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2001 | 48 | 4 | 1025-1042
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Saccharomyces cerevisiae - a model organism for the studies on vacuolar transport.

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The role of the yeast vacuole, a functional analogue of the mammalian lysosome, in the turnover of proteins and organelles has been well documented. This review provides an overview of the current knowledge of vesicle mediated vacuolar transport in the yeast Saccharomyces cerevisiae cells. Due to the conservation of the molecular transport machinery S. cerevisiae has become an important model system of vacuolar trafficking because of the facile application of genetics, molecular biology and biochemistry.

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  • Institute of Biochemistry and Biophysics, Polish Academy of Sciences, Warszawa, Poland
  • Institute of Biochemistry and Biophysics, Polish Academy of Sciences, Warszawa, Poland
  • Abeliovich, H., Grote, E., Novick, P. & Ferro-Novick, S. (1998) Tlg2p, a yeast syntaxin homolog that resides on the Golgi and endocytic structure. J. Biol. Chem. 273, 11719-11727.
  • Abeliovich, H., Darsow, T. & Emr, S.D. (1999) Cytoplasm to vacuole trafficking of aminopeptidase I requires a t-SNARE-Sec1p complex composed of Tlg2p and Vps45p. EMBO J. 18, 6005-6016.
  • Baba, M., Takeshige, K., Baba, N. & Ohsumi, Y. (1994) Ultrastructural analysis of the autophagic process in yeast: Detection of autophagosomes and their characterisation. J. Cell Biol. 124, 903-913.
  • Baba, M., Oshumi, M., Scott, S.V., Klionsky, D.J. & Oshumi, Y. (1997) Two distinct pathways for targeting proteins from the cytoplasm to the vacuole/lysosome. J. Cell Biol. 139, 1687- 1695.
  • Bagnat, M., Keranen, S., Shevchenko, A. & Simons, K. (2000) Lipid rafts function in biosynthetic delivery of proteins to the cell surface in yeast. Proc. Natl. Acad. Sci. U.S.A. 97, 3254-3259.
  • Barlowe, C. (1997) Coupled ER to Golgi transport reconstituted with purified cytosolic components. J. Cell Biol. 139, 1097-1108.
  • Barrowman, J., Sacher, M. & Ferro-Novick, S. (2000) TRAPP stably associates with the Golgi and is required for vesicle docking. EMBO J. 19, 862-869.
  • Benli, M., Doring, F., Robinson, D.G., Yang, X. & Gallwitz, D. (1996) Two GTPase isoforms, Ypt31p and Ypt32p, are essential for Golgi function in yeast. EMBO J. 15, 6460-6475.
  • Bryant, N.J. & Stevens, T.H. (1997) Two separate signals act independently to localise a yeast membrane protein through a combination of retrieval and retention. J. Cell Biol. 136, 287-297.
  • Bryant, N.J. & Stevens, T.H. (1998) Vacuole biogenesis in Saccharomyces cerevisiae: protein transport pathways to the yeast vacuole. Microbiol. Mol. Biol. Rev. 62, 230-247.
  • Catlett, N.L. & Weisman, L.S. (2000) Divide and multiply: Organelle partitioning in yeast. Curr. Opin. Cell Biol. 12, 509-516.
  • Conibear, E. & Stevens, T.H. (1995) Vacuolar biogenesis in yeast: Sorting out the sorting proteins. Cell 83, 513-516.
  • Conibear, E. & Stevens, T.H. (1998) Multiple sorting pathways between the late Golgi and the vacuole in yeast. Biochim. Biophys. Acta 1404, 211-230.
  • Conibear, E. & Stevens, T.H. (2000) Vps52p, Vps53p, and Vps54p form a novel multisubunit complex required for protein sorting at the yeast late Golgi. Mol. Biol. Cell. 11, 305-323.
  • Cooper, A.A. & Stevens, T.H. (1996) Vps10p cycles between the late-Golgi and prevacuolar compartments in its function as the sorting receptor for multiple yeast vacuolar hydrolases. J. Cell Biol. 133, 529-541.
