2 and Bfa1",
      "volume": "277",
      "author": "Geymonat",
      "year": "2002",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2023072916301348600_bib15",
      "doi-asserted-by": "publisher",
      "first-page": "387",
      "DOI": "10.1038/nature00935",
      "article-title": "Functional profiling of the Saccharomyces cerevisiae genome",
      "volume": "418",
      "author": "Giaever",
      "year": "2002",
      "journal-title": "Nature."
    },
    {
      "key": "2023072916301348600_bib16",
      "doi-asserted-by": "publisher",
      "first-page": "226",
      "DOI": "10.1074/mcp.M300099-MCP200",
      "article-title": "Applicability of tandem affinity purification MudPIT to pathway proteomics in yeast",
      "volume": "3",
      "author": "Graumann",
      "year": "2004",
      "journal-title": "Mol. Cell. Proteomics."
    },
    {
      "key": "2023072916301348600_bib17",
      "doi-asserted-by": "publisher",
      "first-page": "913",
      "DOI": "10.1038/ncb1457",
      "article-title": "Plus end-specific depolymerase activity of Kip3, a kinesin-8 protein, explains its role in positioning the yeast mitotic spindle",
      "volume": "8",
      "author": "Gupta",
      "year": "2006",
      "journal-title": "Nat. Cell Biol."
    },
    {
      "key": "2023072916301348600_bib18",
      "doi-asserted-by": "publisher",
      "first-page": "4102",
      "DOI": "10.1074/jbc.M413209200",
      "article-title": "Defining the SUMO-modified proteome by multiple approaches in Saccharomyces cerevisiae",
      "volume": "280",
      "author": "Hannich",
      "year": "2005",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2023072916301348600_bib19",
      "doi-asserted-by": "publisher",
      "first-page": "235",
      "DOI": "10.1021/nl015521e",
      "article-title": "Light-controlled molecular shuttles made from motor proteins carrying cargo on engineered surfaces",
      "volume": "1",
      "author": "Hess",
      "year": "2001",
      "journal-title": "Nano Lett."
    },
    {
      "key": "2023072916301348600_bib20",
      "doi-asserted-by": "crossref",
      "first-page": "817",
      "DOI": "10.4161/cc.3.6.950",
      "article-title": "Temporal coupling of spindle disassembly and cytokinesis is disrupted by deletion of LTE1 in budding yeast",
      "volume": "3",
      "author": "Jensen",
      "year": "2004",
      "journal-title": "Cell Cycle."
    },
    {
      "key": "2023072916301348600_bib21",
      "doi-asserted-by": "publisher",
      "first-page": "922",
      "DOI": "10.1002/pmic.200800666",
      "article-title": "Using mass spectrometry to identify ubiquitin and ubiquitin-like protein conjugation sites",
      "volume": "9",
      "author": "Jeram",
      "year": "2009",
      "journal-title": "Proteomics."
    },
    {
      "key": "2023072916301348600_bib22",
      "doi-asserted-by": "publisher",
      "first-page": "29",
      "DOI": "10.1016/S0168-9525(98)01637-0",
      "article-title": "Feasting, fasting and fermenting. Glucose sensing in yeast and other cells",
      "volume": "15",
      "author": "Johnston",
      "year": "1999",
      "journal-title": "Trends Genet."
    },
    {
      "key": "2023072916301348600_bib23",
      "doi-asserted-by": "publisher",
      "first-page": "129",
      "DOI": "10.1002/cm.970250203",
      "article-title": "Video microscopy of organelle inheritance and motility in budding yeast",
      "volume": "25",
      "author": "Jones",
      "year": "1993",
      "journal-title": "Cell Motil. Cytoskeleton."
    },
    {
      "key": "2023072916301348600_bib24",
      "first-page": "342",
      "article-title": "Finding groups in data: an introduction to cluster analysis",
      "author": "Kaufman",
      "year": "1990"
    },
    {
      "key": "2023072916301348600_bib25",
      "doi-asserted-by": "crossref",
      "first-page": "283",
      "DOI": "10.4161/cc.7.3.5349",
      "article-title": "Assembling the spindle midzone in the right place at the right time",
      "volume": "7",
      "author": "Khmelinskii",
      "year": "2008",
      "journal-title": "Cell Cycle."
