DOI: 10.1083/jcb.147.5.981. Cell Cycle–Regulated Attachment of the Ubiquitin-Related Protein Sumo to the Yeast Septins

Cell Cycle–Regulated Attachment of the Ubiquitin-Related Protein Sumo to the Yeast Septins

10.1083/jcb.147.5.981

Crossref journal-article

Rockefeller University Press

The Journal of Cell Biology (291)

Abstract

SUMO is a ubiquitin-related protein that functions as a posttranslational modification on other proteins. SUMO conjugation is essential for viability in Saccharomyces cerevisiae and is required for entry into mitosis. We have found that SUMO is attached to the septins Cdc3, Cdc11, and Shs1/Sep7 specifically during mitosis, with conjugates appearing shortly before anaphase onset and disappearing abruptly at cytokinesis. Septins are components of a belt of 10-nm filaments encircling the yeast bud neck. Intriguingly, only septins on the mother cell side of the bud neck are sumoylated. We have identified four major SUMO attachment-site lysine residues in Cdc3, one in Cdc11, and two in Shs1, all within the consensus sequence (IVL)KX(ED). Mutating these sites eliminated the vast majority of bud neck-associated SUMO, as well as the bulk of total SUMO conjugates in G2/M-arrested cells, indicating that sumoylated septins are the most abundant SUMO conjugates at this point in the cell cycle. This mutant has a striking defect in disassembly of septin rings, resulting in accumulation of septin rings marking previous division sites. Thus, SUMO conjugation plays a role in regulating septin ring dynamics during the cell cycle.

Bibliography

Johnson, E. S., & Blobel, G. (1999). Cell CycleâRegulated Attachment of the Ubiquitin-Related Protein Sumo to the Yeast Septins. The Journal of Cell Biology, 147(5), 981â994.

Authors 2

Erica S. Johnson (first)
Günter Blobel (additional)

