DOI: 10.1091/mbc.e03-10-0727. Ubiquitin-mediated Targeting of a Mutant Plasma Membrane ATPase, Pma1-7, to the Endosomal/Vacuolar System in Yeast

Ubiquitin-mediated Targeting of a Mutant Plasma Membrane ATPase, Pma1-7, to the Endosomal/Vacuolar System in Yeast

10.1091/mbc.e03-10-0727

Crossref journal-article

American Society for Cell Biology (ASCB)

Molecular Biology of the Cell (1076)

Abstract

Pma1-7 is a mutant plasma membrane ATPase that is impaired in targeting to the cell surface at 37°C and is delivered instead to the endosomal/vacuolar pathway for degradation. We have proposed that Pma1-7 is a substrate for a Golgibased quality control mechanism. By contrast with wild-type Pma1, Pma1-7 is ubiquitinated. Ubiquitination and endosomal targeting of Pma1-7 is dependent on the Rsp5-Bul1-Bul2 ubiquitin ligase protein complex but not the transmembrane ubiquitin ligase Tul1. Analysis of Pma1-7 ubiquitination in mutants blocked in protein transport at various steps of the secretory pathway suggests that ubiquitination occurs after ER exit but before endosomal entry. In the absence of ubiquitination in rsp5-1 cells, Pma1-7 is delivered to the cell surface and remains stable. Nevertheless, Pma1-7 remains impaired in association with detergent-insoluble glycolipid-enriched complexes in rsp5-1 cells, suggesting that ubiquitination is not the cause of Pma1-7 exclusion from rafts. In vps1 cells in which protein transport into the endosomal pathway is blocked, Pma1-7 is routed to the cell surface. On arrival at the plasma membrane in vps1 cells, Pma1-7 remains stable and its ubiquitination disappears, suggesting deubiquitination activity at the cell surface. We suggest that Pma1-7 sorting and fate are regulated by ubiquitination.

Bibliography

Pizzirusso, M., & Chang, A. (2004). Ubiquitin-mediated Targeting of a Mutant Plasma Membrane ATPase, Pma1-7, to the Endosomal/Vacuolar System in Yeast. Molecular Biology of the Cell, 15(5), 2401â2409.

Authors 2

Maddalena Pizzirusso (first)
Amy Chang (additional)

References 55 Referenced 58

Dates

Type	When
Created	21 years, 5 months ago (March 15, 2004, 8:45 p.m.)
Deposited	4 years, 2 months ago (June 14, 2021, 11:41 p.m.)
Indexed	1 year ago (Aug. 11, 2024, 4:27 a.m.)
Issued	21 years, 3 months ago (May 1, 2004)
Published	21 years, 3 months ago (May 1, 2004)
Published Print	21 years, 3 months ago (May 1, 2004)