    },
    {
      "key": "2023072916301348600_bib26",
      "doi-asserted-by": "publisher",
      "first-page": "981",
      "DOI": "10.1083/jcb.200702145",
      "article-title": "Cdc14-regulated midzone assembly controls anaphase B",
      "volume": "177",
      "author": "Khmelinskii",
      "year": "2007",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072916301348600_bib27",
      "doi-asserted-by": "publisher",
      "first-page": "922",
      "DOI": "10.1083/jcb.98.3.922",
      "article-title": "Structural rearrangements of tubulin and actin during the cell cycle of the yeast Saccharomyces",
      "volume": "98",
      "author": "Kilmartin",
      "year": "1984",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072916301348600_bib28",
      "doi-asserted-by": "publisher",
      "first-page": "1036",
      "DOI": "10.1038/nature03159",
      "article-title": "An endoribonuclease-prepared siRNA screen in human cells identifies genes essential for cell division",
      "volume": "432",
      "author": "Kittler",
      "year": "2004",
      "journal-title": "Nature."
    },
    {
      "key": "2023072916301348600_bib29",
      "doi-asserted-by": "crossref",
      "first-page": "2570",
      "DOI": "10.4161/cc.8.16.9267",
      "article-title": "The COMA complex is required for Sli15/INCENP-mediated correction of defective kinetochore attachments",
      "volume": "8",
      "author": "Knockleby",
      "year": "2009",
      "journal-title": "Cell Cycle."
    },
    {
      "key": "2023072916301348600_bib30",
      "doi-asserted-by": "crossref",
      "first-page": "2100",
      "DOI": "10.1128/MCB.18.4.2100",
      "article-title": "DBF2 protein kinase binds to and acts through the cell cycle-regulated MOB1 protein",
      "volume": "18",
      "author": "Komarnitsky",
      "year": "1998",
      "journal-title": "Mol. Cell. Biol."
    },
    {
      "key": "2023072916301348600_bib31",
      "doi-asserted-by": "publisher",
      "first-page": "947",
      "DOI": "10.1083/jcb.144.5.947",
      "article-title": "Control of mitotic spindle position by the Saccharomyces cerevisiae formin Bni1p",
      "volume": "144",
      "author": "Lee",
      "year": "1999",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "2023072916301348600_bib32",
      "doi-asserted-by": "publisher",
      "first-page": "124",
      "DOI": "10.1016/j.molcel.2008.12.025",
      "article-title": "Global map of SUMO function revealed by protein-protein interaction and genetic networks",
      "volume": "33",
      "author": "Makhnevych",
      "year": "2009",
      "journal-title": "Mol. Cell."
    },
    {
      "key": "2023072916301348600_bib33",
      "doi-asserted-by": "publisher",
      "first-page": "711",
      "DOI": "10.1016/S1534-5807(03)00130-8",
      "article-title": "The Cdc14 phosphatase and the FEAR network control meiotic spindle disassembly and chromosome segregation",
      "volume": "4",
      "author": "Marston",
      "year": "2003",
      "journal-title": "Dev. Cell."
    },
    {
      "key": "2023072916301348600_bib34",
      "doi-asserted-by": "publisher",
      "first-page": "591",
      "DOI": "10.1146/annurev.cellbio.16.1.591",
      "article-title": "SUMO\u2014nonclassical ubiquitin",
      "volume": "16",
      "author": "Melchior",
      "year": "2000",
      "journal-title": "Annu. Rev. Cell Dev. Biol."
    },
    {
      "key": "2023072916301348600_bib35",
      "doi-asserted-by": "publisher",
      "first-page": "1213",
      "DOI": "10.1126/science.270.5239.1213",
      "article-title": "Requirement of Saccharomyces cerevisiae Ras for completion of mitosis",
      "volume": "270",
      "author": "Morishita",
      "year": "1995",
      "journal-title": "Science."
    },
    {
      "key": "2023072916301348600_bib36",
      "doi-asserted-by": "publisher",
      "first-page": "202",
      "DOI": "10.1038/35056591",
      "article-title": "SUMO, ubiquitin\u2019s mysterious cousin",
      "volume": "2",
      "author": "M\u00fcller",
      "year": "2001",
      "journal-title": "Nat. Rev. Mol. Cell Biol."
    },
    {
      "key": "2023072916301348600_bib37",
      "doi-asserted-by": "publisher",
      "first-page": "19015",
      "DOI": "10.1073/pnas.0509436102",
      "article-title": "High-dimensional and large-scale phenotyping of yeast mutants",
      "volume": "102",
      "author": "Ohya",
      "year": "2005",
      "journal-title": "Proc. Natl. Acad. Sci. USA."
    },
    {
      "key": "2023072916301348600_bib38",
      "doi-asserted-by": "publisher",
      "first-page": "41346",
      "DOI": "10.1074/jbc.M407950200",
      "article-title": "A proteome-wide approach identifies sumoylated substrate proteins in yeast",
      "volume": "279",
      "author": "Panse",
      "year": "2004",
      "journal-title": "J. Biol. Chem."