References 56 Referenced 324

{'key': '2023072901050816100_Ausubeletal1994', 'volume-title': 'Current Protocols in Molecular Biology', 'author': 'Ausubel', 'year': '1994'} / Current Protocols in Molecular Biology by Ausubel (1994)
10.1101/gad.13.2.176 / Genes Dev / Nim1-related kinases coordinate cell cycle progression with the organization of the peripheral cytoskeleton in yeast by Barral (1999)
10.1083/jcb.142.5.1301 / J. Cell Biol / Involvement of an actomyosin contractile ring in Saccharomyces cerevisiae cytokinesis by Bi (1998)
10.1007/BF00330984 / Mol. Gen. Genet / A positive selection for mutants lacking orotidine-5′-phosphate decarboxylase activity in yeast5-fluoro-orotic acid resistance by Boeke (1984)
10.1083/jcb.143.3.709 / J. Cell Biol / The septins are required for the mitosis-specific activation of the Gin4 kinase by Carroll (1998)
10.1083/jcb.129.3.767 / J. Cell Biol / Role of Bud3p in producing the axial budding pattern of yeast by Chant (1995)
10.1083/jcb.139.1.75 / J. Cell Biol / A septin-based hierarchy of proteins required for localized deposition of chitin in the Saccharomyces cerevisiae cell wall by DeMarini (1997)
10.1016/S0014-5793(97)01305-7 / FEBS Lett / Ubch9 conjugates SUMO but not ubiquitin by Desterro (1997)
10.1016/S1097-2765(00)80133-1 / Mol. Cell / SUMO-1 modification of IκBα inhibits NF-κB activation by Desterro (1998)
10.1074/jbc.270.30.18099 / J. Biol. Chem / An essential yeast gene encoding a homolog of ubiquitin-activating enzyme by Dohmen (1995)
10.1242/jcs.112.3.381 / J. Cell Sci / SUMO-1 modification of the acute promyelocytic leukaemia protein PMLimplications for nuclear localisation by Duprez (1999)
10.1016/S0960-9822(06)00411-8 / Curr. Biol / An IQGAP-related protein controls actin-ring formation and cytokinesis in yeast by Epp (1997)
10.1083/jcb.133.3.605 / J. Cell Biol / A purified Drosophila septin complex forms filaments and exhibits GTPase activity by Field (1996)
{'key': '2023072901050816100_Fieldetal1988', 'first-page': '2159', 'article-title': 'Purification of a RAS-responsive adenylyl cyclase complex from Saccharomyces cerevisiae by use of an epitope addition method', 'volume': '8', 'author': 'Field', 'year': '1988', 'journal-title': 'Mol. Cell. Biol'} / Mol. Cell. Biol / Purification of a RAS-responsive adenylyl cyclase complex from Saccharomyces cerevisiae by use of an epitope addition method by Field (1988)
10.1016/0092-8674(87)90711-2 / Cell / The yeast polyubiquitin gene is essential for resistance to high temperatures, starvation, and other stresses by Finley (1987)
10.1083/jcb.143.3.737 / J. Cell Biol / Polymerization of purified yeast septinsevidence that organized filament arrays may not be required for septin function by Frazier (1998)
10.1006/abio.1996.0012 / Anal. Biochem / Peptide-mass profiles of polyvinylidene difluoride-bound proteins by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry in the presence of nonionic detergents by Gharahdaghi (1996)
10.1091/mbc.8.6.987 / Mol. Biol. Cell / Functional analysis of the interaction between Afr1p and the Cdc12p septin, two proteins involved in pheromone-induced morphogenesis by Giot (1997)
10.1074/jbc.272.45.28198 / J. Biol. Chem / Preferential interaction of sentrin with a ubiquitin-conjugating enzyme, Ubc9 by Gong (1997)
{'key': '2023072901050816100_HarlowandLane1988', 'volume-title': 'AntibodiesA Laboratory Manual', 'author': 'Harlow', 'year': '1988'} / AntibodiesA Laboratory Manual by Harlow (1988)
10.1146/annurev.biochem.67.1.425 / Annu. Rev. Biochem / The ubiquitin system by Hershko (1998)
10.1074/jbc.272.43.26799 / J. Biol. Chem / Ubc9p is the conjugating enzyme for the ubiquitin-like protein Smt3p by Johnson (1997)
10.1002/j.1460-2075.1992.tb05080.x / EMBO (Eur. Mol. Biol. Org.) J / Ubiquitin as a degradation signal by Johnson (1992)
10.1093/emboj/16.18.5509 / EMBO (Eur. Mol. Biol. Org.) J / The ubiquitin-like protein Smt3p is activated for conjugation to other proteins by an Aos1p/Uba2p heterodimer by Johnson (1997)
10.1074/jbc.273.43.28341 / J. Biol. Chem / Interaction of Bnr1p with a novel Src homology 3 domain-containing Hof1p. Implication in cytokinesis in Saccharomyces cerevisiae by Kamei (1998)
10.1074/jbc.273.41.26675 / J. Biol. Chem / Identification of three major sentrinization sites in PML by Kamitani (1998)
10.1074/jbc.273.6.3117 / J. Biol. Chem / Covalent modification of PML by the sentrin family of ubiquitin-like proteins by Kamitani (1998)
10.1083/jcb.112.4.535 / J. Cell Biol / Cellular morphogenesis in the Saccharomyces cerevisiae cell cyclelocalization of the CDC3 gene product and the timing of events at the budding site by Kim (1991)
