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The ins and outs of yeast vacuole trafficking

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Summary

Vacuoles are ubiquitous organelles in the fungal and plant kingdoms. They serve a variety of functions and are important for cell homeostasis. A constant turnover of proteins and membranes makes vacuoles dynamic organelles. Various transport pathways share the vacuole as their joint destination. The trafficking pathways are regulated independently. In yeast cells many components of the protein and membrane transport machinery are known. Recent years have seen much progress in our understanding of the protein-sorting pathways and the biogenesis of this organelle. Improvements of our understanding of the vesicular transport pathways and vacuolar membrane fusion are reviewed.

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Abbreviations

ALP:

alkaline phosphatase

AP:

adaptor protein complex

CPY:

carboxypeptidase Y

CPS:

carboxypeptidase S

NSF:

N-ethylmaleimide-sensitive membrane fusion protein

PIP:

phos-phatidyl inositol phosphate

PVC:

prevacuolar compartment

SNAP:

soluble N-ethylmaleimide-sensitive factor attachment protein

SNARE SNAP:

receptor

TGN:

trans-Golgi network

vam :

vacuolar morphology (mutant)

vps :

vacuolar protein sorting (mutant)

References

  • Albert S, Will E, Gallwitz D (1999) Identification of the catalytic domains and their functionally critical arginine residues of two yeast GTPase-activating proteins specific for Ypt/Rab transport GTPases. EMBO J (in press)

  • Bode H-P, Dumschat M, Garotti S, Fuhrmann GF (1995) Iron sequestration by the yeast vacuole. Eur J Biochem 228: 337–342

    Article  PubMed  CAS  Google Scholar 

  • Bone N, Millar JBA, Toda T, Armstrong J (1998) Regulated vacuole fusion and fission inSchizosaccharomyces pombe: an osmotic response dependent on MAP kinases. Curr Biol 8: 135–144

    Article  PubMed  CAS  Google Scholar 

  • Booth JW, Guidotti G (1997) Phosphate transport in yeast vacuoles. J Biol Chem 272: 20408–20413

    Article  PubMed  CAS  Google Scholar 

  • Bryant NJ, Piper RC, Gerrard, SR, Stevens TH (1998a) Traffic into the prevacuolar compartment ofS. cerevisiae: aVPS45-dependent intracellular route and aVTS45-independent endocytic route. Eur J Cell Biol 76: 43–52

    PubMed  CAS  Google Scholar 

  • — —, Weisman LS, Stevens TH (1998b) Retrograde traffic out of the yeast vacuole to the TGN occurs via the prevacuolar/endosomal compartment. J Cell Biol 142: 651–663

    Article  PubMed  CAS  Google Scholar 

  • Burd CG, Emr SD (1998) Phosphatidylinositol-3-phosphate signalling mediated by specific binding to RING FYVE domains. Mol Cell 2: 157–162

    Article  PubMed  CAS  Google Scholar 

  • —, Peterson M, Cowles CR, Emr SD (1997) A novel Sec18p/NSF-dependent complex required for Golgi-to-endosome transport in yeast. Mol Biol Cell 8: 1089–1104

    PubMed  CAS  Google Scholar 

  • Conibear E, Stevens TH (1998) Multiple sorting pathways between the late golgi and the vacuole in yeast. Biochim Biophys Acta 1404: 211–230

    Article  PubMed  CAS  Google Scholar 

  • Conradt B, Shaw J, Vida, T, Emr S, Wickner W (1992) In vitro reactions of vacuole inheritance inSaccharomyces cerevisiae. J Cell Biol 119: 1469–1479

    Article  PubMed  CAS  Google Scholar 

  • Cooke FT, Dove SK, McEwan RK, Painter G, Holmes AB, Hall MN, Michell RH, Parker PJ (1998) The stress-activated phosphatidyl-inositol-3-phosphate-5-kinase Fab1p is essential for vacuole function inS. cerevisiae. Curr Biol 8: 1219–1222

    Article  PubMed  CAS  Google Scholar 

  • Cowles CR, Snyder WB, Burd CG, Emr SD (1997a) Novel Golgi to vacuole delivery pathway in yeast: identification of a sorting determinant and required transport component. EMBO J 16: 2769–2782

