DOI: 10.1083/jcb.138.3.531. The Membrane Protein Alkaline Phosphatase Is Delivered to the Vacuole by a Route That Is Distinct from the <i>VPS</i>-dependent Pathway

The Membrane Protein Alkaline Phosphatase Is Delivered to the Vacuole by a Route That Is Distinct from the VPS-dependent Pathway

10.1083/jcb.138.3.531

Crossref journal-article

Rockefeller University Press

The Journal of Cell Biology (291)

Abstract

Membrane trafficking intermediates involved in the transport of proteins between the TGN and the lysosome-like vacuole in the yeast Saccharomyces cerevisiae can be accumulated in various vps mutants. Loss of function of Vps45p, an Sec1p-like protein required for the fusion of Golgi-derived transport vesicles with the prevacuolar/endosomal compartment (PVC), results in an accumulation of post-Golgi transport vesicles. Similarly, loss of VPS27 function results in an accumulation of the PVC since this gene is required for traffic out of this compartment. The vacuolar ATPase subunit Vph1p transits to the vacuole in the Golgi-derived transport vesicles, as defined by mutations in VPS45, and through the PVC, as defined by mutations in VPS27. In this study we demonstrate that, whereas VPS45 and VPS27 are required for the vacuolar delivery of several membrane proteins, the vacuolar membrane protein alkaline phosphatase (ALP) reaches its final destination without the function of these two genes. Using a series of ALP derivatives, we find that the information to specify the entry of ALP into this alternative pathway to the vacuole is contained within its cytosolic tail, in the 13 residues adjacent to the transmembrane domain, and loss of this sorting determinant results in a protein that follows the VPS-dependent pathway to the vacuole. Using a combination of immunofluorescence localization and pulse/chase immunoprecipitation analysis, we demonstrate that, in addition to ALP, the vacuolar syntaxin Vam3p also follows this VPS45/27-independent pathway to the vacuole. In addition, the function of Vam3p is required for membrane traffic along the VPS-independent pathway.

Bibliography

Piper, R. C., Bryant, N. J., & Stevens, T. H. (1997). The Membrane Protein Alkaline Phosphatase Is Delivered to the Vacuole by a Route That Is Distinct from the VPS-dependent Pathway. The Journal of Cell Biology, 138(3), 531â545.

Authors 3

Robert C. Piper (first)
Nia J. Bryant (additional)
Tom H. Stevens (additional)