10.1038/18457 / Nature / A new protease required for cell-cycle progression in yeast by Li (1999)
10.1083/jcb.143.7.1947 / J. Cell Biol / Dual function of Cyk2, a cdc15/PSTPIP family protein, in regulating actomyosin ring dynamics and septin distribution by Lippincott (1998)
10.1083/jcb.140.2.355 / J. Cell Biol / Sequential assembly of myosin II, an IQGAP-like protein, and filamentous actin to a ring structure involved in budding yeast cytokinesis by Lippincott (1998)
10.1016/S0955-0674(96)80054-8 / Curr. Opin. Cell Biol / The septinsroles in cytokinesis and other processes by Longtine (1996)
10.1083/jcb.143.3.719 / J. Cell Biol / Role of the yeast Gin4p protein kinase in septin assembly and the relationship between septin assembly and septin function by Longtine (1998)
10.1016/S0092-8674(00)81862-0 / Cell / A small ubiquitin-related polypeptide involved in targeting RanGAP1 to nuclear pore complex protein RanBP2 by Mahajan (1997)
10.1083/jcb.140.2.259 / J. Cell Biol / Molecular characterization of the SUMO-1 modification of RanGAP1 and its role in nuclear envelope association by Mahajan (1998)
10.1083/jcb.135.6.1457 / J. Cell Biol / A novel ubiquitin-like modification modulates the partitioning of the Ran-GTPase-activating protein RanGAP1 between the cytosol and the nuclear pore complex by Matunis (1996)
10.1083/jcb.140.3.499 / J. Cell Biol / SUMO-1 modification and its role in targeting the Ran GTPase-activating protein, RanGAP1, to the nuclear pore complex by Matunis (1998)
10.1091/mbc.6.7.793 / Mol. Biol. Cell / Evidence that the MIF2 gene of Saccharomyces cerevisiae encodes a centromere protein with homology to the mammalian centromere protein CENP-C by Meluh (1995)
10.1006/bbrc.1998.9541 / Biochem. Biophys. Res. Commun / Shs1pa novel member of septin that interacts with spa2p, involved in polarized growth in Saccharomyces cerevisiae by Mino (1998)
10.1093/emboj/17.1.61 / EMBO (Eur. Mol. Biol. Org.) J / Conjugation with the ubiquitin-related modifier SUMO-1 regulates the partitioning of PML within the nucleus by Müller (1998)
10.1006/bbrc.1998.9995 / Biochem. Biophys. Res. Commun / In vitro SUMO-1 modification requires two enzymatic steps, E1 and E2 by Okuma (1999)
10.4049/jimmunol.157.10.4277 / J. Immunol / Protection against Fas/APO-1- and tumor necrosis factor-mediated cell death by a novel protein, sentrin by Okura (1996)
10.1016/0076-6879(91)94055-H / Guide to Yeast Genetics and Molecular Biology. Vol. 194 / Staining of bud scars and other cell wall chitin with calcofluor by Pringle (1991)
10.1016/0076-6879(91)94043-C / Guide to Yeast Genetics and Molecular Biology. Vol. 194 / Immunofluorescence methods for yeast by Pringle (1991)
10.1083/jcb.143.4.887 / J. Cell Biol / Nuclear import and the evolution of a multifunctional RNA-binding protein by Rosenblum (1998)
10.1016/S0960-9822(98)70044-2 / Curr. Biol / Ubc9p and the conjugation of SUMO-1 to RanGAP1 and RanBP2 by Saitoh (1998)
10.1083/jcb.134.2.413 / J. Cell Biol / The BUD4 protein of yeast, required for axial budding, is localized to the mother/BUD neck in a cell cycle-dependent manner by Sanders (1996)
10.1073/pnas.95.2.560 / Proc. Natl. Acad. Sci. USA / The ubiquitin-like proteins SMT3 and SUMO-1 are conjugated by the UBC9 E2 enzyme by Schwarz (1998)
10.1038/373078a0 / Nature / Role of a ubiquitin-conjugating enzyme in degradation of S- and M-phase cyclins by Seufert (1995)
10.1006/geno.1996.0540 / Genomics / Associations of UBE2I with RAD52, UBL1, p53, and RAD51 proteins in a yeast two-hybrid system by Shen (1996)
{'key': '2023072901050816100_Shermanetal1986', 'volume-title': 'Methods in Yeast Genetics', 'author': 'Sherman', 'year': '1986'} / Methods in Yeast Genetics by Sherman (1986)
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)
10.1074/jbc.274.18.12555 / J. Biol Chem / The nuclear dot protein sp100, characterization of domains necessary for dimerization, subcellular localization, and modification by small ubiquitin-like modifiers by Sternsdorf (1999)
10.1083/jcb.139.7.1621 / J. Cell Biol / Evidence for covalent modification of the nuclear dot-associated proteins PML and sp100 by PIC1/SUMO-1 by Sternsdorf (1997)
10.1006/bbrc.1999.0821 / Biochem. Biophys. Res. Commun / Smt3, a SUMO-1 homolog, is conjugated to Cdc3, a component of septin rings at the mother-bud neck in budding yeast by Takahashi (1999)
10.1073/pnas.81.15.4819 / Proc. Natl. Acad. Sci. USA / Two nuclear mutations that block mitochondrial protein import in yeast by Yaffe (1984)