Funders 0

None

BibTeX

@article{Pizzirusso_2004, title={Ubiquitin-mediated Targeting of a Mutant Plasma Membrane ATPase, Pma1-7, to the Endosomal/Vacuolar System in Yeast}, volume={15}, ISSN={1939-4586}, url={http://dx.doi.org/10.1091/mbc.e03-10-0727}, DOI={10.1091/mbc.e03-10-0727}, number={5}, journal={Molecular Biology of the Cell}, publisher={American Society for Cell Biology (ASCB)}, author={Pizzirusso, Maddalena and Chang, Amy}, year={2004}, month=may, pages={2401–2409} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2024,
        8,
        11
      ]
    ],
    "date-time": "2024-08-11T08:27:27Z",
    "timestamp": 1723364847459
  },
  "reference-count": 55,
  "publisher": "American Society for Cell Biology (ASCB)",
  "issue": "5",
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        2004,
        5
      ]
    ]
  },
  "abstract": "<jats:p>Pma1-7 is a mutant plasma membrane ATPase that is impaired in targeting to the cell surface at 37\u00b0C and is delivered instead to the endosomal/vacuolar pathway for degradation. We have proposed that Pma1-7 is a substrate for a Golgibased quality control mechanism. By contrast with wild-type Pma1, Pma1-7 is ubiquitinated. Ubiquitination and endosomal targeting of Pma1-7 is dependent on the Rsp5-Bul1-Bul2 ubiquitin ligase protein complex but not the transmembrane ubiquitin ligase Tul1. Analysis of Pma1-7 ubiquitination in mutants blocked in protein transport at various steps of the secretory pathway suggests that ubiquitination occurs after ER exit but before endosomal entry. In the absence of ubiquitination in rsp5-1 cells, Pma1-7 is delivered to the cell surface and remains stable. Nevertheless, Pma1-7 remains impaired in association with detergent-insoluble glycolipid-enriched complexes in rsp5-1 cells, suggesting that ubiquitination is not the cause of Pma1-7 exclusion from rafts. In vps1 cells in which protein transport into the endosomal pathway is blocked, Pma1-7 is routed to the cell surface. On arrival at the plasma membrane in vps1 cells, Pma1-7 remains stable and its ubiquitination disappears, suggesting deubiquitination activity at the cell surface. We suggest that Pma1-7 sorting and fate are regulated by ubiquitination.</jats:p>",
  "DOI": "10.1091/mbc.e03-10-0727",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2004,
        3,
        16
      ]
    ],
    "date-time": "2004-03-16T01:45:19Z",
    "timestamp": 1079401519000
  },
  "page": "2401-2409",
  "source": "Crossref",
  "is-referenced-by-count": 58,
  "title": "Ubiquitin-mediated Targeting of a Mutant Plasma Membrane ATPase, Pma1-7, to the Endosomal/Vacuolar System in Yeast",
  "prefix": "10.1091",
  "volume": "15",
  "author": [
    {
      "given": "Maddalena",
      "family": "Pizzirusso",
      "sequence": "first",
      "affiliation": [
        {
          "name": "Department of Molecular, Cellular, and Developmental Biology, University of Michigan, Ann Arbor, Michigan 48109-1048"
        }
      ]
    },
    {
      "given": "Amy",
      "family": "Chang",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Department of Molecular, Cellular, and Developmental Biology, University of Michigan, Ann Arbor, Michigan 48109-1048"
        }
      ]
    }
  ],
  "member": "1076",
  "reference": [
    {
      "key": "REF1",
      "doi-asserted-by": "crossref",