  • Costaguta, G., Stefan, C.J., Bensen, E.S., Emr, S.D., Payne, G.S., Leber, R., Silles, E., Sandoval, I.V. & Mazon, M.J. (2001) Yeast Gga coat proteins function with clathrin in Golgi to endosome transport. Mol. Biol. Cell. 12, 1885-1896.
  • Darsow, T., Rieder, S.E. & Emr, S.D. (1997) A multi-specific syntaxin homolog, Vam3p, essential for autophagic and biosynthetic protein transport to the vacuole. J. Cell Biol. 138, 517-529.
  • D'Hondt, K., Heese-Peck, A. & Riezman, H. (2000) Protein and lipid requirement for endocytosis. Annu. Rev. Genet. 34, 255-295.
  • Fischer von Mollard, G. & Stevens, T.H. (1999) The Saccharomyces cerevisiae v-SNARE Vti1p is required for multiple membrane transport pathways to the vacuole. Mol. Biol. Cell 10, 1719-1732.
  • Finken-Eigen, M., Muller, S. & Kohrer, K. (1997) Cloning and characterisation of a dominant- negative vps1 allele of the yeast Saccharomyces cerevisiae. Biol. Chem. 378, 1187-1191.
  • Fukui, K., Sasaki, T., Imazumi, K., Matsuura, Y., Nakanishi, H. & Takai,Y. (1997) Isolation and characterisation of a GTPase activating protein specific for the Rab3 subfamily small G proteins. J. Biol. Chem. 272, 4655-4658.
  • Gagny, B., Wiederkehr, A., Dumoulin, P., Winsor, B., Riezman, H. & Haguenauer-Tsapis, R. (2000) A novel EH domain protein of Saccharomyces cerevisiae, Ede1p, involved in endocytosis. J. Cell Sci. 113, 3309-3319.
  • Gallwitz, D., Donath, C. & Sander, C. (1983) A yeast gene encoding a protein homologous to the human c-has/bas proto-encogene product. Nature 306, 704-707.
  • Gerrard, S.R., Bryant, N.J. & Stevens, T.H. (2000) VPS21 controls entry of endocytosed and biosynthetic proteins into the yeast prevacuolar compartment. Mol. Biol. Cell 11, 613-626.
  • Gotte, M. & Lazar, T. (1999) The ins and outs of yeast vacuole trafficking. Protoplasma 209, 9-18.
  • Gotte, M., Lazar, T., Yoo, J.S., Scheglmann, D. & Gallwitz, D. (2000) The full complement of yeast Ypt/Rab-GTPases and their involvement in exo- and endocytic trafficking. Subcell. Biochem. 34, 133-173.
  • Graham, T.R. & Emr, S.D. (1991) Compartmental organisation of Golgi-specific protein modification and vacuolar protein sorting events defined in a yeast sec18 (NSF) mutant. J. Cell Biol. 114, 207-218.
  • Griff, I.C., Schekman, R., Rothman, J.E. & Kaiser, C.A. (1992) The yeast SEC17 gene product is functionally equivalent to mammalian alpha-SNAP protein. J. Biol. Chem. 267, 12106-12115.
  • Harding, T.M., Morano, K.A., Scott, S.V. & Klionsky, D.J. (1995) Isolation and characterisation of yeast mutants in the cytoplasm to vacuole protein targeting pathway. J. Cell Biol. 131, 591-602.
  • Harding, T.M., Hefner-Gravink, A., Thumm, M. & Klionsky, D.J. (1996) Genetic and phenotypic overlap between autophagy and the cytoplasm to vacuole protein targeting pathway. J. Biol. Chem. 271, 17621-17624.
  • Harris, S.L. & Waters, M.G. (1996) Localisation of yeast early Golgi mannosyltransferase, Och1p, involves retrograde transport. J. Cell Biol. 132, 985-998.
