DOI: 10.1091/mbc.e02-11-0736. Suppression of Coatomer Mutants by a New Protein Family with COPI and COPII Binding Motifs in<i>Saccharomyces cerevisiae</i>

Suppression of Coatomer Mutants by a New Protein Family with COPI and COPII Binding Motifs inSaccharomyces cerevisiae

10.1091/mbc.e02-11-0736

Crossref journal-article

American Society for Cell Biology (ASCB)

Molecular Biology of the Cell (1076)

Abstract

Protein trafficking is achieved by a bidirectional vesicle flow between the various compartments of the eukaryotic cell. COPII coated vesicles mediate anterograde protein transport from the endoplasmic reticulum to the Golgi apparatus, whereas retrograde Golgi-to-endoplasmic reticulum vesicles use the COPI coat. Inactivation of COPI vesicle formation in conditional sec21 (γ-COP) mutants rapidly blocks transport of certain proteins along the early secretory pathway. We have identified the integral membrane protein Mst27p as a strong suppressor of sec21-3 and ret1-1 mutants. A C-terminal KKXX motif of Mst27p that allows direct binding to the COPI complex is crucial for its suppression ability. Mst27p and its homolog Yar033w (Mst28p) are part of the same complex. Both proteins contain cytoplasmic exposed C termini that have the ability to interact directly with COPI and COPII coat complexes. Site-specific mutations of the COPI binding domain abolished suppression of the sec21 mutants. Our results indicate that overexpression of MST27 provides an increased number of coat binding sites on membranes of the early secretory pathway and thereby promotes vesicle formation. As a consequence, the amount of cargo that can bind COPI might be important for the regulation of the vesicle flow in the early secretory pathway.

Bibliography

Sandmann, T., Herrmann, J. M., Dengjel, J., Schwarz, H., & Spang, A. (2003). Suppression of Coatomer Mutants by a New Protein Family with COPI and COPII Binding Motifs inSaccharomyces cerevisiae. Molecular Biology of the Cell, 14(8), 3097â3113.

Authors 5

Thomas Sandmann (first)
Johannes M. Herrmann (additional)
Jörn Dengjel (additional)
Heinz Schwarz (additional)
Anne Spang (additional)

References 54 Referenced 33

Dates

Type	When
Created	22 years, 3 months ago (May 5, 2003, 8:16 p.m.)
Deposited	4 years, 2 months ago (June 6, 2021, 7:59 p.m.)
Indexed	1 year ago (Aug. 29, 2024, 4:30 p.m.)
Issued	22 years ago (Aug. 1, 2003)
Published	22 years ago (Aug. 1, 2003)
Published Print	22 years ago (Aug. 1, 2003)