Dates

Type	When
Created	23 years, 1 month ago (July 26, 2002, 12:45 p.m.)
Deposited	2 years ago (July 28, 2023, 9:06 p.m.)
Indexed	3 weeks, 4 days ago (Aug. 2, 2025, 1:04 a.m.)
Issued	25 years, 8 months ago (Nov. 29, 1999)
Published	25 years, 8 months ago (Nov. 29, 1999)
Published Online	25 years, 8 months ago (Nov. 29, 1999)
Published Print	25 years, 8 months ago (Nov. 29, 1999)

Funders 0

None

BibTeX

@article{Johnson_1999, title={Cell Cycle–Regulated Attachment of the Ubiquitin-Related Protein Sumo to the Yeast Septins}, volume={147}, ISSN={1540-8140}, url={http://dx.doi.org/10.1083/jcb.147.5.981}, DOI={10.1083/jcb.147.5.981}, number={5}, journal={The Journal of Cell Biology}, publisher={Rockefeller University Press}, author={Johnson, Erica S. and Blobel, Günter}, year={1999}, month=nov, pages={981–994} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        8,
        2
      ]
    ],
    "date-time": "2025-08-02T05:04:40Z",
    "timestamp": 1754111080587
  },
  "reference-count": 56,
  "publisher": "Rockefeller University Press",
  "issue": "5",
  "content-domain": {
    "domain": [
      "rupress.org"
    ],
    "crossmark-restriction": true
  },
  "published-print": {
    "date-parts": [
      [
        1999,
        11,
        29
      ]
    ]
  },
  "abstract": "<jats:p>SUMO is a ubiquitin-related protein that functions as a posttranslational modification on other proteins. SUMO conjugation is essential for viability in Saccharomyces cerevisiae and is required for entry into mitosis. We have found that SUMO is attached to the septins Cdc3, Cdc11, and Shs1/Sep7 specifically during mitosis, with conjugates appearing shortly before anaphase onset and disappearing abruptly at cytokinesis. Septins are components of a belt of 10-nm filaments encircling the yeast bud neck. Intriguingly, only septins on the mother cell side of the bud neck are sumoylated. We have identified four major SUMO attachment-site lysine residues in Cdc3, one in Cdc11, and two in Shs1, all within the consensus sequence (IVL)KX(ED). Mutating these sites eliminated the vast majority of bud neck-associated SUMO, as well as the bulk of total SUMO conjugates in G2/M-arrested cells, indicating that sumoylated septins are the most abundant SUMO conjugates at this point in the cell cycle. This mutant has a striking defect in disassembly of septin rings, resulting in accumulation of septin rings marking previous division sites. Thus, SUMO conjugation plays a role in regulating septin ring dynamics during the cell cycle.</jats:p>",
  "DOI": "10.1083/jcb.147.5.981",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2002,
        7,
        26
      ]
    ],
    "date-time": "2002-07-26T16:45:41Z",
    "timestamp": 1027701941000
  },
  "page": "981-994",
  "update-policy": "http://dx.doi.org/10.1083/jcb.crossmarkpolicy",
  "source": "Crossref",
  "is-referenced-by-count": 324,
  "title": "Cell Cycle\u2013Regulated Attachment of the Ubiquitin-Related Protein Sumo to the Yeast Septins",
  "prefix": "10.1083",
  "volume": "147",
  "author": [
    {
      "given": "Erica S.",
      "family": "Johnson",
      "sequence": "first",
      "affiliation": [
        {
          "name": "aLaboratory of Cell Biology, Howard Hughes Medical Institute, Rockefeller University, New York, New York 10021"
        }
      ]
    },
    {
      "given": "G\u00fcnter",
      "family": "Blobel",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "aLaboratory of Cell Biology, Howard Hughes Medical Institute, Rockefeller University, New York, New York 10021"
        }
      ]
    }
  ],
  "member": "291",
  "published-online": {
    "date-parts": [
      [
        1999,
        11,
        29
      ]
    ]
  },
  "reference": [
    {
      "key": "2023072901050816100_Ausubeletal1994",
      "volume-title": "Current Protocols in Molecular Biology",
      "author": "Ausubel",
      "year": "1994"
    },
    {
      "key": "2023072901050816100_Barraletal1999",
      "doi-asserted-by": "crossref",
      "first-page": "176",
      "DOI": "10.1101/gad.13.2.176",
      "article-title": "Nim1-related kinases coordinate cell cycle progression with the organization of the peripheral cytoskeleton in yeast",
      "volume": "13",
      "author": "Barral",
      "year": "1999",
      "journal-title": "Genes Dev"
    },
    {
      "key": "2023072901050816100_Bietal1998",
      "doi-asserted-by": "crossref",
      "first-page": "1301",
      "DOI": "10.1083/jcb.142.5.1301",
      "article-title": "Involvement of an actomyosin contractile ring in Saccharomyces cerevisiae cytokinesis",
      "volume": "142",
      "author": "Bi",
      "year": "1998",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2023072901050816100_Boekeetal1984",
      "doi-asserted-by": "crossref",
      "first-page": "345",
      "DOI": "10.1007/BF00330984",
      "article-title": "A positive selection for mutants lacking orotidine-5\u2032-phosphate decarboxylase activity in yeast5-fluoro-orotic acid resistance",
      "volume": "197",
      "author": "Boeke",
      "year": "1984",
      "journal-title": "Mol. Gen. Genet"
    },
    {
      "key": "2023072901050816100_Carrolletal1998",
      "doi-asserted-by": "crossref",
      "first-page": "709",