References 68 Referenced 131

10.1016/0092-8674(92)90462-L / Cell / A family of proteins involved in intracellular transport by Aalto (1992)
10.1073/pnas.83.23.9075 / Proc Natl Acad Sci USA / Isolation of yeast mutants defective in protein targeting to the vacuole by Bankaitis (1986)
{'key': '2023072822544349300_B3', 'first-page': '4638', 'article-title': 'Characterization of yeast Vps33p, a protein required for vacuolar protein sorting and vacuole biogenesis', 'volume': '10', 'author': 'Banta', 'year': '1990', 'journal-title': 'Mol Cell Biol'} / Mol Cell Biol / Characterization of yeast Vps33p, a protein required for vacuolar protein sorting and vacuole biogenesis by Banta (1990)
10.1111/j.1749-6632.1994.tb17273.x / Ann NY Acad Sci / Biogenesis of secretory granules and synaptic vesicles. Facts and hypotheses by Bauerfeind (1994)
10.1091/mbc.7.4.579 / Mol Biol Cell / Novel syntaxin homolog, Pep12p, required for the sorting of lumenal hydrolases to the lysosome-like vacuole in yeast by Becherer (1996)
10.1091/mbc.5.11.1185 / Mol Biol Cell / Metabolic instability and constitutive endocytosis of STE6, the a-factor transporter of Saccharomyces cerevisiae. by Berkower (1994)
10.1007/BF00330984 / Mol Gen Genet / A positive selection for mutants lacking orotidine-5′-phosphate decarboxylase activity in yeast: 5-fluororotic acid resistance by Boeke (1984)
10.1083/jcb.136.2.287 / J Cell Biol / Two separate signals act independently to localize a yeast late Golgi membrane protein through a combination of retrieval and retention by Bryant (1997)
10.1128/MCB.16.5.2369 / Mol Cell Biol / A yeast protein related to a mammalian Ras-binding protein, Vps9p, is required for localization of vacuolar proteins by Burd (1996)
10.1091/mbc.6.9.1089 / Mol Biol Cell / The cytoplasmic tail domain of the vacuolar protein sorting receptor Vps10p and a subset of VPS gene products regulate receptor stability, function, and localization by Cereghino (1995)
10.1016/0092-8674(95)90088-8 / Cell / Vacuolar biogenesis in yeast: sorting out the sorting proteins by Conibear (1995)
10.1083/jcb.133.3.529 / J Cell Biol / Vps10p cycles between the late-Golgi and prevacuolar compartments in its function as the sorting receptor for multiple yeast vacuolar hydrolases by Cooper (1996)
10.1242/jcs.107.12.3449 / J Cell Sci / Mutations in the VPS45 gene, a SEC1homologue, result in vacuolar protein sorting defects and accumulation of membrane vesicles by Cowles (1994)
10.1083/jcb.122.1.53 / J Cell Biol / Cis- and trans-acting functions required for endocytosis of the yeast pheromone receptors by Davis (1993)
10.1016/0959-4388(95)80059-X / Curr Opin Neurobiol / The function of dynamin in endocytosis by De Camilli (1995)
{'key': '2023072822544349300_B16', 'first-page': '2347', 'article-title': 'Invertase beta-galactosidase hybrid proteins fail to be transported from the endoplasmic reticulum in Saccharomyces cerevisiae.', 'volume': '4', 'author': 'Emr', 'year': '1984', 'journal-title': 'Mol Cell Biol'} / Mol Cell Biol / Invertase beta-galactosidase hybrid proteins fail to be transported from the endoplasmic reticulum in Saccharomyces cerevisiae. by Emr (1984)
10.1083/jcb.128.6.1055 / J Cell Biol / The role of Myo2, a yeast class V myosin, in vesicular transport by Govidan (1995)
10.1083/jcb.114.2.207 / J Cell Biol / Compartmental organization of Golgi-specific protein modification and vacuolar protein sorting events defined in a yeast sec18(NSF) mutant by Graham (1991)
10.1002/j.1460-2075.1995.tb00210.x / EMBO (Eur Mol Biol Organ) J / The GTPase Ypt7p of Saccharomyces cerevisiaeis required on both partner vacuoles for the homotypic fusion step of vacuole inheritance by Haas (1995)
10.1083/jcb.132.6.985 / J Cell Biol / Localization of a yeast early Golgi mannosyltransferase, Och1p, involves retrograde transport by Harris (1996)
10.1083/jcb.131.2.297 / J Cell Biol / Parallel secretory pathways to the cell surface in yeast by Harsay (1995)