Funders 0

None

BibTeX

@article{Sandmann_2003, title={Suppression of Coatomer Mutants by a New Protein Family with COPI and COPII Binding Motifs inSaccharomyces cerevisiae}, volume={14}, ISSN={1939-4586}, url={http://dx.doi.org/10.1091/mbc.e02-11-0736}, DOI={10.1091/mbc.e02-11-0736}, number={8}, journal={Molecular Biology of the Cell}, publisher={American Society for Cell Biology (ASCB)}, author={Sandmann, Thomas and Herrmann, Johannes M. and Dengjel, Jörn and Schwarz, Heinz and Spang, Anne}, year={2003}, month=aug, pages={3097–3113} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2024,
        8,
        29
      ]
    ],
    "date-time": "2024-08-29T20:30:42Z",
    "timestamp": 1724963442476
  },
  "reference-count": 54,
  "publisher": "American Society for Cell Biology (ASCB)",
  "issue": "8",
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        2003,
        8
      ]
    ]
  },
  "abstract": "<jats:p>Protein trafficking is achieved by a bidirectional vesicle flow between the various compartments of the eukaryotic cell. COPII coated vesicles mediate anterograde protein transport from the endoplasmic reticulum to the Golgi apparatus, whereas retrograde Golgi-to-endoplasmic reticulum vesicles use the COPI coat. Inactivation of COPI vesicle formation in conditional sec21 (\u03b3-COP) mutants rapidly blocks transport of certain proteins along the early secretory pathway. We have identified the integral membrane protein Mst27p as a strong suppressor of sec21-3 and ret1-1 mutants. A C-terminal KKXX motif of Mst27p that allows direct binding to the COPI complex is crucial for its suppression ability. Mst27p and its homolog Yar033w (Mst28p) are part of the same complex. Both proteins contain cytoplasmic exposed C termini that have the ability to interact directly with COPI and COPII coat complexes. Site-specific mutations of the COPI binding domain abolished suppression of the sec21 mutants. Our results indicate that overexpression of MST27 provides an increased number of coat binding sites on membranes of the early secretory pathway and thereby promotes vesicle formation. As a consequence, the amount of cargo that can bind COPI might be important for the regulation of the vesicle flow in the early secretory pathway.</jats:p>",
  "DOI": "10.1091/mbc.e02-11-0736",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2003,
        5,
        6
      ]
    ],
    "date-time": "2003-05-06T00:16:26Z",
    "timestamp": 1052180186000
  },
  "page": "3097-3113",
  "source": "Crossref",
  "is-referenced-by-count": 33,
  "title": "Suppression of Coatomer Mutants by a New Protein Family with COPI and COPII Binding Motifs in<i>Saccharomyces cerevisiae</i>",
  "prefix": "10.1091",
  "volume": "14",
  "author": [
    {
      "given": "Thomas",
      "family": "Sandmann",
      "sequence": "first",
      "affiliation": [
        {
          "name": "Friedrich Miescher Laboratorium der Max Planck Gesellschaft, D-72076 T\u00fcbingen, Germany"
        }
      ]
    },
    {
      "given": "Johannes M.",
      "family": "Herrmann",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Institut f\u00fcr Physiologische Chemie, Universit\u00e4t M\u00fcnchen, 81377 M\u00fcnchen, Germany"
        }
      ]
    },
    {
      "given": "J\u00f6rn",
      "family": "Dengjel",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Institut f\u00fcr Immunologie, Universit\u00e4t T\u00fcbingen, D-72076 T\u00fcbingen, Germany"
        }
      ]
    },
    {
      "given": "Heinz",
      "family": "Schwarz",
      "sequence": "additional",
      "affiliation": [
        {
          "name": "Max Planck Institut f\u00fcr Entwicklungsbiologie, D-72076 T\u00fcbingen, Germany"
        }
      ]
    },
    {
      "given": "Anne",
      "family": "Spang",
      "sequence": "additional",
      "affiliation": []
    }
  ],
  "member": "1076",
  "reference": [
    {
      "key": "REF1",
      "doi-asserted-by": "crossref",
      "unstructured": "Aoe, T., Cukierman, E., Lee, A., Cassel, D., Peters, P.J., and Hsu, V.W. (1997). The KDEL receptor, ERD2, regulates intracellular traffic by recruiting a GTPase-activating protein for ARF1.EMBO J.16, 7305\u20137316.",