      "DOI": "10.1083/jcb.143.3.709",
      "article-title": "The septins are required for the mitosis-specific activation of the Gin4 kinase",
      "volume": "143",
      "author": "Carroll",
      "year": "1998",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2023072901050816100_Chantetal1995",
      "doi-asserted-by": "crossref",
      "first-page": "767",
      "DOI": "10.1083/jcb.129.3.767",
      "article-title": "Role of Bud3p in producing the axial budding pattern of yeast",
      "volume": "129",
      "author": "Chant",
      "year": "1995",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2023072901050816100_DeMarinietal1997",
      "doi-asserted-by": "crossref",
      "first-page": "75",
      "DOI": "10.1083/jcb.139.1.75",
      "article-title": "A septin-based hierarchy of proteins required for localized deposition of chitin in the Saccharomyces cerevisiae cell wall",
      "volume": "139",
      "author": "DeMarini",
      "year": "1997",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2023072901050816100_Desterroetal1997",
      "doi-asserted-by": "crossref",
      "first-page": "297",
      "DOI": "10.1016/S0014-5793(97)01305-7",
      "article-title": "Ubch9 conjugates SUMO but not ubiquitin",
      "volume": "417",
      "author": "Desterro",
      "year": "1997",
      "journal-title": "FEBS Lett"
    },
    {
      "key": "2023072901050816100_Desterroetal1998",
      "doi-asserted-by": "crossref",
      "first-page": "233",
      "DOI": "10.1016/S1097-2765(00)80133-1",
      "article-title": "SUMO-1 modification of I\u03baB\u03b1 inhibits NF-\u03baB activation",
      "volume": "2",
      "author": "Desterro",
      "year": "1998",
      "journal-title": "Mol. Cell"
    },
    {
      "key": "2023072901050816100_Dohmenetal1995",
      "doi-asserted-by": "crossref",
      "first-page": "18099",
      "DOI": "10.1074/jbc.270.30.18099",
      "article-title": "An essential yeast gene encoding a homolog of ubiquitin-activating enzyme",
      "volume": "270",
      "author": "Dohmen",
      "year": "1995",
      "journal-title": "J. Biol. Chem"
    },
    {
      "key": "2023072901050816100_Duprezetal1999",
      "doi-asserted-by": "crossref",
      "first-page": "381",
      "DOI": "10.1242/jcs.112.3.381",
      "article-title": "SUMO-1 modification of the acute promyelocytic leukaemia protein PMLimplications for nuclear localisation",
      "volume": "112",
      "author": "Duprez",
      "year": "1999",
      "journal-title": "J. Cell Sci"
    },
    {
      "key": "2023072901050816100_EppandChant1997",
      "doi-asserted-by": "crossref",
      "first-page": "921",
      "DOI": "10.1016/S0960-9822(06)00411-8",
      "article-title": "An IQGAP-related protein controls actin-ring formation and cytokinesis in yeast",
      "volume": "7",
      "author": "Epp",
      "year": "1997",
      "journal-title": "Curr. Biol"
    },
    {
      "key": "2023072901050816100_Fieldetal1996",
      "doi-asserted-by": "crossref",
      "first-page": "605",
      "DOI": "10.1083/jcb.133.3.605",
      "article-title": "A purified Drosophila septin complex forms filaments and exhibits GTPase activity",
      "volume": "133",
      "author": "Field",
      "year": "1996",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2023072901050816100_Fieldetal1988",
      "first-page": "2159",
      "article-title": "Purification of a RAS-responsive adenylyl cyclase complex from Saccharomyces cerevisiae by use of an epitope addition method",
      "volume": "8",
      "author": "Field",
      "year": "1988",
      "journal-title": "Mol. Cell. Biol"
    },
    {
      "key": "2023072901050816100_Finleyetal1987",
      "doi-asserted-by": "crossref",
      "first-page": "1035",
      "DOI": "10.1016/0092-8674(87)90711-2",
      "article-title": "The yeast polyubiquitin gene is essential for resistance to high temperatures, starvation, and other stresses",
      "volume": "48",
      "author": "Finley",
      "year": "1987",
      "journal-title": "Cell"
    },
    {
      "key": "2023072901050816100_Frazieretal1998",
      "doi-asserted-by": "crossref",
      "first-page": "737",
      "DOI": "10.1083/jcb.143.3.737",
      "article-title": "Polymerization of purified yeast septinsevidence that organized filament arrays may not be required for septin function",
      "volume": "143",
      "author": "Frazier",
      "year": "1998",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2023072901050816100_Gharahdaghietal1996",
      "doi-asserted-by": "crossref",
      "first-page": "94",
      "DOI": "10.1006/abio.1996.0012",
      "article-title": "Peptide-mass profiles of polyvinylidene difluoride-bound proteins by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry in the presence of nonionic detergents",
      "volume": "233",
      "author": "Gharahdaghi",
      "year": "1996",
      "journal-title": "Anal. Biochem"
    },
    {
      "key": "2023072901050816100_GiotandKonopka1997",
      "doi-asserted-by": "crossref",
      "first-page": "987",
      "DOI": "10.1091/mbc.8.6.987",
      "article-title": "Functional analysis of the interaction between Afr1p and the Cdc12p septin, two proteins involved in pheromone-induced morphogenesis",
      "volume": "8",
      "author": "Giot",