    Article  PubMed  CAS  Google Scholar 

  • —, Odorizzi G, Payne GS, Emr SD (1997b) The AP-3 adaptor complex is essential for cargo-selective transport to the yeast vacuole. Cell 91: 109–118

    Article  PubMed  CAS  Google Scholar 

  • Darsow T, Rieder SE, Emr SD (1997) A multispecificity syntaxin homologue, Vam3p, essential for autophagic and biosynthetic protein transport to the vacuole. J Cell Biol 138: 517–52

    Article  PubMed  CAS  Google Scholar 

  • —, Burd CG, Emr SD (1998) Acidic di-leucine motif essential for AP-3 dependent sorting and restriction of the functional specificity of the Vam3p vacuolar t-SNARE. J Cell Biol 142: 913–922

    Article  PubMed  CAS  Google Scholar 

  • Fleckenstein D, Rohde M, Klionsky DJ, Rüdiger M (1998) Vac8p, an armadillo repeat protein related to plakoglobin and importin α, is associated with the yeast vacuole membrane. J Cell Sci 111: 3109–3118

    PubMed  CAS  Google Scholar 

  • Gary JD, Wurmser AE, Bonangelino, CJ, Weisman LS, Emr SD (1998) Fab1p is essential for PtdIns(3)P-5-kinase activity and the maintenance of vacular size and membrane homeostasis. J Cell Biol 143: 65–79

    Article  PubMed  CAS  Google Scholar 

  • Geli MI, Riezman H (1998) Endocytic internalization in yeast and animal cells: similar and different. J Cell Sci 111: 1031–1037

    PubMed  CAS  Google Scholar 

  • Gerhardt B, Kordas TJ, Thompson CM, Patel P, Vida T (1998) The vesicle transport protein Vps33p is an ATP-binding protein that localizes to the cytosol in an energy-dependent manner. J Biol Chem 273: 15818–15829

    Article  PubMed  CAS  Google Scholar 

  • Götte M (1998) Genetic and two-hybrid interactions of yeastVPS33, aSEC1 family member involved in vacuolar protein transport. Mol Biol Cell 9 Suppl: 2731–2731

    Google Scholar 

  • —, Fischer von Mollard G (1998) A new beat for the SNARE drum. Trends Cell Biol 8: 215–218

    Article  PubMed  Google Scholar 

  • — Gallwitz D (1997) High expression of the yeast syntaxin-related Vam3 protein suppresses the protein-transport defects of apep12 null mutant. FEBS Lett 411: 48–52

    Article  PubMed  Google Scholar 

  • Haas A, Wickner W (1996) Homotypic vacuole fusion requires Sec17p (yeast α-SNAP) and Sec18p (yeast NSF). EMBO J 15: 3296–3305

    PubMed  CAS  Google Scholar 

  • —, Scheglmann D, Lazar T, Gallwitz D, Wickner W (1995) The GTPase Ypt7p ofSaccharomyces cerevisiae is required on both partner vacuoles for the homotypic fusion step in vacuole inheritance. EMBO J 14: 5258–5270

    PubMed  CAS  Google Scholar 

  • 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/NSF. Mol Biol Cell 8: 13–31

    PubMed  CAS  Google Scholar 

  • Huang P-H, Chiang H-L (1997) Identification of novel vesicles in the cytosol to vacuole protein degradation pathway. J Cell Biol 136: 803–810

    Article  PubMed  CAS  Google Scholar 

  • Jaquemin-Faure I, Thomas D, Laporte J, Cibert C, Surdin-Kerjan Y (1994) The vacuolar compartment is required for sulfur amino acid homeostasis inS. cerevisiae. Mol Gen Genet 244: 519–529

    Article  Google Scholar 

  • Klionsky DJ (1998) Nonclassical protein sorting to the yeast vacuole. J Biol Chem 273: 10807–10810

    Article  PubMed  CAS  Google Scholar 

  • Lazar T, Götte M, Gallwitz D (1997) Vesicular transport: how many Ypt/Rab-GTPases make a eukaryotic cell? Trends Biochem Sci 22: 468–472