      "DOI": "10.1093/emboj/16.24.7305"
    },
    {
      "key": "REF2",
      "doi-asserted-by": "crossref",
      "unstructured": "Aridor, M., and Traub, L.M. (2002). Cargo selection in vesicular transport: the making and breaking of a coat.Traffic3, 537\u2013546.",
      "DOI": "10.1034/j.1600-0854.2002.30804.x"
    },
    {
      "key": "REF3",
      "doi-asserted-by": "crossref",
      "unstructured": "Arnott, D., O'Connell, K.L., King, K.L., and Stults, J.T. (1998). An integrated approach to proteome analysis: identification of proteins associated with cardiac hypertrophy.Anal. Biochem.258, 1\u201318.",
      "DOI": "10.1006/abio.1998.2566"
    },
    {
      "key": "REF4",
      "doi-asserted-by": "crossref",
      "unstructured": "Baker, D., Hicke, L., Rexach, M., Schleyer, M., and Schekman, R. (1988). Reconstitution of SEC gene product-dependent intercompartmental protein transport.Cell54, 335\u2013344.",
      "DOI": "10.1016/0092-8674(88)90196-1"
    },
    {
      "key": "REF5",
      "doi-asserted-by": "crossref",
      "unstructured": "Barlowe, C., Orci, L., Yeung, T., Hosobuchi, M., Hamamoto, S., Salama, N., Rexach, M.F., Ravazzola, M., Amherdt, M., and Schekman, R. (1994). COPII: a membrane coat formed by Sec proteins that drive vesicle budding from the endoplasmic reticulum.Cell77, 895\u2013907.",
      "DOI": "10.1016/0092-8674(94)90138-4"
    },
    {
      "key": "REF6",
      "doi-asserted-by": "crossref",
      "unstructured": "Bednarek, S.Y., Orci, L., and Schekman, R. (1996). Traffic COP's and formation of vesicle coats.Trends Cell Biol.6, 468\u2013473.",
      "DOI": "10.1016/0962-8924(96)84943-9"
    },
    {
      "key": "REF7",
      "doi-asserted-by": "crossref",
      "unstructured": "Belden, W.J., and Barlowe, C. (1996). Erv25p, a component of COPII-coated vesicles, forms a complex with Emp24p that is required for efficient endoplasmic reticulum to Golgi transport.J. Biol. Chem.271, 26939\u201326946.",
      "DOI": "10.1074/jbc.271.43.26939"
    },
    {
      "key": "REF8",
      "doi-asserted-by": "crossref",
      "unstructured": "Belden, W.J., and Barlowe, C. (2001). Role of Erv29p in collecting soluble secretory proteins into ER-derived transport vesicles.Science294, 1528\u20131531.",
      "DOI": "10.1126/science.1065224"
    },
    {
      "key": "REF9",
      "doi-asserted-by": "crossref",
      "unstructured": "Carlson, M., and Botstein, D. (1982). Two differentially regulated mRNAs with different 5\u2032 ends encode secreted with intracellular forms of yeast invertase.Cell28, 145\u2013154.",
      "DOI": "10.1016/0092-8674(82)90384-1"
    },
    {
      "key": "REF10",
      "doi-asserted-by": "crossref",
      "unstructured": "Chuang, J.S., and Schekman, R.W. (1996). Differential trafficking and timed localization of two chitin synthase proteins, Chs2p and Chs3p.J. Cell Biol.135, 597\u2013610.",
      "DOI": "10.1083/jcb.135.3.597"
    },
    {
      "key": "REF11",
      "doi-asserted-by": "crossref",
      "unstructured": "Cosson, P., and Letourneur, F. (1994). Coatomer interaction with di-lysine endoplasmic reticulum retention motifs.Science263, 1629\u20131631.",
      "DOI": "10.1126/science.8128252"
    },
    {
      "key": "REF12",
      "doi-asserted-by": "crossref",
      "unstructured": "Cosson, P., and Letourneur, F. (1997). Coatomer (COPI)-coated vesicles: role in intracellular transport and protein sorting.Curr. Opin. Cell Biol.9, 484\u2013487.",
      "DOI": "10.1016/S0955-0674(97)80023-3"
    },
    {
      "key": "REF13",
      "doi-asserted-by": "crossref",
      "unstructured": "Dominguez, M., Dejgaard, K., Fullekrug, J., Dahan, S., Fazel, A., Paccaud, J.P., Thomas, D.Y., Bergeron, J.J., and Nilsson, T. (1998). gp25L/emp24/p24 protein family members of the cis-Golgi network bind both COP I and II coatomer.J. Cell Biol.140, 751\u2013765.",
      "DOI": "10.1083/jcb.140.4.751"
    },
    {
      "key": "REF14",
      "doi-asserted-by": "crossref",