      "year": "1997",
      "journal-title": "Mol. Biol. Cell"
    },
    {
      "key": "2023072901050816100_Gongetal1997",
      "doi-asserted-by": "crossref",
      "first-page": "28198",
      "DOI": "10.1074/jbc.272.45.28198",
      "article-title": "Preferential interaction of sentrin with a ubiquitin-conjugating enzyme, Ubc9",
      "volume": "272",
      "author": "Gong",
      "year": "1997",
      "journal-title": "J. Biol. Chem"
    },
    {
      "key": "2023072901050816100_HarlowandLane1988",
      "volume-title": "AntibodiesA Laboratory Manual",
      "author": "Harlow",
      "year": "1988"
    },
    {
      "key": "2023072901050816100_HershkoandCiechanover1998",
      "doi-asserted-by": "crossref",
      "first-page": "425",
      "DOI": "10.1146/annurev.biochem.67.1.425",
      "article-title": "The ubiquitin system",
      "volume": "67",
      "author": "Hershko",
      "year": "1998",
      "journal-title": "Annu. Rev. Biochem"
    },
    {
      "key": "2023072901050816100_JohnsonandBlobel1997",
      "doi-asserted-by": "crossref",
      "first-page": "26799",
      "DOI": "10.1074/jbc.272.43.26799",
      "article-title": "Ubc9p is the conjugating enzyme for the ubiquitin-like protein Smt3p",
      "volume": "272",
      "author": "Johnson",
      "year": "1997",
      "journal-title": "J. Biol. Chem"
    },
    {
      "key": "2023072901050816100_Johnsonetal1992",
      "doi-asserted-by": "crossref",
      "first-page": "497",
      "DOI": "10.1002/j.1460-2075.1992.tb05080.x",
      "article-title": "Ubiquitin as a degradation signal",
      "volume": "11",
      "author": "Johnson",
      "year": "1992",
      "journal-title": "EMBO (Eur. Mol. Biol. Org.) J"
    },
    {
      "key": "2023072901050816100_Johnsonetal1997",
      "doi-asserted-by": "crossref",
      "first-page": "5509",
      "DOI": "10.1093/emboj/16.18.5509",
      "article-title": "The ubiquitin-like protein Smt3p is activated for conjugation to other proteins by an Aos1p/Uba2p heterodimer",
      "volume": "16",
      "author": "Johnson",
      "year": "1997",
      "journal-title": "EMBO (Eur. Mol. Biol. Org.) J"
    },
    {
      "key": "2023072901050816100_Kameietal1998",
      "doi-asserted-by": "crossref",
      "first-page": "28341",
      "DOI": "10.1074/jbc.273.43.28341",
      "article-title": "Interaction of Bnr1p with a novel Src homology 3 domain-containing Hof1p. Implication in cytokinesis in Saccharomyces cerevisiae",
      "volume": "273",
      "author": "Kamei",
      "year": "1998",
      "journal-title": "J. Biol. Chem"
    },
    {
      "key": "2023072901050816100_Kamitanietal1998a",
      "doi-asserted-by": "crossref",
      "first-page": "26675",
      "DOI": "10.1074/jbc.273.41.26675",
      "article-title": "Identification of three major sentrinization sites in PML",
      "volume": "273",
      "author": "Kamitani",
      "year": "1998",
      "journal-title": "J. Biol. Chem"
    },
    {
      "key": "2023072901050816100_Kamitanietal1998b",
      "doi-asserted-by": "crossref",
      "first-page": "3117",
      "DOI": "10.1074/jbc.273.6.3117",
      "article-title": "Covalent modification of PML by the sentrin family of ubiquitin-like proteins",
      "volume": "273",
      "author": "Kamitani",
      "year": "1998",
      "journal-title": "J. Biol. Chem"
    },
    {
      "key": "2023072901050816100_Kimetal1991",
      "doi-asserted-by": "crossref",
      "first-page": "535",
      "DOI": "10.1083/jcb.112.4.535",
      "article-title": "Cellular morphogenesis in the Saccharomyces cerevisiae cell cyclelocalization of the CDC3 gene product and the timing of events at the budding site",
      "volume": "112",
      "author": "Kim",
      "year": "1991",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2023072901050816100_LiandHochstrasser1999",
      "doi-asserted-by": "crossref",
      "first-page": "246",
      "DOI": "10.1038/18457",
      "article-title": "A new protease required for cell-cycle progression in yeast",
      "volume": "398",
      "author": "Li",
      "year": "1999",
      "journal-title": "Nature"
    },
    {
      "key": "2023072901050816100_LippincottandLi1998a",
      "doi-asserted-by": "crossref",
      "first-page": "1947",
      "DOI": "10.1083/jcb.143.7.1947",
      "article-title": "Dual function of Cyk2, a cdc15/PSTPIP family protein, in regulating actomyosin ring dynamics and septin distribution",
      "volume": "143",
      "author": "Lippincott",
      "year": "1998",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2023072901050816100_LippincottandLi1998b",
      "doi-asserted-by": "crossref",
      "first-page": "355",
      "DOI": "10.1083/jcb.140.2.355",
      "article-title": "Sequential assembly of myosin II, an IQGAP-like protein, and filamentous actin to a ring structure involved in budding yeast cytokinesis",
      "volume": "140",
      "author": "Lippincott",
      "year": "1998",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2023072901050816100_Longtineetal1996",
      "doi-asserted-by": "crossref",
      "first-page": "106",
      "DOI": "10.1016/S0955-0674(96)80054-8",
      "article-title": "The septinsroles in cytokinesis and other processes",
      "volume": "8",
      "author": "Longtine",