    Article  PubMed  CAS  Google Scholar 

  • Löwe M, Nakamura N, Warren G (1998) Golgi division and membrane traffic. Trends Cell Biol 8: 40–44

    Article  PubMed  Google Scholar 

  • Mayer A, Wickner W (1997) Docking of yeast vacuoles is catalyzed by the Ras-like GTPase Ypt7p after symmetric priming by Sec18p (NSF). J Cell Biol 136: 307–317

    Article  PubMed  CAS  Google Scholar 

  • — Haas A (1996) Sec18p (NSF)-driven release of Sec17p (α-SNAP) can precede docking and fusion of yeast vacuoles. Cell 85: 83–94

    Article  PubMed  CAS  Google Scholar 

  • Nakamura N, Hirata A, Ohsumi Y, Wada Y (1997) Vam2/Vps41p and Vam6/Vps39p are components of a protein complex on the vacuolar membranes are involved in the vacuolar assembly in the yeastSaccharomyces cerevisiae. J Biol Chem 272: 11344–11349

    Article  PubMed  CAS  Google Scholar 

  • Nichols BJ, Ungermann C, Pelham HRB, Wickner WT, Haas A (1997) Homotypic vacuolar fusion mediated by t- and v-SNAREs. Nature 387: 199–202

    Article  PubMed  CAS  Google Scholar 

  • Nothwehr SF, Hindes AE (1997) The yeast VPS5/GRD2 gene encodes a sorting nexin-1-like protein required for localizing membrane proteins to the late Golgi. J Cell Sci 110: 1063–1072

    PubMed  CAS  Google Scholar 

  • Pan X, Goldfarb DS (1998)YEB3/VAC8 encodes a myristylated armadillo protein of theS. cerevisiae vacuolar membrane that functions in vacuole fusion and inheritance. J Cell Sci 111: 237–2147

    Google Scholar 

  • Peters C, Mayer A (1998) Ca2+/calmodulin signals the completion of docking and triggers a late step of vacuole fusion. Nature 396: 575–580

    Article  PubMed  CAS  Google Scholar 

  • Piper RC, Bryant NJ, Stevens TH (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

    Article  PubMed  CAS  Google Scholar 

  • Prescianotto-Baschong C, Riezman H (1998) Morphology of the yeast endocytic pathway. Mol Biol Cell 9: 173–189

    PubMed  CAS  Google Scholar 

  • Ramsay LM, Gadd GM (1997) Mutants ofS. cerevisiae defective in vacuolar function confirm a role for the vacuole in toxic metalion detoxification. FEMS Microbiol Lett 152: 293–298

    Article  PubMed  CAS  Google Scholar 

  • Raymond CK, Howald-Stevenson I, Vater CA, Stevens TH (1992) Morphological classification of the yeast vacuolar protein sorting mutants: evidence for a prevacuolar compartment in class Evps mutants. Mol Biol Cell 3: 1389–1402

    PubMed  CAS  Google Scholar 

  • Rieder SE, Emr SD (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

    PubMed  CAS  Google Scholar 

  • Robinson DG, Hinz G (1997) Vacuole biogenesis and protein transport to the plant vacuole: a comparison with the yeast vacuole and the mammalian lysosome. Protoplasma 197: 1–25

    Article  CAS  Google Scholar 

  • Sacher M, Jiang Y, Barrowman J, Scarpa A, Burston J, Zhang L, Schieltz D, Yates JR, Abeliovich H, Ferro-Novick S (1998) TRAPP, a highly conserved novel complex on the cis-Golgi that mediates vesicle docking and fusion. EMBO J 17: 2494–2503

    Article  PubMed  CAS  Google Scholar 

  • Sato TK, Darsow T, Emr SD (1998) Vam7p, a SNAP-25-like molecule, and Vam3p, a syntaxin homolog, function together in yeast vacuolar protein trafficking. Mol Cell Biol 18: 5308–5319

    PubMed  CAS  Google Scholar 

  • Seaman MNJ, Marcusson EG, Cereghino JL, Emr SD (1997) Endosome to Golgi retrieval of the vacuolar protein sorting receptor, Vps10p, requires the function of theVPS29, VPS30 andVPS35 gene products. J Cell Biol 137: 79–82