      "unstructured": "Andoh, T., Hirata, Y., and Kikuchi, A. (2000). Yeast glycogen synthase kinase 3 is involved in protein degradation in cooperation with Bul1, Bul2, and Rsp5.Mol. Cell. Biol.20, 6712\u20136720.",
      "DOI": "10.1128/MCB.20.18.6712-6720.2000"
    },
    {
      "key": "REF2",
      "doi-asserted-by": "crossref",
      "unstructured": "Armstrong, J., Patel, S., and Riddle, P. (1990). Lysosomal sorting mutants of coronavirus E1 protein, a Golgi membrane protein.J. Cell Sci.95, 191\u2013197.",
      "DOI": "10.1242/jcs.95.2.191"
    },
    {
      "key": "REF3",
      "doi-asserted-by": "crossref",
      "unstructured": "Arvan, P., Zhao, X., Ramos-Castaneda, J., and Chang, A. (2002). Secretory pathway quality control in the Golgi, plasmalemmal, and endosomal systems.Traffic3, 771-780.",
      "DOI": "10.1034/j.1600-0854.2002.31102.x"
    },
    {
      "key": "REF4",
      "doi-asserted-by": "crossref",
      "unstructured": "Babst, M., Katzmann, D.J., Estepa-Sabal, E.J., Meerloo, T., and Emr, S.D. (2002). ESCRT-III: an endosome-associated heterooligomeric protein complex required for MVB sorting.Dev. Cell3, 271\u2013282.",
      "DOI": "10.1016/S1534-5807(02)00220-4"
    },
    {
      "key": "REF5",
      "doi-asserted-by": "publisher",
      "DOI": "10.1091/mbc.12.12.4129"
    },
    {
      "key": "REF6",
      "doi-asserted-by": "crossref",
      "unstructured": "Bagnat, M., Keranen, S., Shevchenko, A., and Simons, K. (2000). Lipid rafts function in biosynthetic delivery of proteins to the cell surface in yeast.Proc. Natl. Acad. Sci. USA97, 3254\u20133259.",
      "DOI": "10.1073/pnas.97.7.3254"
    },
    {
      "key": "REF7",
      "doi-asserted-by": "crossref",
      "unstructured": "Beck, T., Schmidt, A., and Hall, M.N. (1999). Starvation induces vacuolar targeting and degradation of the tryptophan permease in yeast.J. Cell Biol.146, 1227\u20131237.",
      "DOI": "10.1083/jcb.146.6.1227"
    },
    {
      "key": "REF8",
      "doi-asserted-by": "crossref",
      "unstructured": "Benito, B., Moreno, E., and Lagunas, R. (1991). Half-life of plasma membrane ATPase and its activating system in resting yeast cells.Biochim. Biophys. Acta1063, 265\u2013268.",
      "DOI": "10.1016/0005-2736(91)90381-H"
    },
    {
      "key": "REF9",
      "doi-asserted-by": "crossref",
      "unstructured": "Bonifacino, J.S., and Weissman, A.M. (1998). Ubiquitin and the control of protein fate in the secretory and endocytic pathways.Annu. Rev. Cell Dev. Biol.14, 19\u201357.",
      "DOI": "10.1146/annurev.cellbio.14.1.19"
    },
    {
      "key": "REF10",
      "doi-asserted-by": "crossref",
      "unstructured": "Chang, A. (2002). Plasma membrane biogenesis.Methods Enzymol.351, 339\u2013350.",
      "DOI": "10.1016/S0076-6879(02)51856-5"
    },
    {
      "key": "REF11",
      "doi-asserted-by": "crossref",
      "unstructured": "Chang, A., and Fink, G.R. (1995). Targeting of the yeast plasma membrane [H+]ATPase: a novel geneAST1prevents mislocalization of mutant ATPase to the vacuole.J. Cell Biol.128, 39\u201349.",
      "DOI": "10.1083/jcb.128.1.39"
    },
    {
      "key": "REF12",
      "doi-asserted-by": "crossref",
      "unstructured": "Chang, A., and Slayman, C.W. (1991). Maturation of the yeast plasma membrane [H+]ATPase involves phosphorylation during intracellular transport.J. Cell Biol.115, 289\u2013295.",
      "DOI": "10.1083/jcb.115.2.289"
    },
    {
      "key": "REF13",
      "doi-asserted-by": "crossref",