      "year": "1996",
      "journal-title": "Curr. Opin. Cell Biol"
    },
    {
      "key": "2023072901050816100_Longtineetal1998",
      "doi-asserted-by": "crossref",
      "first-page": "719",
      "DOI": "10.1083/jcb.143.3.719",
      "article-title": "Role of the yeast Gin4p protein kinase in septin assembly and the relationship between septin assembly and septin function",
      "volume": "143",
      "author": "Longtine",
      "year": "1998",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2023072901050816100_Mahajanetal1997",
      "doi-asserted-by": "crossref",
      "first-page": "97",
      "DOI": "10.1016/S0092-8674(00)81862-0",
      "article-title": "A small ubiquitin-related polypeptide involved in targeting RanGAP1 to nuclear pore complex protein RanBP2",
      "volume": "88",
      "author": "Mahajan",
      "year": "1997",
      "journal-title": "Cell"
    },
    {
      "key": "2023072901050816100_Mahajanetal1998",
      "doi-asserted-by": "crossref",
      "first-page": "259",
      "DOI": "10.1083/jcb.140.2.259",
      "article-title": "Molecular characterization of the SUMO-1 modification of RanGAP1 and its role in nuclear envelope association",
      "volume": "140",
      "author": "Mahajan",
      "year": "1998",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2023072901050816100_Matunisetal1996",
      "doi-asserted-by": "crossref",
      "first-page": "1457",
      "DOI": "10.1083/jcb.135.6.1457",
      "article-title": "A novel ubiquitin-like modification modulates the partitioning of the Ran-GTPase-activating protein RanGAP1 between the cytosol and the nuclear pore complex",
      "volume": "135",
      "author": "Matunis",
      "year": "1996",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2023072901050816100_Matunisetal1998",
      "doi-asserted-by": "crossref",
      "first-page": "499",
      "DOI": "10.1083/jcb.140.3.499",
      "article-title": "SUMO-1 modification and its role in targeting the Ran GTPase-activating protein, RanGAP1, to the nuclear pore complex",
      "volume": "140",
      "author": "Matunis",
      "year": "1998",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2023072901050816100_MeluhandKoshland1995",
      "doi-asserted-by": "crossref",
      "first-page": "793",
      "DOI": "10.1091/mbc.6.7.793",
      "article-title": "Evidence that the MIF2 gene of Saccharomyces cerevisiae encodes a centromere protein with homology to the mammalian centromere protein CENP-C",
      "volume": "6",
      "author": "Meluh",
      "year": "1995",
      "journal-title": "Mol. Biol. Cell"
    },
    {
      "key": "2023072901050816100_Minoetal1998",
      "doi-asserted-by": "crossref",
      "first-page": "732",
      "DOI": "10.1006/bbrc.1998.9541",
      "article-title": "Shs1pa novel member of septin that interacts with spa2p, involved in polarized growth in Saccharomyces cerevisiae",
      "volume": "251",
      "author": "Mino",
      "year": "1998",
      "journal-title": "Biochem. Biophys. Res. Commun"
    },
    {
      "key": "2023072901050816100_N0x2f3cd80N0x324db40",
      "doi-asserted-by": "crossref",
      "first-page": "61",
      "DOI": "10.1093/emboj/17.1.61",
      "article-title": "Conjugation with the ubiquitin-related modifier SUMO-1 regulates the partitioning of PML within the nucleus",
      "volume": "17",
      "author": "M\u00fcller",
      "year": "1998",
      "journal-title": "EMBO (Eur. Mol. Biol. Org.) J"
    },
    {
      "key": "2023072901050816100_Okumaetal1999",
      "doi-asserted-by": "crossref",
      "first-page": "693",
      "DOI": "10.1006/bbrc.1998.9995",
      "article-title": "In vitro SUMO-1 modification requires two enzymatic steps, E1 and E2",
      "volume": "254",
      "author": "Okuma",
      "year": "1999",
      "journal-title": "Biochem. Biophys. Res. Commun"
    },
    {
      "key": "2023072901050816100_Okuraetal1996",
      "doi-asserted-by": "crossref",
      "first-page": "4277",
      "DOI": "10.4049/jimmunol.157.10.4277",
      "article-title": "Protection against Fas/APO-1- and tumor necrosis factor-mediated cell death by a novel protein, sentrin",
      "volume": "157",
      "author": "Okura",
      "year": "1996",
      "journal-title": "J. Immunol"
    },
    {
      "key": "2023072901050816100_Pringle1991",
      "doi-asserted-by": "crossref",
      "first-page": "732",
      "DOI": "10.1016/0076-6879(91)94055-H",
      "article-title": "Staining of bud scars and other cell wall chitin with calcofluor",
      "volume-title": "Guide to Yeast Genetics and Molecular Biology. Vol. 194",
      "author": "Pringle",
      "year": "1991"
    },
    {
      "key": "2023072901050816100_Pringleetal1991",
      "doi-asserted-by": "crossref",
      "first-page": "565",
      "DOI": "10.1016/0076-6879(91)94043-C",
      "article-title": "Immunofluorescence methods for yeast",
      "volume-title": "Guide to Yeast Genetics and Molecular Biology. Vol. 194",
      "author": "Pringle",
      "year": "1991"
    },
    {
      "key": "2023072901050816100_Rosenblumetal1998",
      "doi-asserted-by": "crossref",
      "first-page": "887",
      "DOI": "10.1083/jcb.143.4.887",
      "article-title": "Nuclear import and the evolution of a multifunctional RNA-binding protein",