    Article  PubMed  CAS  Google Scholar 

  • —, McCaffery JM, Emr SD (1998) A membrane coat complex essential for endosome-to-Golgi retrograde transport in yeast. J Cell Biol 142: 665–681

    Article  PubMed  CAS  Google Scholar 

  • Shirahama K, Yazaki Y, Sakano K, Wada Y, Ohsumi Y (1996) Vacuolar function in the phosphate homestasis of the yeast S.cerevisiae. Plant Cell Physiol 37: 1090–1093

    PubMed  CAS  Google Scholar 

  • Singer-Krüger B, Frank R, Crausaz F, Riezman H (1993) Partial purification and characterization of early and late endosomes from yeast: identification of four novel proteins. J Biol Chem 268: 14376–14386

    PubMed  Google Scholar 

  • Srinivasan S, Seaman M, Nemoto Y, Daniell L, Suchy SF, Emr SD, DeCamilli P, Nussbaum R (1997) Disruption of 3-phosphatidyl-inositol-polyphosphate-5-phosphatase genes fromS. cerevisiae results in pleiotropic abnormalities of vacuole morphology, cell shape, and osmohomeostasis. Eur J Cell Biol 74: 350–360

    PubMed  CAS  Google Scholar 

  • Stack JH, Horazdovsky B, Emr SD (1995) Receptor-mediated protein sorting to the vacuole in yeast: roles for a protein kinase, a lipid kinase and GTP-binding proteins. Annu Rev Cell Dev Biol 11: 1–33

    Article  PubMed  CAS  Google Scholar 

  • Stepp JD, Huang K, Lemmon SK (1997) The yeast adaptor protein complex, AP-3, is essential for the efficient delivery of alkaline phosphatase by the alternate pathway to the vacuole. J Cell Biol 139: 1761–1774

    Article  PubMed  CAS  Google Scholar 

  • Szczypka MS, Zhu Z, Silar P, Thiele DJ (1997)S. cerevisiae mutants altered in vacuole function are defective in copper detoxification and iron-responsive gene transscription. Yeast 13: 1423–1435

    Article  PubMed  CAS  Google Scholar 

  • Tall GG, Hama H, De Wald DB, Horazdovsky BF (1999) The phosphatidyIinositol-3-phosphate binding protein Vaclp interacts with a Rab GTPase and a Sec1p homologue to facilitate vesicle-mediated vacuolar protein sorting. Mol Biol Cell 10: 1873–1889

    PubMed  CAS  Google Scholar 

  • TerBush DR, Maurice T, Roth D, Novick P (1996) The exocyst is a multiprotein complex required for exocytosis inS. cerevisiae. EMBO J 15: 6483–6494

    PubMed  CAS  Google Scholar 

  • Thatcher JW, Shaw JM, Dickinson WJ (1998) Marginal fitness contributions of non-essential genes in yeast. Proc Natl Acad Sci USA 95: 253–257

    Article  PubMed  CAS  Google Scholar 

  • Tsukada M, Gallwitz D (1996) Isolation and characterization ofSYS genes from yeast, multicopy suppressors of the functional loss of the transport GTPase Ypt6p. J Cell Sci 109: 2471–2481

    PubMed  CAS  Google Scholar 

  • —, Will E, Gallwitz D (1999) Structural and functional analysis of a novel coiled-coil protein involved in Ypt6 GTPase-regulated protein transport in yeast. Mol Biol Cell 10: 63–75

    PubMed  CAS  Google Scholar 

  • Tuttle DL, Dunn WA (1995) Divergent modes of autophagy in the methylotrophic yeastPichia pastoris. J Cell Sci 108: 25–35

    PubMed  CAS  Google Scholar 

  • Ungermann C, Wickner W (1998) Vam7p, a vacuolar SNAP-25 homologue, is required for SNARE complex integrity and vacuole docking and fusion. EMBO J 17: 3269–3276