      "unstructured": "Cowles, C.R., Emr, S.D., and Horazdovsky, B.F. (1994). Mutations in theVPS45gene, aSEC1homologue, result in vacuolar protein sorting defects and accumulation of membrane vesicles.J. Cell Sci.107, 3449\u20133459.",
      "DOI": "10.1242/jcs.107.12.3449"
    },
    {
      "key": "REF14",
      "doi-asserted-by": "crossref",
      "unstructured": "Cross, F. (1997). `Marker swap' plasmids: convenient tools for budding yeast molecular genetics.Yeast13, 647\u2013653.",
      "DOI": "10.1002/(SICI)1097-0061(19970615)13:7<647::AID-YEA115>3.0.CO;2-#"
    },
    {
      "key": "REF15",
      "doi-asserted-by": "crossref",
      "unstructured": "Ellgard, L., Molinari, M., and Helenius, A. (1999). Setting the standards: quality control in the secretory pathway.Science286, 1882\u20131888.",
      "DOI": "10.1126/science.286.5446.1882"
    },
    {
      "key": "REF16",
      "doi-asserted-by": "crossref",
      "unstructured": "Fisk, H. A., and Yaffe, M. P. (1999). A role for ubiquitination in mitochondrial inheritance inSaccharomyces cerevisiae.J. Cell Biol.145, 1199\u20131208.",
      "DOI": "10.1083/jcb.145.6.1199"
    },
    {
      "key": "REF17",
      "doi-asserted-by": "crossref",
      "unstructured": "Gong, X., and Chang, A. (2001). A mutant plasma membrane ATPase, Pma1\u201310, is defective in stability at the yeast cell surface.Proc. Natl. Acad. Sci. USA98, 9104\u20139109.",
      "DOI": "10.1073/pnas.161282998"
    },
    {
      "key": "REF18",
      "doi-asserted-by": "crossref",
      "unstructured": "Gormley, K., Dong, Y., and Sagnella, G.A. (2003). Regulation of the epithelial sodium channel by accessory proteins.Biochem. J.371, 1\u201314.",
      "DOI": "10.1042/bj20021375"
    },
    {
      "key": "REF19",
      "doi-asserted-by": "crossref",
      "unstructured": "Helliwell, S.B., Losko, S., and Kaiser, C.A. (2001). Components of a ubiquitin ligase complex specify polyubiquitination and intracellular trafficking of the general amino acid permease.J. Cell Biol.153, 649\u2013662.",
      "DOI": "10.1083/jcb.153.4.649"
    },
    {
      "key": "REF20",
      "doi-asserted-by": "crossref",
      "unstructured": "Hicke, L. (1999). Gettin'down with ubiquitin: turning off cell-surface receptors, transporters and channels.Trends Cell Biol.9, 107\u2013112.",
      "DOI": "10.1016/S0962-8924(98)01491-3"
    },
    {
      "key": "REF21",
      "doi-asserted-by": "crossref",
      "unstructured": "Hicke, L. (2001). Protein regulation by monoubiquitin.Nat. Rev. Mol. Cell Biol.2, 195\u2013201.",
      "DOI": "10.1038/35056583"
    },
    {
      "key": "REF22",
      "doi-asserted-by": "crossref",
      "unstructured": "Hinners, I., and Tooze, S.A. (2003). Changing directions: clathrin-mediated transport between the Golgi and endosomes.J. Cell Sci.116, 763\u2013771.",
      "DOI": "10.1242/jcs.00270"
    },
    {
      "key": "REF23",
      "doi-asserted-by": "crossref",
      "unstructured": "Hochstrasser, M. (1996). Ubiquitin dependent protein degradation.Annu. Rev. Genet.30, 405\u2013439.",
      "DOI": "10.1146/annurev.genet.30.1.405"
    },
    {
      "key": "REF24",
      "doi-asserted-by": "crossref",
      "unstructured": "Hong, E., Davidson, A.R., and Kaiser, C.A. (1996). A pathway for targeting soluble misfolded proteins to the yeast vacuole.J. Cell Biol.135, 623\u2013633.",
      "DOI": "10.1083/jcb.135.3.623"
    },
    {
      "key": "REF25",
      "doi-asserted-by": "crossref",