{'key': '2023072822544349300_B22', 'first-page': '6742', 'article-title': 'Characterization of VPS34, a gene required for vacuolar protein sorting and vacuolar segregation', 'volume': '10', 'author': 'Herman', 'year': '1990', 'journal-title': 'Mol Cell Biol'} / Mol Cell Biol / Characterization of VPS34, a gene required for vacuolar protein sorting and vacuolar segregation by Herman (1990)
10.1002/j.1460-2075.1994.tb06382.x / EMBO (Eur Mol Biol Organ) J / VPS21encodes a rab5-like GTP binding protein that is required for the sorting of yeast vacuolar proteins by Horazdovsky (1994)
10.1016/0955-0674(95)80012-3 / Curr Biol / Protein transport to the yeast vacuole by Horazdovsky (1995)
10.1074/jbc.271.52.33607 / J Biol Chem / A novel RING finger protein, Vps8p, functionally interacts with the small GTPase, Vps21p, to facilitate soluble vacuolar protein localization by Horazdovsky (1996)
10.1002/bies.950180508 / Bioessays / Intracellular trafficking of lysosomal membrane proteins by Hunziker (1996)
10.1016/0092-8674(95)90078-0 / Cell / Different requirements for NSF, SNAP, and Rab proteins in apical and basolateral transport in MDCK cells by Ikonen (1995)
10.1146/annurev.ne.17.030194.001251 / Annu Rev Neurosci / Synaptic vesicles and exocytosis by Jahn (1994)
10.1016/0076-6879(90)85033-K / Methods Enzymol / Vacuolar proteases in yeast Saccharomyces cerevisiae. by Jones (1990)
10.1016/S0021-9258(18)92922-4 / J Biol Chem / Three proteolytic systems in the yeast Saccharomyces cerevisiae. by Jones (1991)
10.1016/0378-1119(87)90036-9 / Gene (Amst) / Structural characteristics of the PHO8 gene encoding repressible alkaline phosphatase in Saccharomyces cerevisiae. by Kaneko (1987)
10.1002/j.1460-2075.1989.tb08348.x / EMBO (Eur Mol Biol Organ) J / Membrane protein sorting: biosynthesis, transport and processing of yeast vacuolar alkaline phosphatase by Klionsky (1989)
10.1146/annurev.cb.05.110189.002411 / Annu Rev Cell Biol / The biogenesis of lysosomes by Kornfeld (1989)
10.1016/0076-6879(87)54085-X / Methods Enzymol / Rapid and efficient site-specific mutagenesis without phenotypic selection by Kunkel (1987)
10.1016/S0021-9258(19)49711-1 / J Biol Chem / The VPH1 gene encodes a 95-kDa integral membrane polypeptide required for in vivoassembly and activity of the yeast vacuolar H(+)-ATPase by Manolson (1992)
10.1016/0092-8674(94)90219-4 / Cell / The sorting receptor for yeast vacuolar carboxypeptidase Y is encoded by the VPS10gene by Marcusson (1994)
{'key': '2023072822544349300_B37', 'first-page': '229', 'article-title': 'Endocytosis and antigen processing', 'volume': '2', 'author': 'Mellman', 'year': '1990', 'journal-title': 'Semin Immunol'} / Semin Immunol / Endocytosis and antigen processing by Mellman (1990)
10.1083/jcb.121.6.1197 / J Cell Biol / Membrane protein retention in the yeast Golgi apparatus: dipeptidyl aminopeptidase A is retained by a cytoplasmic signal containing aromatic residues by Nothwehr (1993)
10.1083/jcb.129.1.35 / J Cell Biol / Golgi and vacuolar membrane proteins reach the vacuole in vps1 mutant yeast cells via the plasma membrane by Nothwehr (1995)
10.1038/387199a0 / Nature (Lond) / Homotypic vacuolar fusion mediated by t- and v-SNAREs by Nichols (1997)
10.1016/0092-8674(81)90064-7 / Cell / Order of events in the yeast secretory pathway by Novick (1981)
10.1016/0092-8674(93)90479-A / Cell / Sorting of membrane proteins in the secretory pathway by Pelham (1993)
{'key': '2023072822544349300_B43', 'first-page': '305', 'article-title': 'Yeast Vps45p is a Sec1p-like protein required for the consumption of vacuole-targeted, post-Golgi vesicles', 'volume': '65', 'author': 'Piper', 'year': '1994', 'journal-title': 'Eur J Cell Biol'} / Eur J Cell Biol / Yeast Vps45p is a Sec1p-like protein required for the consumption of vacuole-targeted, post-Golgi vesicles by Piper (1994)