      "unstructured": "Evan, G.I., Lewis, G.K., Ramsay, G., and Bishop, J.M. (1985). Isolation of monoclonal antibodies specific for human c-myc protooncogene product.Mol. Cell. Biol.5, 3610\u20133616.",
      "DOI": "10.1128/MCB.5.12.3610"
    },
    {
      "key": "REF15",
      "doi-asserted-by": "crossref",
      "unstructured": "Feuermann, M., de Montigny, J., Potier, S., and Souciet, J.L. (1997). The characterization of two new clusters of duplicated genes suggests a `Lego' organization of the yeastSaccharomyces cerevisiaechromosomes.Yeast13, 861\u2013869.",
      "DOI": "10.1002/(SICI)1097-0061(199707)13:9<861::AID-YEA125>3.0.CO;2-9"
    },
    {
      "key": "REF16",
      "doi-asserted-by": "crossref",
      "unstructured": "Fiedler, K., and Rothman, J.E. (1997). Sorting determinants in the transmembrane domain of p24 proteins.J. Biol. Chem.272, 24739\u201324742.",
      "DOI": "10.1074/jbc.272.40.24739"
    },
    {
      "key": "REF17",
      "doi-asserted-by": "crossref",
      "unstructured": "Frangioni, J.V., and Neel, B.G. (1993). Solubilization and purification of enzymatically active glutathioneS-transferase (pGEX) fusion proteins.Anal. Biochem.210, 179\u2013187.",
      "DOI": "10.1006/abio.1993.1170"
    },
    {
      "key": "REF18",
      "doi-asserted-by": "crossref",
      "unstructured": "Gaynor, E.C., and Emr, S.D. (1997). COPI-independent anterograde transport: cargo-selective ER to Golgi protein transport in yeast COPI mutants.J. Cell Biol.136, 789\u2013802.",
      "DOI": "10.1083/jcb.136.4.789"
    },
    {
      "key": "REF19",
      "doi-asserted-by": "crossref",
      "unstructured": "Gaynor, E.C., te Heesen, S., Graham, T.R., Aebi, M., and Emr, S.D. (1994). Signal-mediated retrieval of a membrane protein from the Golgi to the ER in yeast.J. Cell Biol.127, 653\u2013665.",
      "DOI": "10.1083/jcb.127.3.653"
    },
    {
      "key": "REF20",
      "doi-asserted-by": "crossref",
      "unstructured": "Goffeau, A.et al. (1996). Life with 6000 genes.Science274, 546, 563\u2013547.",
      "DOI": "10.1126/science.274.5287.546"
    },
    {
      "key": "REF21",
      "doi-asserted-by": "crossref",
      "unstructured": "Hartmann, E., Rapoport, T.A., and Lodish, H.F. (1989). Predicting the orientation of eukaryotic membrane-spanning proteins.Proc. Natl. Acad. Sci. USA86, 5786\u20135790.",
      "DOI": "10.1073/pnas.86.15.5786"
    },
    {
      "key": "REF22",
      "doi-asserted-by": "crossref",
      "unstructured": "Heiman, M.G., and Walter, P. (2000). Prm1p, a pheromone-regulated multispanning membrane protein, facilitates plasma membrane fusion during yeast mating.J. Cell Biol.151, 719\u2013730.",
      "DOI": "10.1083/jcb.151.3.719"
    },
    {
      "key": "REF23",
      "doi-asserted-by": "crossref",
      "unstructured": "Herrmann, J.M., Malkus, P., and Schekman, R. (1999). Out of the ER\u2013outfitters, escorts and guides.Trends Cell Biol.9, 5\u20137.",
      "DOI": "10.1016/S0962-8924(98)01414-7"
    },
    {
      "key": "REF24",
      "doi-asserted-by": "crossref",
      "unstructured": "Hicke, L., and Riezman, H. (1996). Ubiquitination of a yeast plasma membrane receptor signals its ligand-stimulated endocytosis.Cell84, 277\u2013287.",
      "DOI": "10.1016/S0092-8674(00)80982-4"
    },
    {
      "key": "REF25",
      "doi-asserted-by": "publisher",
      "DOI": "10.1091/mbc.5.9.1039"
    },
    {
      "key": "REF26",
      "doi-asserted-by": "crossref",
      "unstructured": "Hohenberg, H., Mannweiler, K., and Muller, M. (1994). High-pressure freezing of cell suspensions in cellulose capillary tubes.J. Microsc.175, 34\u201343.",
      "DOI": "10.1111/j.1365-2818.1994.tb04785.x"
    },
    {
      "key": "REF27",
      "doi-asserted-by": "crossref",
      "unstructured": "Hosobuchi, M., Kreis, T., and Schekman, R. (1992). SEC21 is a gene required for ER to Golgi protein transport that encodes a subunit of a yeast coatomer.Nature360, 603\u2013605.",
      "DOI": "10.1038/360603a0"
    },
    {
      "key": "REF28",
      "doi-asserted-by": "crossref",
      "unstructured": "Kahn, R.A., Clark, J., Rulka, C., Stearns, T., Zhang, C.J., Randazzo, P.A., Terui, T., and Cavenagh, M. (1995). Mutational analysis ofSaccharomyces cerevisiaeARF1.J. Biol. Chem.270, 143\u2013150.",