  • Harsay, E. & Bretscher, A. (1995) Parallel secretory pathway to the cell surface in yeast. J. Cell Biol. 131, 297-310.
  • Hershko, A., Ciechanover, A. & Varshavsky, A. (2000) The ubiquitin system. Nat. Med. 6, 1073-1081.
  • Hicke, L. (2001) A new ticket for entry into budding vesicles - ubiquitin . Cell 106, 527-530.
  • Hicke, L., Zanolari, B., Pypaert, M., Rohrer, J. & Riezman, H. (1997) Transport through the yeast endocytic pathway occurs through morphologically distinct compartments and requires an active secretory pathway and Sec18p/ N-ethylmaleimide-sensitive fusion protein. Mol. Biol. Cell 8, 13-31.
  • Holthius, J.C., Nichols, B.J., Dhruvakumar, S. & Pelham, H.R. (1998) Two syntaxin homologues in the TGN/endosomal system of yeast. EMBO J. 17, 113-126.
  • Horazdovsky, B.F., DeWald, D.B. & Emr, S.D. (1995) Protein transport to the yeast vacuole. Curr. Opin. Cell. Biol 7, 544-551.
  • Hutchins, M.U. & Klionsky, D.J. (2001) Vacuolar localisation of oligomeric α-mannosidase requires the cytoplasm to vacuole targeting and autophagy pathway components in Saccharomyces cerevisiae. J Biol. Chem. 276, 20491- 20498.
  • Johnson, L.M., Baankaitis, V.A. & Emr, S.D. (1987) Distinct sequence determinants direct intracellular sorting and modification of a yeast vacuolar protease. Cell 48, 875-885.
  • Jones, E.W., Webb, G.C. & Hiller, M.A. (1997) Biogenesis and function of the yeast vacuole; in Molecular Biology of the Yeast Saccharomyces cerevisiae (Pringle, J.R., Broach, J.R. & Jones, E.W., eds.) vol. 3, 363-469, CSH Laboratory Press, Cold Spring Harbor, N.Y.
  • Katzmann, D.J., Babst, M. & Emr, S.D. (2001) Ubiquitin-dependent sorting into multivesicular body pathway requires the function of a conserved endosomal protein sorting complex, ESCRT-I. Cell 106, 145-155.
  • Kim, J. & Klionsky, D.J. (2000) Autophagy, cytoplasm-to-vacuole targeting pathway, and pexophagy in yeast and mammalian cells. Annu. Rev. Biochem. 69, 303-342.
  • Klionsky, D. J. (1998) Nonclassical protein sorting to the yeast vacuole. J. Biol. Chem. 273, 10807-10810.
  • Klionsky, D.J. & Emr, S.D. (2000) Autophagy as a regulated pathway of cellular degradation. Science 290, 1717-1721.
  • Klumperman, J. (2000) Transport between ER and Golgi. Curr. Opin. Cell Biol. 12, 445-449.
  • Kucharczyk, R., Dupre, S., Avaro, S., Haguenauer- Tsapis, R., Slonimski, P. & Rytka, J. (2000) The novel protein Ccz1p required for vacuolar assembly in Saccharomyces cerevisiae functions in the same transport pathway as Ypt7p. J. Cell Sci. 113, 4301-4311.
  • Kucharczyk, R., Kierzek, A.M., Slonimski, P.P. & Rytka, J. (2001) The Ccz1 protein interacts with Ypt7 GTPase during fusion of multiple transport intermediates with the vacuole in S. cerevisiae. J. Cell Sci. 114, 3137-3145.
  • Lang, T., Schaeffeler, E., Bernreuther, D., Bredschneider, M., Wolf, D.H. & Thumm, M. (1998) Aut2p and Aut7p, two novel microtubule associated proteins are essential for delivery of autophagic vesicles to the vacuole. EMBO J. 17, 3597-3607.
  • Lazar, T., Gotte, M. & Gallwitz, D.(1997) Vesicular transport: How many Ypt/Rab-GTPases make a eukaryotic cell? Trends Biochem. Sci. 22, 468-472.