    },
    {
      "key": "2023072916301348600_bib39",
      "doi-asserted-by": "publisher",
      "first-page": "2120",
      "DOI": "10.1126/science.1091936",
      "article-title": "Separase regulates INCENP-Aurora B anaphase spindle function through Cdc14",
      "volume": "302",
      "author": "Pereira",
      "year": "2003",
      "journal-title": "Science."
    },
    {
      "key": "2023072916301348600_bib40",
      "doi-asserted-by": "publisher",
      "first-page": "1",
      "DOI": "10.1016/S1097-2765(00)00002-2",
      "article-title": "The Bub2p spindle checkpoint links nuclear migration with mitotic exit",
      "volume": "6",
      "author": "Pereira",
      "year": "2000",
      "journal-title": "Mol. Cell."
    },
    {
      "key": "2023072916301348600_bib41",
      "doi-asserted-by": "publisher",
      "first-page": "6359",
      "DOI": "10.1093/emboj/20.22.6359",
      "article-title": "Modes of spindle pole body inheritance and segregation of the Bfa1p-Bub2p checkpoint protein complex",
      "volume": "20",
      "author": "Pereira",
      "year": "2001",
      "journal-title": "EMBO J."
    },
    {
      "key": "2023072916301348600_bib42",
      "doi-asserted-by": "publisher",
      "first-page": "559",
      "DOI": "10.1146/annurev.cellbio.20.010403.103108",
      "article-title": "Mechanisms of polarized growth and organelle segregation in yeast",
      "volume": "20",
      "author": "Pruyne",
      "year": "2004",
      "journal-title": "Annu. Rev. Cell Dev. Biol."
    },
    {
      "key": "2023072916301348600_bib43",
      "doi-asserted-by": "publisher",
      "first-page": "5436",
      "DOI": "10.1073/pnas.062059999",
      "article-title": "Bfa1 can regulate Tem1 function independently of Bub2 in the mitotic exit network of Saccharomyces cerevisiae",
      "volume": "99",
      "author": "Ro",
      "year": "2002",
      "journal-title": "Proc. Natl. Acad. Sci. USA."
    },
    {
      "key": "2023072916301348600_bib44",
      "doi-asserted-by": "publisher",
      "first-page": "35",
      "DOI": "10.1186/1471-2105-3-35",
      "article-title": "FunSpec: a web-based cluster interpreter for yeast",
      "volume": "3",
      "author": "Robinson",
      "year": "2002",
      "journal-title": "BMC Bioinformatics."
    },
    {
      "key": "2023072916301348600_bib45",
      "doi-asserted-by": "publisher",
      "first-page": "230",
      "DOI": "10.1016/j.cell.2007.10.002",
      "article-title": "The chromosomal passenger complex: one for all and all for one",
      "volume": "131",
      "author": "Ruchaud",
      "year": "2007",
      "journal-title": "Cell."
    },
    {
      "key": "2023072916301348600_bib46",
      "doi-asserted-by": "publisher",
      "first-page": "336",
      "DOI": "10.1038/24550",
      "article-title": "Hsp90 as a capacitor for morphological evolution",
      "volume": "396",
      "author": "Rutherford",
      "year": "1998",
      "journal-title": "Nature."
    },
    {
      "key": "2023072916301348600_bib47",
      "doi-asserted-by": "publisher",
      "first-page": "690",
      "DOI": "10.1038/nrm1200",
      "article-title": "Nuclear and unclear functions of SUMO",
      "volume": "4",
      "author": "Seeler",
      "year": "2003",
      "journal-title": "Nat. Rev. Mol. Cell Biol."
    },
    {
      "key": "2023072916301348600_bib48",
      "doi-asserted-by": "publisher",
      "first-page": "661",
      "DOI": "10.1002/yea.1130",
      "article-title": "Optimized cassettes for fluorescent protein tagging in Saccharomyces cerevisiae",
      "volume": "21",
      "author": "Sheff",
      "year": "2004",
      "journal-title": "Yeast."
    },
    {
      "key": "2023072916301348600_bib49",
      "doi-asserted-by": "publisher",
      "first-page": "319",
      "DOI": "10.1016/j.molcel.2005.12.011",
      "article-title": "Mapping pathways and phenotypes by systematic gene overexpression",
      "volume": "21",
      "author": "Sopko",
      "year": "2006",
      "journal-title": "Mol. Cell."
    },
    {
      "key": "2023072916301348600_bib50",
      "doi-asserted-by": "publisher",
      "first-page": "203",
      "DOI": "10.1146/annurev.genet.38.072902.093051",
      "article-title": "Closing mitosis: the functions of the Cdc14 phosphatase and its regulation",
      "volume": "38",
      "author": "Stegmeier",
      "year": "2004",
      "journal-title": "Annu. Rev. Genet."