10.1083/jcb.131.3.603 / J Cell Biol / VPS27 controls vacuolar and endocytic traffic through a prevacuolar compartment in Saccharomyces cerevisiae. by Piper (1995)
10.1083/jcb.120.1.55 / J Cell Biol / end3 and end4: two mutants defective in receptor-mediated and fluid-phase endocytosis in Saccharomyces cerevisiae. by Raths (1993)
10.1083/jcb.111.3.877 / J Cell Biol / Molecular analysis of the yeast VPS3gene and the role of its product in vacuolar protein sorting and vacuolar segregation during the cell cycle by Raymond (1990)
10.1091/mbc.3.12.1389 / Mol Biol Cell / Morphological classification of the yeast vacuolar protein sorting mutants: evidence for a prevacuolar compartment in class E vpsmutants by Raymond (1992)
10.1083/jcb.113.3.527 / J Cell Biol / Immunolocalization of Kex2p protease identifies a putative late Golgi compartment in the yeast Saccharomyces cerevisiae. by Redding (1991)
10.1091/mbc.7.6.985 / Mol Biol Cell / Multilamellar endosome-like compartment accumulates in the yeast vps28 vacuolar protein sorting mutant by Rieder (1996)
10.1083/jcb.108.4.1363 / J Cell Biol / Structure, biosynthesis, and localization of dipeptidyl aminopeptidase B, an integral membrane glycoprotein of the yeast vacuole by Roberts (1989)
10.1016/0076-6879(91)94047-G / Methods Enzymol / Methods for studying the yeast vacuole by Roberts (1991)
10.1016/0955-0674(94)90074-4 / Curr Opin Cell Biol / The role of clathrin, adaptors and dynamin in endocytosis by Robinson (1994)
10.1016/0092-8674(86)90819-6 / Cell / Protein sorting in yeast: mutants defective in vacuolar biogenesis mislocalize proteins into the late secretory pathway by Rothman (1986)
10.1126/science.272.5259.227 / Science (Wash DC) / Protein sorting by transport vesicles by Rothman (1996)
10.1126/science.271.5255.1526 / Science (Wash DC) / Coat proteins and vesicle budding by Schekman (1996)
10.1242/jcs.106.3.823 / J Cell Sci / Involvement of Ypt7p, a small GTPase, in traffic from late endosome to the vacuole in yeast by Schimmoller (1993)
10.1016/S0962-8924(97)01050-7 / Trends Cell Biol / Nonclassical protein sorting by Scott (1997)
10.1002/j.1460-2075.1992.tb05348.x / EMBO (Eur Mol Biol Organ) J / A role for clathrin in the sorting of vacuolar proteins in the Golgi complex of yeast by Seeger (1992)
10.1002/j.1460-2075.1992.tb05348.x / EMBO (Eur Mol Biol Organ) J / A role for clathrin in the sorting of vacuolar proteins in the Golgi complex of yeast by Seeger (1992)
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)
10.1083/jcb.110.6.1911 / J Cell Biol / Detection of an intermediate compartment involved in transport of α-factor from the plasma membrane to the vacuole in yeast by Singer (1990)
10.1083/jcb.125.2.283 / J Cell Biol / Role of three rab5-like GTPases, Ypt51p, Ypt52p, and Ypt53p, in the endocytic and vacuolar protein sorting pathways of yeast by Singer-Kruger (1994)
10.1146/annurev.cb.11.110195.000245 / Annu Rev Cell Dev Biol / Receptor-mediated protein sorting to the vacuole in yeast: roles for a protein kinase, a lipid kinase and GTP-binding proteins by Stack (1995)
10.1083/jcb.121.6.1245 / J Cell Biol / Yeast vacuolar proenzymes are sorted in the late Golgi complex and transported to the vacuole via a prevacuolar endosome-like compartment by Vida (1993)
10.1016/S0021-9258(19)37012-7 / J Biol Chem / Genes for directing vacuolar morphogenesis in Saccharomyces cerevisiae. I. Isolation and characterization of two classes of vammutants by Wada (1992)
10.1016/S0092-8674(05)80062-5 / Cell / Endocytosis in yeast: evidence for the involvement of a small GTP-binding protein (Ypt7p) by Wichmann (1992)
10.1002/j.1460-2075.1993.tb05974.x / EMBO (Eur Mol Biol Organ) J / Vps1p, a member of the dynamin GTPase family, is necessary for Golgi membrane protein retention in Saccharomyces cerevisiae. by Wilsbach (1993)
10.1093/genetics/102.4.679 / Genetics / Genetic properties of mutations at the PEP4 locus in Saccharomyces cerevisiae. by Zubenko (1982)