  • Lemmon, S.K. & Traub, L.M. (2000) Sorting in the endosomal system in yeast and animal cells. Curr. Opin. Cell Biol. 12, 457-466.
  • Marcusson, E.G., Horazdovsky, B.F., Cereghino, J.L., Gharakhanian, E. & Emr, S.D. (1994) The sorting receptor for yeast vacuolar carboxypeptidase Y is encoded by VPS10 gene. Cell 77, 579-586.
  • Martinez, E., Jimenez, M.A., Segui-Real, B., Vandekerckhove, J. & Sandoval, I.V. (1997) Folding of the presequence of yeast pAPI into an amphipathic helix determines transport of the protein from the cytosol to the vacuole. J. Mol. Biol. 267, 1124-1138.
  • Matsuura, A., Tsukada, M., Wada, Y. & Ohsumi, Y. (1997) Apg1p, a novel protein kinase required for the autophagic process in Saccharomyces cerevisiae. Gene 192, 245-250.
  • Mayer, A. & Wickner, W. (1997) Docking of yeast vacuoles is catalysed by the Ras-like GTPase Ypt7p after symmetric priming by Sec18p (NSF). J. Cell Biol. 136, 307-317.
  • McMahon, H.T., Wigge, P. & Smith, C. (1997) Clathrin interacts specifically with amphiphysin and is displaced by dynamin. FEBS Lett. 413, 319-322.
  • Nichols, B.J. & Pelham, H.R. (1998) SNAREs and membrane fusion in the Golgi apparatus. Biochim. Biophys. Acta 1404, 9-31.
  • Nichols, B.J., Holthuis, J.C. & Pelham, H.R. (1998) The Sec1p homologue Vps45p binds to the syntaxin Tlg2p. Eur. J. Cell Biol. 77, 263-268.
  • Oda, M.N., Scott, S.V., Hefner-Gravink, A., Caffarelli, A.D. & Klionsky, D.J. (1996) Identification of a cytoplasm to vacuole targeting determinant in aminopeptidase I. J. Cell Biol. 132, 999-1010.
  • Odorizzi, G., Cowles, Ch.R. & Emr, S.D. (1998) The AP-3 complex a coat of many colours. Trends Cell Biol. 8, 282-288.
  • Payne, G.S., Baker, D., van Tuinen, E. & Schekman, R. (1998) Protein transport to the vacuole and receptor-mediated endocytosis by clathrin heavy chain deficient yeast. J. Cell Biol. 106, 1453-1461.
  • Peng, R., Grabowski, R., De Antoni, A. & Gallwitz, D. (1999) Specific interaction of the yeast cis-Golgi syntaxin Sed5p and the coat protein complex II component Sec24p of endoplasmic reticulum-derived transport vesicles. Proc. Natl. Acad. Sci. U.S.A. 96, 3751-3756.
  • 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. J. Cell Biol. 138, 531-545.
  • Preuss, D., Mulholland, J., Franzusoff, A., Segev, N. & Botstein, D. (1992) Characterisation of the Saccharomyces Golgi complex through the cell cycle by immunoelectron microscopy. Mol. Biol. Cell 3, 789-803.
  • Price, A., Seals, D., Wickner, W. & Ungermann, C. (2000) The docking stage of yeast vacuole fusion requires the transfer of proteins from a cis-SNARE complex to a Rab/Ypt protein. J.Cell Biol. 148, 1231-1238.
  • Prescianotto-Baschong, C. & Riezman, H. (1998) Morphology of the yeast endocytic pathway. Mol. Biol. Cell 9, 173-189.
  • Raymond, C.K., Howald-Stevenson, I., Vater, C.A. & Stevens, T.H. (1992) Morphological classification of the yeast vacuolar protein sorting mutants: Evidence for a prevacuolar compartment in class E vps mutants. Mol. Biol. Cell 3, 1389-1402.