      "volume": "143",
      "author": "Rosenblum",
      "year": "1998",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2023072901050816100_Saitohetal1998",
      "doi-asserted-by": "crossref",
      "first-page": "121",
      "DOI": "10.1016/S0960-9822(98)70044-2",
      "article-title": "Ubc9p and the conjugation of SUMO-1 to RanGAP1 and RanBP2",
      "volume": "8",
      "author": "Saitoh",
      "year": "1998",
      "journal-title": "Curr. Biol"
    },
    {
      "key": "2023072901050816100_SandersandHerskowitz1996",
      "doi-asserted-by": "crossref",
      "first-page": "413",
      "DOI": "10.1083/jcb.134.2.413",
      "article-title": "The BUD4 protein of yeast, required for axial budding, is localized to the mother/BUD neck in a cell cycle-dependent manner",
      "volume": "134",
      "author": "Sanders",
      "year": "1996",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2023072901050816100_Schwarzetal1998",
      "doi-asserted-by": "crossref",
      "first-page": "560",
      "DOI": "10.1073/pnas.95.2.560",
      "article-title": "The ubiquitin-like proteins SMT3 and SUMO-1 are conjugated by the UBC9 E2 enzyme",
      "volume": "95",
      "author": "Schwarz",
      "year": "1998",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
    {
      "key": "2023072901050816100_Seufertetal1995",
      "doi-asserted-by": "crossref",
      "first-page": "78",
      "DOI": "10.1038/373078a0",
      "article-title": "Role of a ubiquitin-conjugating enzyme in degradation of S- and M-phase cyclins",
      "volume": "373",
      "author": "Seufert",
      "year": "1995",
      "journal-title": "Nature"
    },
    {
      "key": "2023072901050816100_Shenetal1996",
      "doi-asserted-by": "crossref",
      "first-page": "183",
      "DOI": "10.1006/geno.1996.0540",
      "article-title": "Associations of UBE2I with RAD52, UBL1, p53, and RAD51 proteins in a yeast two-hybrid system",
      "volume": "37",
      "author": "Shen",
      "year": "1996",
      "journal-title": "Genomics"
    },
    {
      "key": "2023072901050816100_Shermanetal1986",
      "volume-title": "Methods in Yeast Genetics",
      "author": "Sherman",
      "year": "1986"
    },
    {
      "key": "2023072901050816100_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": "2023072901050816100_Sternsdorfetal1999",
      "doi-asserted-by": "crossref",
      "first-page": "12555",
      "DOI": "10.1074/jbc.274.18.12555",
      "article-title": "The nuclear dot protein sp100, characterization of domains necessary for dimerization, subcellular localization, and modification by small ubiquitin-like modifiers",
      "volume": "274",
      "author": "Sternsdorf",
      "year": "1999",
      "journal-title": "J. Biol Chem"
    },
    {
      "key": "2023072901050816100_Sternsdorfetal1997",
      "doi-asserted-by": "crossref",
      "first-page": "1621",
      "DOI": "10.1083/jcb.139.7.1621",
      "article-title": "Evidence for covalent modification of the nuclear dot-associated proteins PML and sp100 by PIC1/SUMO-1",
      "volume": "139",
      "author": "Sternsdorf",
      "year": "1997",
      "journal-title": "J. Cell Biol"
    },
    {
      "key": "2023072901050816100_Takahashietal1999",
      "doi-asserted-by": "crossref",
      "first-page": "582",
      "DOI": "10.1006/bbrc.1999.0821",
      "article-title": "Smt3, a SUMO-1 homolog, is conjugated to Cdc3, a component of septin rings at the mother-bud neck in budding yeast",
      "volume": "259",
      "author": "Takahashi",
      "year": "1999",
      "journal-title": "Biochem. Biophys. Res. Commun"
    },
    {
      "key": "2023072901050816100_YaffeandSchatz1984",
      "doi-asserted-by": "crossref",
      "first-page": "4819",
      "DOI": "10.1073/pnas.81.15.4819",
      "article-title": "Two nuclear mutations that block mitochondrial protein import in yeast",
      "volume": "81",
      "author": "Yaffe",
      "year": "1984",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    }
  ],
  "container-title": "The Journal of Cell Biology",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://rupress.org/jcb/article-pdf/147/5/981/1852944/9909057.pdf",
      "content-type": "application/pdf",
      "content-version": "vor",
      "intended-application": "syndication"
    },
    {
      "URL": "https://rupress.org/jcb/article-pdf/147/5/981/1852944/9909057.pdf",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2023,
        7,
        29
      ]
    ],
    "date-time": "2023-07-29T01:06:43Z",
    "timestamp": 1690592803000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://rupress.org/jcb/article/147/5/981/44639/Cell-Cycle-Regulated-Attachment-of-the-Ubiquitin"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        1999,
        11,
        29
      ]
    ]
  },
  "references-count": 56,
  "journal-issue": {
    "issue": "5",
    "published-print": {
      "date-parts": [
        [
          1999,
          11,
          29
        ]
      ]
    }
  },
  "URL": "http://dx.doi.org/10.1083/jcb.147.5.981",
  "relation": {},
  "ISSN": [
    "0021-9525",
    "1540-8140"
  ],
  "subject": [],
  "published": {
    "date-parts": [
      [
        1999,
        11,
        29
      ]
    ]
  }
}