Dates

Type	When
Created	23 years, 1 month ago (July 26, 2002, 12:47 p.m.)
Deposited	2 years, 1 month ago (July 28, 2023, 6:55 p.m.)
Indexed	11 months, 3 weeks ago (Sept. 9, 2024, 4:38 p.m.)
Issued	28 years ago (Aug. 11, 1997)
Published	28 years ago (Aug. 11, 1997)
Published Online	28 years ago (Aug. 11, 1997)
Published Print	28 years ago (Aug. 11, 1997)

Funders 0

None

BibTeX

@article{Piper_1997, title={The Membrane Protein Alkaline Phosphatase Is Delivered to the Vacuole by a Route That Is Distinct from the VPS-dependent Pathway}, volume={138}, ISSN={1540-8140}, url={http://dx.doi.org/10.1083/jcb.138.3.531}, DOI={10.1083/jcb.138.3.531}, number={3}, journal={The Journal of Cell Biology}, publisher={Rockefeller University Press}, author={Piper, Robert C. and Bryant, Nia J. and Stevens, Tom H.}, year={1997}, month=aug, pages={531–545} }

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      "article-title": "A family of proteins involved in intracellular transport",
      "volume": "68",
      "author": "Aalto",
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      "journal-title": "Cell"
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      "doi-asserted-by": "crossref",
      "first-page": "9075",
      "DOI": "10.1073/pnas.83.23.9075",
      "article-title": "Isolation of yeast mutants defective in protein targeting to the vacuole",
      "volume": "83",
      "author": "Bankaitis",
      "year": "1986",
      "journal-title": "Proc Natl Acad Sci USA"
    },
    {
      "key": "2023072822544349300_B3",
      "first-page": "4638",
      "article-title": "Characterization of yeast Vps33p, a protein required for vacuolar protein sorting and vacuole biogenesis",
      "volume": "10",
      "author": "Banta",
      "year": "1990",
      "journal-title": "Mol Cell Biol"
    },
    {
      "key": "2023072822544349300_B4",
      "doi-asserted-by": "crossref",
      "first-page": "233",
      "DOI": "10.1111/j.1749-6632.1994.tb17273.x",
      "article-title": "Biogenesis of secretory granules and synaptic vesicles. Facts and hypotheses",
      "volume": "733",
      "author": "Bauerfeind",
      "year": "1994",
      "journal-title": "Ann NY Acad Sci"
    },
    {
      "key": "2023072822544349300_B5",
      "doi-asserted-by": "crossref",
      "first-page": "579",
      "DOI": "10.1091/mbc.7.4.579",
      "article-title": "Novel syntaxin homolog, Pep12p, required for the sorting of lumenal hydrolases to the lysosome-like vacuole in yeast",
      "volume": "7",
      "author": "Becherer",
      "year": "1996",
      "journal-title": "Mol Biol Cell"
    },
    {
      "key": "2023072822544349300_B6",
      "doi-asserted-by": "crossref",
      "first-page": "1185",
      "DOI": "10.1091/mbc.5.11.1185",
      "article-title": "Metabolic instability and constitutive endocytosis of STE6, the a-factor transporter of Saccharomyces cerevisiae.",
      "volume": "5",
      "author": "Berkower",
      "year": "1994",
      "journal-title": "Mol Biol Cell"
    },
    {
      "key": "2023072822544349300_B7",
      "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 yeast: 5-fluororotic acid resistance",
      "volume": "197",
      "author": "Boeke",
      "year": "1984",
      "journal-title": "Mol Gen Genet"
    },
    {
      "key": "2023072822544349300_B8",
      "doi-asserted-by": "crossref",
      "first-page": "287",
      "DOI": "10.1083/jcb.136.2.287",
      "article-title": "Two separate signals act independently to localize a yeast late Golgi membrane protein through a combination of retrieval and retention",
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      "author": "Bryant",
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    {
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      "journal-title": "J Cell Biol"
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      "author": "Cowles",
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      "volume": "122",
      "author": "Davis",
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      "journal-title": "J Cell Biol"
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    {
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      "first-page": "559",
      "DOI": "10.1016/0959-4388(95)80059-X",
      "article-title": "The function of dynamin in endocytosis",
      "volume": "5",
      "author": "De Camilli",
      "year": "1995",
      "journal-title": "Curr Opin Neurobiol"
    },
    {
      "key": "2023072822544349300_B16",
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      "article-title": "Invertase beta-galactosidase hybrid proteins fail to be transported from the endoplasmic reticulum in Saccharomyces cerevisiae.",
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      "author": "Emr",
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      "journal-title": "Mol Cell Biol"
    },
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      "author": "Govidan",
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      "author": "Haas",
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      "author": "Harsay",
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      "volume": "10",
      "author": "Herman",
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      "volume": "13",
      "author": "Horazdovsky",
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      "volume": "81",
      "author": "Ikonen",
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      "volume": "17",
      "author": "Jahn",
      "year": "1994",
      "journal-title": "Annu Rev Neurosci"
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      "volume": "185",
      "author": "Jones",
      "year": "1990",
      "journal-title": "Methods Enzymol"
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      "key": "2023072822544349300_B31",
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      "volume": "58",
      "author": "Kaneko",
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      "volume": "8",
      "author": "Klionsky",
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      "author": "Kornfeld",
      "year": "1989",
      "journal-title": "Annu Rev Cell Biol"