  • Rehling, P., Darsow, T., Katzmann, D.J. & Emr, S.D. (1999) Formation of AP-3 transport intermediates requires Vps41p function. Nat. Cell Biol. 1, 346-353.
  • Rieder, S. & Emr, S.D. (1997) A novel RING finger protein complex essential for a late step in protein transport to the yeast vacuole. Mol. Biol. Cell 8, 2307-2327.
  • Rotin, D., Staub, O. & Haguenauer-Tsapis, R. (2000) Ubiquitination and endocytosis of plasma membrane proteins: Role of Nedd4/ Rsp5p family of ubiquitin-protein ligases. J. Membr. Biol. 176, 1-17.
  • Rothman, J.E. (1996) The protein machinery of vesicle budding and fusion. Protein Sci. 5, 185-194.
  • Salminen, A. & Novick, P.J. (1987) A ras-like protein is required for a post-Golgi event in yeast secretion. Cell 49, 527-538.
  • Sato, T.K., Rehling, P., Peterson, M.R. & Emr, S.D. (2000) Class C Vps protein complex regulates vacuolar SNARE pairing and is required for vesicle docking/fusion. Mol. Cell 6, 661-671.
  • Schekman, R. & Orci, L. (1996) Coat proteins and vesicle budding. Science 271, 1526-1533.
  • Scott, S.V., Hefner-Gravink, A., Morano, K.A., Noda, T., Ohsumi, Y. & Klionsky, D.J. (1997) Cytoplasm to vacuole targeting and autophagy employ the same machinery to deliver proteins to the yeast vacuole. Proc. Natl. Acad. Sci. U.S.A. 93, 12304-12308.
  • Shieh, H.L., Chen, Y., Brown, C.R. & Chiang, H.L. (2001) Biochemical analysis of fructose-1,6-bisphosphatase import into vacuole import and degradation vesicles reveales a role of UBC1 in vesicle biogenesis. J. Biol. Chem. 276, 10398-10406.
  • Simonsen, A., Wurmser, A.E., Emr, S.D. & Stenmark, H. (2001) The role of phosphoinositides in membrane transport. Curr. Opin. Cell Biol. 13, 485-492.
  • Singer-Kruger, B., Frank, R., Crausaz, F. & Riezman, H. (1993) Partial purification and characterisation of early and late endosomes from yeast. Identification of four novel proteins. J. Biol. Chem. 268, 14376-86.
  • Singer-Kruger, B., Nemoto, Y., Daniell, L., Ferro-Novick, S. & De Camilli, P. (1998) TRAPP, a highly conserved novel complex on the cis-Golgi that mediates vesicle docking and fusion. EMBO J. 17, 2494-2503.
  • Soldati, T., Shapiro, A.D., Dirac Svejstrup, A.B. & Pfiffer, S.R. (1994) Membrane targeting of the small GTPase Rab9 is accompanied by nucleotide exchange. Nature 369, 76-78.
  • Sollner, T., Whiteheart, S.W., Brunner, M., Erdjument-Bromage, H., Geromanos, S., Tempst, P. & Rothman, J.E. (1993) SNAP receptors implicated in vesicle targeting and fusion. Nature 362, 318-324.
  • Sorkin, A. (2000) The endocytosis machinery. J. Cell Sci. 113, 4375-4376.
  • Stack, J.H., Herman, P.K., Schu, P.V. & Emr, S.D. (1993) A membrane-associated complex containing the Vps15 protein kinase and the Vps34 PI 3-kinase is essential for protein sorting to the yeast lysosome-like vacuole. EMBO J. 12, 2195-2204.
  • Stone, S., Sacher, M., Mao, Y., Carr, C., Lyons, P., Quinn, A.M. & Ferro-Novick, S. (1997) Bet1p activates the v-SNARE Bos1p. Mol. Biol. Cell 8, 1175-1181.
  • Strom, M., Vollmer, P., Tan, T.J. & Gallwitz, D. (1993) A yeast GTPase-activating protein that interacts specifically with a member of the Ypt/Rab family. Nature 361, 736-739.