      "unstructured": "Hoppe, T., Matuschewski, K., Rape, M., Schlenker, S., Ulrich, H.D., and Jentsch, S. (2000). Activation of a membrane-bound transcription factor by regulated ubiquitin/proteasome-dependent processing.Cell102, 577\u2013586.",
      "DOI": "10.1016/S0092-8674(00)00080-5"
    },
    {
      "key": "REF26",
      "doi-asserted-by": "crossref",
      "unstructured": "Jenness, D.D., Li, Y., Tipper, C., and Spatrick, P. (1997). Elimination of defective \u03b1-factor pheromone receptors.Mol. Cell Biol.17, 6236\u20136245.",
      "DOI": "10.1128/MCB.17.11.6236"
    },
    {
      "key": "REF27",
      "doi-asserted-by": "crossref",
      "unstructured": "Jones, E.W. (1977). Proteinase mutants ofSaccharomyces cerevisiae.Genetics35, 23\u201333.",
      "DOI": "10.1093/genetics/85.1.23"
    },
    {
      "key": "REF28",
      "doi-asserted-by": "crossref",
      "unstructured": "Katzmann, D.J., Babst, M., and Emr, S.D. (2001). Ubiquitin-dependent sorting into the multivesicular body pathway requires the function of a conserved endosomal protein sorting complex, ESCRT-1.Cell106, 145\u2013155.",
      "DOI": "10.1016/S0092-8674(01)00434-2"
    },
    {
      "key": "REF29",
      "doi-asserted-by": "crossref",
      "unstructured": "Katzmann, D.J., Odorizzi, G., and Emr, S.D. (2002). Receptor downregulation and multivesicular-body sorting.Nat. Rev.3, 893\u2013905.",
      "DOI": "10.1038/nrm973"
    },
    {
      "key": "REF30",
      "doi-asserted-by": "crossref",
      "unstructured": "Kolling, R., and Losko, S. (1997). The linker region of the ABC-transporter Ste6 mediates ubiquitination and fast turnover of the protein.EMBO J.16, 2251\u20132261.",
      "DOI": "10.1093/emboj/16.9.2251"
    },
    {
      "key": "REF31",
      "doi-asserted-by": "crossref",
      "unstructured": "Lee, M.C.S., Hamamoto, S., and Schekman, R. (2002). Ceramide biosynthesis is required for the formation of oligomeric H+-ATPase, Pma1p, in the yeast endoplasmic reticulum.J. Biol. Chem.277, 22395\u201322401.",
      "DOI": "10.1074/jbc.M200450200"
    },
    {
      "key": "REF32",
      "doi-asserted-by": "crossref",
      "unstructured": "Liu, X.F., and Culotta, V.C. (1999). Post-translation control of Nramp metal transport in yeast.J. Biol. Chem.274, 4863\u20134868.",
      "DOI": "10.1074/jbc.274.8.4863"
    },
    {
      "key": "REF33",
      "doi-asserted-by": "publisher",
      "DOI": "10.1091/mbc.11.2.579"
    },
    {
      "key": "REF34",
      "doi-asserted-by": "crossref",
      "unstructured": "Luo, W.J., and Chang, A. (1997). Novel genes involved in endosomal traffic in yeast revealed by suppression of a targeting-defective plasma membrane ATPase mutant.J. Cell Biol.138, 731-746.",
      "DOI": "10.1083/jcb.138.4.731"
    },
    {
      "key": "REF35",
      "doi-asserted-by": "crossref",
      "unstructured": "Magasanik, B., and Kaiser, C.A. (2002). Nitrogen regulation inSaccharomyces cerevisiae.Gene290, 1\u201318.",
      "DOI": "10.1016/S0378-1119(02)00558-9"
    },
    {
      "key": "REF36",
      "doi-asserted-by": "crossref",
      "unstructured": "Minami, Y., Weissman, A.M., Samelson, L.E., and Klausner, R.D. (1987). Building a multichain receptor: synthesis, degradation, and assembly of the T-cell antigen receptor.Proc. Natl. Acad. Sci. USA84, 2688\u20132692.",
      "DOI": "10.1073/pnas.84.9.2688"
    },
    {
      "key": "REF37",
      "doi-asserted-by": "crossref",