    },
    {
      "key": "2023072916301348600_bib51",
      "doi-asserted-by": "publisher",
      "first-page": "207",
      "DOI": "10.1016/S0092-8674(02)00618-9",
      "article-title": "Separase, polo kinase, the kinetochore protein Slk19, and Spo12 function in a network that controls Cdc14 localization during early anaphase",
      "volume": "108",
      "author": "Stegmeier",
      "year": "2002",
      "journal-title": "Cell."
    },
    {
      "key": "2023072916301348600_bib52",
      "doi-asserted-by": "publisher",
      "first-page": "5465",
      "DOI": "10.1091/mbc.E05-04-0337",
      "article-title": "The mitotic exit network Mob1p-Dbf2p kinase complex localizes to the nucleus and regulates passenger protein localization",
      "volume": "16",
      "author": "Stoepel",
      "year": "2005",
      "journal-title": "Mol. Biol. Cell."
    },
    {
      "key": "2023072916301348600_bib53",
      "doi-asserted-by": "publisher",
      "first-page": "249",
      "DOI": "10.1038/ncb940",
      "article-title": "A non-proteolytic function of separase links the onset of anaphase to mitotic exit",
      "volume": "5",
      "author": "Sullivan",
      "year": "2003",
      "journal-title": "Nat. Cell Biol."
    },
    {
      "key": "2023072916301348600_bib54",
      "doi-asserted-by": "publisher",
      "first-page": "771",
      "DOI": "10.1038/ncb0901-771",
      "article-title": "Orchestrating anaphase and mitotic exit: separase cleavage and localization of Slk19",
      "volume": "3",
      "author": "Sullivan",
      "year": "2001",
      "journal-title": "Nat. Cell Biol."
    },
    {
      "key": "2023072916301348600_bib55",
      "doi-asserted-by": "publisher",
      "first-page": "3820",
      "DOI": "10.1091/mbc.E07-03-0201",
      "article-title": "A Bir1p Sli15p kinetochore passenger complex regulates septin organization during anaphase",
      "volume": "18",
      "author": "Thomas",
      "year": "2007",
      "journal-title": "Mol. Biol. Cell."
    },
    {
      "key": "2023072916301348600_bib56",
      "doi-asserted-by": "publisher",
      "first-page": "2364",
      "DOI": "10.1126/science.1065810",
      "article-title": "Systematic genetic analysis with ordered arrays of yeast deletion mutants",
      "volume": "294",
      "author": "Tong",
      "year": "2001",
      "journal-title": "Science."
    },
    {
      "key": "2023072916301348600_bib57",
      "doi-asserted-by": "publisher",
      "first-page": "808",
      "DOI": "10.1126/science.1091317",
      "article-title": "Global mapping of the yeast genetic interaction network",
      "volume": "303",
      "author": "Tong",
      "year": "2004",
      "journal-title": "Science."
    },
    {
      "key": "2023072916301348600_bib58",
      "doi-asserted-by": "crossref",
      "first-page": "1103",
      "DOI": "10.1002/j.1460-2075.1994.tb06359.x",
      "article-title": "The Dbf2 and Dbf20 protein kinases of budding yeast are activated after the metaphase to anaphase cell cycle transition",
      "volume": "13",
      "author": "Toyn",
      "year": "1994",
      "journal-title": "EMBO J."
    },
    {
      "key": "2023072916301348600_bib59",
      "doi-asserted-by": "publisher",
      "first-page": "189",
      "DOI": "10.1002/neu.10314",
      "article-title": "Dynein: An ancient motor protein involved in multiple modes of transport",
      "volume": "58",
      "author": "Vallee",
      "year": "2004",
      "journal-title": "J. Neurobiol."
    },
    {
      "key": "2023072916301348600_bib60",
      "doi-asserted-by": "publisher",
      "first-page": "79",
      "DOI": "10.1101/gad.1601308",
      "article-title": "APC/C-Cdh1-mediated degradation of the Polo kinase Cdc5 promotes the return of Cdc14 into the nucleolus",
      "volume": "22",
      "author": "Visintin",
      "year": "2008",
      "journal-title": "Genes Dev."
    },
    {
      "key": "2023072916301348600_bib61",
      "doi-asserted-by": "publisher",
      "first-page": "1656",
      "DOI": "10.1016/j.febslet.2009.03.068",
      "article-title": "A picture is worth a thousand words: genomics to phenomics in the yeast Saccharomyces cerevisiae",
      "volume": "583",
      "author": "Vizeacoumar",
      "year": "2009",
      "journal-title": "FEBS Lett."
    },
    {
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