      "DOI": "10.1074/jbc.270.1.143"
    },
    {
      "key": "REF29",
      "doi-asserted-by": "crossref",
      "unstructured": "Kappeler, F., Klopfenstein, D.R., Foguet, M., Paccaud, J.P., and Hauri, H.P. (1997). The recycling of ERGIC-53 in the early secretory pathway. ERGIC-53 carries a cytosolic endoplasmic reticulum-exit determinant interacting with COPII.J. Biol. Chem.272, 31801\u201331808.",
      "DOI": "10.1074/jbc.272.50.31801"
    },
    {
      "key": "REF30",
      "doi-asserted-by": "crossref",
      "unstructured": "Kuehn, M.J., Herrmann, J.M., and Schekman, R. (1998). COPII-cargo interactions direct protein sorting into ER-derived transport vesicles.Nature391, 187\u2013190.",
      "DOI": "10.1038/34438"
    },
    {
      "key": "REF31",
      "doi-asserted-by": "crossref",
      "unstructured": "Kumar, A.et al. (2002). Subcellular localization of the yeast proteome.Genes Dev.16, 707\u2013719.",
      "DOI": "10.1101/gad.970902"
    },
    {
      "key": "REF32",
      "doi-asserted-by": "crossref",
      "unstructured": "Kuthan, M., Devaux, F., Janderova, B., Slaninova, I., Jacq, C., and Palkova, Z. (2003). Domestication of wildSaccharomyces cerevisiaeis accompanied by changes in gene expression and colony morphology.Mol. Microbiol.47, 745\u2013754.",
      "DOI": "10.1046/j.1365-2958.2003.03332.x"
    },
    {
      "key": "REF33",
      "doi-asserted-by": "crossref",
      "unstructured": "Lafontaine, D., and Tollervey, D. (1996). One-step PCR mediated strategy for the construction of conditionally expressed and epitope tagged yeast proteins.Nucleic Acids Res.24, 3469\u20133471.",
      "DOI": "10.1093/nar/24.17.3469"
    },
    {
      "key": "REF34",
      "doi-asserted-by": "crossref",
      "unstructured": "Lupas, A., Van Dyke, M., and Stock, J. (1991). Predicting coiled coils from protein sequences.Science252, 1162\u20131164.",
      "DOI": "10.1126/science.252.5009.1162"
    },
    {
      "key": "REF35",
      "doi-asserted-by": "publisher",
      "DOI": "10.1091/mbc.10.6.1923"
    },
    {
      "key": "REF36",
      "doi-asserted-by": "crossref",
      "unstructured": "Muniz, M., Nuoffer, C., Hauri, H.P., and Riezman, H. (2000). The Emp24 complex recruits a specific cargo molecule into endoplasmic reticulum-derived vesicles.J. Cell Biol.148, 925\u2013930.",
      "DOI": "10.1083/jcb.148.5.925"
    },
    {
      "key": "REF37",
      "doi-asserted-by": "crossref",
      "unstructured": "Muniz, M., and Riezman, H. (2000). Intracellular transport of GPI-anchored proteins.EMBO J.19, 10\u201315.",
      "DOI": "10.1093/emboj/19.1.10"
    },
    {
      "key": "REF38",
      "doi-asserted-by": "crossref",
      "unstructured": "Orci, L., Glick, B.S., and Rothman, J.E. (1986). A new type of coated vesicular carrier that appears not to contain clathrin: its possible role in protein transport within the Golgi stack.Cell46, 171\u2013184.",
      "DOI": "10.1016/0092-8674(86)90734-8"
    },
    {
      "key": "REF39",
      "doi-asserted-by": "crossref",
      "unstructured": "Perkins, D.N., Pappin, D.J., Creasy, D.M., and Cottrell, J.S. (1999). Probability-based protein identification by searching sequence databases using mass spectrometry data.Electrophoresis20, 3551\u20133567.",
      "DOI": "10.1002/(SICI)1522-2683(19991201)20:18<3551::AID-ELPS3551>3.0.CO;2-2"
    },
    {
      "key": "REF40",
      "doi-asserted-by": "crossref",
      "unstructured": "Rein, U., Andag, U., Duden, R., Schmitt, H.D., and Spang, A. (2002). ARF-GAP-mediated interaction between the ER-Golgi v-SNAREs and the COPI coat.J. Cell Biol.157, 395\u2013404.",
      "DOI": "10.1083/jcb.200112092"
    },
    {
      "key": "REF41",
      "doi-asserted-by": "crossref",
      "unstructured": "Reinhard, C., Harter, C., Bremser, M., Brugger, B., Sohn, K., Helms, J.B., and Wieland, F. (1999). Receptor-induced polymerization of coatomer.Proc. Natl. Acad. Sci. USA96, 1224\u20131228.",
      "DOI": "10.1073/pnas.96.4.1224"
    },
    {
      "key": "REF42",
      "doi-asserted-by": "crossref",