      "unstructured": "Mullins, C., and Bonifacino, J.S. (2001). Structural requirements for function of yeast GGAs in vacuolar protein sorting, \u03b1-factor maturation, and interactions with clathrin.Mol. Cell Biol.21, 7981-7994.",
      "DOI": "10.1128/MCB.21.23.7981-7994.2001"
    },
    {
      "key": "REF38",
      "doi-asserted-by": "crossref",
      "unstructured": "Nothwehr, S.F., Conibear, E., and Stevens, T.H. (1995). Golgi and vacuolar membrane proteins reach the vacuole invps1mutant yeast cells via the plasma membrane.J. Cell Biol.129, 35\u201346.",
      "DOI": "10.1083/jcb.129.1.35"
    },
    {
      "key": "REF39",
      "doi-asserted-by": "crossref",
      "unstructured": "Pickart, C.M. (2001). Mechanisms underlying ubiquitination.Annu. Rev. Biochem.70, 503\u201333.",
      "DOI": "10.1146/annurev.biochem.70.1.503"
    },
    {
      "key": "REF40",
      "doi-asserted-by": "crossref",
      "unstructured": "Rape, M., Hoppe, T., Gorr, I., Kalocay, M., Richly, H., and Jentsch, S. (2001). Mobilization of processed, membrane-tethered SPT23 transcription factor by CDC48UFD1/NPL4, a ubiquitin-selective chaperone.Cell107, 667\u2013677.",
      "DOI": "10.1016/S0092-8674(01)00595-5"
    },
    {
      "key": "REF41",
      "doi-asserted-by": "crossref",
      "unstructured": "Reggiori, F., and Pelham, H.R.B. (2002). A transmembrane ubiquitin ligase required to sort membrane proteins into multivesicular bodies.Nat. Cell Biol.4, 117\u2013123.",
      "DOI": "10.1038/ncb743"
    },
    {
      "key": "REF42",
      "doi-asserted-by": "crossref",
      "unstructured": "Roth, A.F., Sullivan, D.M., and Davis, N.G. (1998). A large PEST-like sequence directs the ubiquitination, endocytosis, and vacuolar degradation of the yeast a-factor receptor.J. Cell Biol.142, 949\u2013961.",
      "DOI": "10.1083/jcb.142.4.949"
    },
    {
      "key": "REF43",
      "doi-asserted-by": "crossref",
      "unstructured": "Rothman, J.H., Raymond, C.K., Gilbert, T., O'Hara, P.J., and Stevens, T.H. (1990). A putative GTP binding protein homologous to interferon-inducible Mx proteins performs an essential function in yeast protein sorting.Cell61, 1063\u20131074.",
      "DOI": "10.1016/0092-8674(90)90070-U"
    },
    {
      "key": "REF44",
      "doi-asserted-by": "crossref",
      "unstructured": "Rotin, D., Staub, O., and Haguenauer-Tsapis, R. (2000). Ubiquitination and endocytosis of plasma membrane proteins: role of Nedd4/Rsp5p family of ubiquitin-protein ligases.J. Membr. Biol.176, 1\u201317.",
      "DOI": "10.1007/s00232001079"
    },
    {
      "key": "REF45",
      "unstructured": "Sherman, F., Hicks, J.B., and Fink, G.R. (1986).Methods in Yeast Genetics: A Laboratory Manual, Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press."
    },
    {
      "key": "REF46",
      "doi-asserted-by": "crossref",
      "unstructured": "Shih, S.C., Katzmann, D.J., Schnell, J.D., Sutanto, M., Emr, S.D., and Hicke, L. (2002). Epsins and Vps27p/Hrs contain ubiquitin-binding domains that function in receptor endocytosis.Nat. Cell Biol.4, 389\u2013393.",
      "DOI": "10.1038/ncb790"
    },
    {
      "key": "REF47",
      "doi-asserted-by": "crossref",
      "unstructured": "Shih, S.C., Sloper-Mould, K.E., and Hicke, L. (2000). Monoubiquitin carries a novel internalization signal that is appended to activated receptors.EMBO J.19, 187\u2013198.",
      "DOI": "10.1093/emboj/19.2.187"
    },
    {
      "key": "REF48",