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      "volume": "154",
      "author": "Kunkel",
      "year": "1987",
      "journal-title": "Methods Enzymol"
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    {
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      "volume": "267",
      "author": "Manolson",
      "year": "1992",
      "journal-title": "J Biol Chem"
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    {
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      "first-page": "579",
      "DOI": "10.1016/0092-8674(94)90219-4",
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      "volume": "77",
      "author": "Marcusson",
      "year": "1994",
      "journal-title": "Cell"
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    {
      "key": "2023072822544349300_B37",
      "first-page": "229",
      "article-title": "Endocytosis and antigen processing",
      "volume": "2",
      "author": "Mellman",
      "year": "1990",
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      "key": "2023072822544349300_B38",
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      "first-page": "1197",
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      "volume": "121",
      "author": "Nothwehr",
      "year": "1993",
      "journal-title": "J Cell Biol"
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      "first-page": "35",
      "DOI": "10.1083/jcb.129.1.35",
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      "volume": "129",
      "author": "Nothwehr",
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      "journal-title": "J Cell Biol"
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    {
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      "first-page": "199",
      "DOI": "10.1038/387199a0",
      "article-title": "Homotypic vacuolar fusion mediated by t- and v-SNAREs",
      "volume": "387",
      "author": "Nichols",
      "year": "1997",
      "journal-title": "Nature (Lond)"
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      "key": "2023072822544349300_B41",
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      "first-page": "461",
      "DOI": "10.1016/0092-8674(81)90064-7",
      "article-title": "Order of events in the yeast secretory pathway",
      "volume": "25",
      "author": "Novick",
      "year": "1981",
      "journal-title": "Cell"
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      "key": "2023072822544349300_B42",
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      "volume": "75",
      "author": "Pelham",
      "year": "1993",
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      "article-title": "Yeast Vps45p is a Sec1p-like protein required for the consumption of vacuole-targeted, post-Golgi vesicles",
      "volume": "65",
      "author": "Piper",
      "year": "1994",
      "journal-title": "Eur J Cell Biol"
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      "volume": "131",
      "author": "Piper",
      "year": "1995",
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      "first-page": "55",
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      "volume": "120",
      "author": "Raths",
      "year": "1993",
      "journal-title": "J Cell Biol"
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    {
      "key": "2023072822544349300_B46",
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      "first-page": "877",
      "DOI": "10.1083/jcb.111.3.877",
      "article-title": "Molecular analysis of the yeast VPS3gene and the role of its product in vacuolar protein sorting and vacuolar segregation during the cell cycle",
      "volume": "111",
      "author": "Raymond",
      "year": "1990",
      "journal-title": "J Cell Biol"
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    {
      "key": "2023072822544349300_B47",
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      "first-page": "1389",
      "DOI": "10.1091/mbc.3.12.1389",
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      "volume": "3",
      "author": "Raymond",
      "year": "1992",
      "journal-title": "Mol Biol Cell"
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    {
      "key": "2023072822544349300_B48",
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      "first-page": "527",
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      "volume": "113",
      "author": "Redding",
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    {
      "key": "2023072822544349300_B49",
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      "first-page": "985",
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      "author": "Rieder",
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      "volume": "108",
      "author": "Roberts",
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      "first-page": "644",
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      "author": "Roberts",
      "year": "1991",
      "journal-title": "Methods Enzymol"
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      "author": "Robinson",
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      "volume": "106",
      "author": "Schimmoller",
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      "DOI": "10.1016/S0962-8924(97)01050-7",
      "article-title": "Nonclassical protein sorting",
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      "author": "Scott",
      "year": "1997",
      "journal-title": "Trends Cell Biol"
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      "volume": "11",
      "author": "Seeger",
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      "author": "Seeger",
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      "volume": "122",
      "author": "Sikorski",
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      "volume": "110",
      "author": "Singer",
      "year": "1990",
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      "volume": "11",
      "author": "Stack",
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    "1540-8140"
  ],
  "subject": [],
  "published": {
    "date-parts": [
      [
        1997,
        8,
        11
      ]
    ]
  }
}