      "unstructured": "Rexach, M.F., Latterich, M., and Schekman, R.W. (1994). Characteristics of endoplasmic reticulum-derived transport vesicles.J. Cell Biol.126, 1133\u20131148.",
      "DOI": "10.1083/jcb.126.5.1133"
    },
    {
      "key": "REF43",
      "doi-asserted-by": "crossref",
      "unstructured": "Serafini, T., Orci, L., Amherdt, M., Brunner, M., Kahn, R.A., and Rothman, J.E. (1991). ADP-ribosylation factor is a subunit of the coat of Golgi-derived COP-coated vesicles: a novel role for a GTP-binding protein.Cell67, 239\u2013253.",
      "DOI": "10.1016/0092-8674(91)90176-Y"
    },
    {
      "key": "REF44",
      "doi-asserted-by": "crossref",
      "unstructured": "Sharrocks, A.D. (1994). A T7 expression vector for producing N- and C-terminal fusion proteins with glutathioneS-transferase.Gene138, 105\u2013108.",
      "DOI": "10.1016/0378-1119(94)90789-7"
    },
    {
      "key": "REF45",
      "doi-asserted-by": "crossref",
      "unstructured": "Sherman, F. (1991). Getting started with yeast.Methods Enzymol.194, 3\u201321.",
      "DOI": "10.1016/0076-6879(91)94004-V"
    },
    {
      "key": "REF46",
      "doi-asserted-by": "crossref",
      "unstructured": "Shevchenko, A., Wilm, M., Vorm, O., and Mann, M. (1996). Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels.Anal. Chem.68, 850\u2013858.",
      "DOI": "10.1021/ac950914h"
    },
    {
      "key": "REF47",
      "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": "REF48",
      "doi-asserted-by": "crossref",
      "unstructured": "Sonnhammer, E.L., Eddy, S.R., Birney, E., Bateman, A., and Durbin, R. (1998). Pfam: multiple sequence alignments and HMM-profiles of protein domains.Nucleic Acids Res.26, 320\u2013322.",
      "DOI": "10.1093/nar/26.1.320"
    },
    {
      "key": "REF49",
      "doi-asserted-by": "crossref",
      "unstructured": "Spang, A. (2002). ARF1 regulatory factors and COPI vesicle formation.Curr. Opin. Cell Biol.14, 423.",
      "DOI": "10.1016/S0955-0674(02)00346-0"
    },
    {
      "key": "REF50",
      "doi-asserted-by": "publisher",
      "DOI": "10.1091/mbc.12.4.1035"
    },
    {
      "key": "REF51",
      "doi-asserted-by": "crossref",
      "unstructured": "Spang, A., and Schekman, R. (1998). Reconstitution of retrograde transport from the Golgi to the ER in vitro.J. Cell Biol.143, 589\u2013599.",
      "DOI": "10.1083/jcb.143.3.589"
    },
    {
      "key": "REF52",
      "doi-asserted-by": "crossref",
      "unstructured": "te Heesen, S., Janetzky, B., Lehle, L., and Aebi, M. (1992). The yeast WBP1 is essential for oligosaccharyl transferase activity in vivo and in vitro.EMBO J.11, 2071\u20132075.",
      "DOI": "10.1002/j.1460-2075.1992.tb05265.x"
    },
    {
      "key": "REF53",
      "doi-asserted-by": "publisher",
      "DOI": "10.1091/mbc.9.9.2667"
    },
    {
      "key": "REF54",
      "doi-asserted-by": "crossref",
      "unstructured": "Yeung, T., Barlowe, C., and Schekman, R. (1995). Uncoupled packaging of targeting and cargo molecules during transport vesicle budding from the endoplasmic reticulum.J. Biol. Chem.270, 30567\u201330570.",
      "DOI": "10.1074/jbc.270.51.30567"
    }
  ],
  "container-title": "Molecular Biology of the Cell",
  "original-title": [],
  "language": "en",
  "deposited": {
    "date-parts": [
      [
        2021,
        6,
        6
      ]
    ],
    "date-time": "2021-06-06T23:59:31Z",
    "timestamp": 1623023971000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://www.molbiolcell.org/doi/10.1091/mbc.e02-11-0736"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        2003,
        8
      ]
    ]
  },
  "references-count": 54,
  "journal-issue": {
    "issue": "8",
    "published-print": {
      "date-parts": [
        [
          2003,
          8
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1091/mbc.e02-11-0736"
  ],
  "URL": "http://dx.doi.org/10.1091/mbc.e02-11-0736",
  "relation": {},
  "ISSN": [
    "1059-1524",
    "1939-4586"
  ],
  "subject": [],
  "container-title-short": "MBoC",
  "published": {
    "date-parts": [
      [
        2003,
        8
      ]
    ]
  }
}