      "doi-asserted-by": "crossref",
      "unstructured": "Sikorski, R.S., and Hieter, P. (1989). A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA inSaccharomyces cerevisiae.Genetics122, 19\u201327.",
      "DOI": "10.1093/genetics/122.1.19"
    },
    {
      "key": "REF49",
      "doi-asserted-by": "crossref",
      "unstructured": "Swerdlow, P.S., Finley, D., and Varshavsky, A. (1986). Enhancement of immunoblot sensitivity by heating of hydrated filters.Anal. Biochem.156, 147\u2013153.",
      "DOI": "10.1016/0003-2697(86)90166-1"
    },
    {
      "key": "REF50",
      "doi-asserted-by": "crossref",
      "unstructured": "Tsai, B., Ye, Y., and Rapoport, T. (2002). Retro-translocation of proteins from the endoplasmic reticulum into the cytosol.Nat. Rev.3, 246\u2013255.",
      "DOI": "10.1038/nrm780"
    },
    {
      "key": "REF51",
      "doi-asserted-by": "crossref",
      "unstructured": "Umebayashi, K., and Nakano, A. (2003). Ergosterol is required for targeting of tryptophan permease to the yeast plasma membrane.J. Cell Biol.161, 1117\u20131131.",
      "DOI": "10.1083/jcb.200303088"
    },
    {
      "key": "REF52",
      "doi-asserted-by": "crossref",
      "unstructured": "Wang, Q., and Chang, A. (2002). Sphingoid base synthesis is required for oligomerization and cell surface stability of the yeast plasma membrane ATPase, Pma1.Proc. Natl. Acad. Sci., USA99, 12853\u201312858.",
      "DOI": "10.1073/pnas.202115499"
    },
    {
      "key": "REF53",
      "doi-asserted-by": "crossref",
      "unstructured": "Wilsbach, K., and Payne, G.S. (1993). Vps1p, a member of the dynamin GTPase family, is necessary for Golgi membrane protein retention inSaccharomyces cerevisiae.EMBO J.12, 3049\u20133059.",
      "DOI": "10.1002/j.1460-2075.1993.tb05974.x"
    },
    {
      "key": "REF54",
      "doi-asserted-by": "crossref",
      "unstructured": "Yashiroda, H., Oguchi, T., Yasuda, Y., Toh-e, A., and Kikuchi, Y. (1996). Bul1, a new protein that binds to the Rps5 ubiquitin ligase inSaccharomyces cerevisiae.Mol. Cell Biol.16, 3255\u20133263.",
      "DOI": "10.1128/MCB.16.7.3255"
    },
    {
      "key": "REF55",
      "doi-asserted-by": "crossref",
      "unstructured": "Zhang, B.Y., Chang, A., Kjeldsen, T.B., and Arvan, P. (2001). Intracellular retention of newly-synthesized insulin in yeast is caused by endoproteolytic processing in the Golgi complex.J. Cell Biol.153, 1187\u20131197.",
      "DOI": "10.1083/jcb.153.6.1187"
    }
  ],
  "container-title": "Molecular Biology of the Cell",
  "original-title": [],
  "language": "en",
  "deposited": {
    "date-parts": [
      [
        2021,
        6,
        15
      ]
    ],
    "date-time": "2021-06-15T03:41:55Z",
    "timestamp": 1623728515000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://www.molbiolcell.org/doi/10.1091/mbc.e03-10-0727"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        2004,
        5
      ]
    ]
  },
  "references-count": 55,
  "journal-issue": {
    "issue": "5",
    "published-print": {
      "date-parts": [
        [
          2004,
          5
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1091/mbc.e03-10-0727"
  ],
  "URL": "http://dx.doi.org/10.1091/mbc.e03-10-0727",
  "relation": {},
  "ISSN": [
    "1059-1524",
    "1939-4586"
  ],
  "subject": [],
  "container-title-short": "MBoC",
  "published": {
    "date-parts": [
      [
        2004,
        5
      ]
    ]
  }
}