    Article  PubMed  CAS  Google Scholar 

  • —, Nichols BJ, Pelham HRB, Wickner W (1998) A vacuolar v-t-SNARE complex, the predominant form in vivo and on isolated vacuoles, is disassembled and activated for docking and fusion. J Cell Biol 140: 61–69

    Article  PubMed  CAS  Google Scholar 

  • —, Fischer von Mollard G, Jensen ON, Margolis N, Stevens TH, 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: 1435–1442

    Article  PubMed  CAS  Google Scholar 

  • van den Hazel HB, Kielland-Brandt MC, Winther JR (1996) Review: Biosynthesis and function of yeast vacuolar proteases. Yeast 12: 1–16

    Article  Google Scholar 

  • Vollmer P, Will E, Scheglmann D, Strom M, Gallwitz D (1999) Primary structure and biochemical characterization of yeast GTPase-activating proteins with substrate preferences for the transport GTP-ase Ypt7p. Eur J Biochem 260: 284–290

    Article  PubMed  CAS  Google Scholar 

  • Wada Y, Anraku Y (1992) Genes for directing vacuolar morphogenesis inSaccharomyces cerevisiae II:VAM7, a gene for regulating morphogenic assembly of the vacuoles. J Biol Chem 267: 18671–18675

    PubMed  CAS  Google Scholar 

  • —, Ohsumi Y, Anraku Y (1992) Genes for directing vacuolar morphogenesis inSaccharomyces cerevisiae I: isolation and characterization of two classes ofvam mutants. J Biol Chem 267: 18665–18670

    PubMed  CAS  Google Scholar 

  • —, Kawai E, Ohsumi M (1996) Mutational analysis of Ypt7p function in the vacuolar biogenesis and morphogenesis in the yeast S.cerevisiae. Protoplasma 191: 126–135

    Article  CAS  Google Scholar 

  • —, Nakamura N, Ohsumi Y, Hirata A (1997) Vam3p, a new member of syntaxin related proteins, is required for vacuolar assembly in the yeastSaccharomyces cerevisiae. J Cell Sci 110: 1299–1306

    PubMed  CAS  Google Scholar 

  • Wang Y-X, Catlett NL, Weisman LS (1998) Vac8p, a vacuolar protein with armadillo repeats, functions in both vacuole inheritance and protein targeting from the cytoplasm to vacuole. J Cell Biol 140: 1063–1074

    Article  PubMed  CAS  Google Scholar 

  • Wichmann H, Hengst L. Gallwitz D (1992) Endocytosis in yeast: evidence for the involvement of a small GTP-binding protein (Ypt7p). Cell 71: 1131–1142

    Article  PubMed  CAS  Google Scholar 

  • Wilsbach K, Payne GS (1993) Dynamic retention of TGN membrane proteins inSaccharomyces cerevisiae. Trends Cell Biol 3: 426–432

    Article  PubMed  CAS  Google Scholar 

  • Wurmser AE, Emr SD (1998) Phosphoinositide signaling and turnover: PtdIns(3)P, a regulator of membrane traffic, is transported to the vacuole and degraded by a process that requires lumenal vacuolar hydrolase activities. EMBO J 17: 4930–4942

    Article  PubMed  CAS  Google Scholar 

  • Xu Z, Mayer A, Muller E, Wickner W (1997) A heterodimer of thioredoxin and IB 2 cooperates with Sec18p (NSF) to promote yeast vacuole inheritance. J Cell Biol 136: 299–306

    Article  PubMed  CAS  Google Scholar 

  • —, Sato K, Wickner W (1998) LMA1 binds to vacuoles at Sec18p (NSF), transfers upon ATP hydrolysis to a t-SNARE (Vam3p) complex, and is released during fusion. Cell 93: 1125–1134

    Article  PubMed  CAS  Google Scholar 

  • Yuan DS, Dancis A, Klausner RD (1997) Restriction of copper export inSaccharomyces cerevisiae to a late Golgi or post-Golgi compartment in the secretory pathway. J Biol Chem 272: 25787–25793

    Article  PubMed  CAS  Google Scholar 

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Götte, M., Lazar, T. The ins and outs of yeast vacuole trafficking. Protoplasma 209, 9–18 (1999). https://doi.org/10.1007/BF01415696

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