  • Suriapranata, I., Epple, U.D., Bernreuther, D., Bredschneider, M., Sovarasteanu, K. & Thumm, M. (2000) The breakdown of autophagic vesicles inside the vacuole depends on Aut4p. J. Cell Sci. 113, 4025-4033.
  • Sutton, R.B., Fasshauer, D., Jahn, R. & Brunger, A.T. (1998) Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 Å resolution. Nature 395, 347-353.
  • Tall, G.G., Hama, H., DeWald, D.B. & Horazdovsky, B.F. (1999) The phosphatidylinositol 3-phosphate binding protein Vac1p interacts with a Rab GTPase and Sec1p homologue to facilitate vesicle-mediated vacuolar protein sorting. Mol. Biol. Cell 10, 1873-1889.
  • Tan, P.K., Howard, J.P. & Payne, G.S. (1996) The sequence NPFXD defines a new class of endocytosis signal in Saccharomyces cerevisiae. J. Cell Biol. 135, 1789-1800.
  • Tang, H.Y., Munn, A. & Cai, M. (1997) EH domain proteins Pan1p and End3p are components of a complex that plays a dual role in organisation of the cortical actin cytoskeleton and endocytosis in Saccharomyces cerevisiae. Mol. Cell Biol. 17, 4294-4304.
  • Thumm, M., Egner, R., Koch, B., Schlumpberger, M., Straub, M., Veenhuis, M. & Wolf, D.H. (1994) Isolation of autophagocytosis mutants of Saccharomyces cerevisiae. FEBS Lett. 349, 275-280.
  • Ullrich, O., Horiuchi, V.I., Bucci, C. & Zerial, M. (1994) Membrane association of Rab5 mediated by GDP-dissociation inhibitor and accompanied by GDP/GTP exchange. Nature 368, 157-160.
  • Ungermann, C., Sato, K. & Wickner, W. (1998) Defining the functions of trans-SNARE pairs. Nature 396, 543-548.
  • Ungermann, C., von Mollard, G.F., Jensen, O.N., Margolis, N., Stevens, T.H. & Wickner, W. (1999) Three v-SNAREs and two t-SNAREs, present in a pentameric cis-SNARE complex on isolated vacuoles, are essential for homotypic fusion. J. Cell Biol.145, 1435-1454.
  • Vida, T.A. & Emr, S.D. (1995) A new vital stain for visualising vacuolar membrane dynamics and endocytosis in yeast. J. Cell Biol. 128, 779- 792.
  • Wang, W., Sacher, M. & Ferro-Novick, S. (2000) TRAPP stimulates guanine nucleotide exchange on Ypt1p. J. Cell Biol. 151, 289-296.
  • Weber, T., Zemelmann, B., McNew, J.A., Westermann, B., Gmachl, M., Parlati, F., Sollner, T.H. & Rothman, J.E. (1998) SNAREpins: Minimal machinery for membrane fusion. Cell 92, 759-772.
  • Wendland, B., Emr, S.D. & Riezman, H. (1998) Protein traffic in the yeast endocytic and vacuolar protein sorting pathways. Curr. Opin. Cell Biol. 10, 513-522.
  • Westphal, V., Marcusson, E.G., Winther, J.R., Emr, S.D. & van den Hazel, H.B. (1996) Multiple pathways for vacuolar sorting of yeast proteinase A. J. Biol. Chem. 271, 11865- 11870.
  • Wilson, D.W., Wilcox, C.A., Flynn, G.C., Chen, E., Kuang, W.J., Henzel, W.J., Block, M.R., Ullrich, A. & Rothman, J.E. (1989) A fusion protein required for vesicle-mediated transport in both mammalian cells and yeast. Nature 339, 355-359.
  • Wurmser, A.E., Sato, T.K. & Emr, S. (2000) New component of the vacuolar class C-Vps complex couples nucleotide exchange on the Ypt7 GTPase to SNARE-dependent docking and fusion. J. Cell Biol. 151, 551-562.
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