Cytoplasm to vacuole trafficking of aminopeptidase I requires a t-SNARE-Sec1p complex composed of Tlg2p and Vps45p

EMBO Journal

Volumn 18, Issue 21, 1999, Pages 6005-6016

  Abeliovich, Hagai ^a   Darsow, Tamara ^a   Emr, Scott D ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

Autophagy; Cvt; Rapamycin; Sec1p; Tlg2 t SNARE

Indexed keywords

AMINOPEPTIDASE I; ENZYME PRECURSOR; SYNTAXIN;

ARTICLE; AUTOPHAGY; CELL VACUOLE; COMPLEX FORMATION; CYTOPLASM; LYSOSOME; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN TRANSPORT; YEAST;

AMINOPEPTIDASES; AUTOPHAGY; FUNGAL PROTEINS; LYSOSOMES; MEMBRANE PROTEINS; MEMBRANE TRANSPORT PROTEINS; MICROSCOPY, ELECTRON; MUNC18 PROTEINS; MUTATION; NERVE TISSUE PROTEINS; PROTEIN PRECURSORS; QA-SNARE PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SIROLIMUS; SNARE PROTEINS; VACUOLES; VESICULAR TRANSPORT PROTEINS;

EID: 0033231275     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/18.21.6005     Document Type: Article

References (53)

1. Abeliovich, H., Grote, E., Novick, P. and Ferro-Novick, S. (1998) Tlg2p, a yeast syntaxin homolog that resides on the Golgi and endocytic structures. J. Biol. Chem., 273, 11719-11727.
2. Baba, M., Takeshige, K., Baba, N. and Ohsumi, Y. (1994) Ultrastructural analysis of the autophagic process in yeast: detection of autophagosomes and their characterization. J. Cell Biol., 124, 903-913.
3. Baba, M., Osumi, M., Scott, S.V., Klionsky, D.J. and Ohsumi, Y. (1997) Two distinct pathways for targeting proteins from the cytoplasm to the vacuole/lysosome. J. Cell Biol., 139, 1687-1695.
4. Babst, M., Sato, T.K., Banta, L.M. and Emr, S.D. (1997) Endosomal transport function in yeast requires a novel AAA-type ATPase, Vps4p. EMBO J., 16, 1820-1831.
5. 1 progression in yeast. Mol. Biol. Cell, 7, 25-42.
6. Becherer, K.A., Rieder, S.E., Emr, S.D. and Jones, E.W. (1996) Novel syntaxin homologue. Pep12p, required for the sorting of lumenal hydrolases to the lysosome-like vacuole in yeast. Mol. Biol. Cell, 7, 579-594.
7. Burd, C.G., Peterson, M., Cowles, C.R. and Emr, S.D. (1997) A novel Sec 18p/NSF-dependent complex required for Golgi to endosome transport in yeast. Mol. Biol. Cell, 8, 1089-1104.
8. Coe, J.G.S., Lim, A.B.C., Xu, J. and Hong, W. (1999) A role for TIg1p in the transport of proteins within the Golgi apparatus of Saccharomyces cerevisiae. Mol. Biol. Cell, 10, 2407-2423.
9. Cowles, C.R., Emr, S.D. and Horazdovsky, B.F. (1994) Mutations in the VPS45 gene, a SEC1 homolog, result in vacuolar protein sorting defects and accumulation of membrane vesicles. J. Cell Sci., 107, 3449-3459.
10. Cowles, C.R., Odorizzi, G., Payne, G.S. and Emr, S.D. (1997a) The AP-3 adaptor protein complex is essential for cargo-selective transport to the yeast vacuole. Cell, 91, 109-118.
11. Cowles, C.R., Snyder, W.B., Burd, C.G. and Emr, S.D. (1997b) Novel Golgi to vacuole delivery pathway in yeast: identification of a sorting determinant and required transport component. EMBO J., 16, 2769-2782.
12. Darsow, T., Rieder, S.E. and Emr, S.D. (1997) A multispecificity syntaxin homolog, Vam3p. Essential for autophagic and biosynthetic protein transport to the vacuole. J. Cell Biol., 138, 517-529.
13. Egner, R., Thumm, M., Straub, M., Simeon, A., Schuller, H.J. and Wolf, D.H. (1993) Tracing intracellular proteolytic pathways. Proteolysis of fatty acid synthase and other cytoplasmic proteins in the yeast Saccharomyces cerevisiae. J. Biol. Chem., 268, 27269-27276.
14. Fischer von Mollard, G., Nothwehr, S.F. and Stevens, T.H. (1997) The yeast v-SNARE Vti 1p mediates two vesicle transport pathways through interactions with the t-SNAREs Sed5p and Pep12p. J. Cell Biol., 137, 1511-1524.
15. Fischer von Mollard, G. and Stevens, T.H. (1999) The Saccharomyces cerevisiae v-SNARE Vti 1p is required for multiple membrane transport pathways to the vacuole. Mol. Biol. Cell, 10, 1719-1732.
16. Guthrie, C. and Fink, G.R. (eds) (1991) Guide to Yeast Genetics and Molecular Biology. Academic Press, New York, NY.
17. Harding, T.M., Morano, K.A., Scott, S.V. and Klionsky, D.J. (1995) Isolation and characterization of yeast mutants in the cytoplasm to vacuole protein targeting pathway. J. Cell Biol., 131, 591-602.
18. Harding, T.M., Hefner-Gravink, A., Thumm, M. and Klionsky, D.J. (1996) Genetic and phenotypic overlap between autophagy and the cytoplasm to vacuole protein targeting pathway. J. Biol. Chem., 271, 17621-17624.
19. Hicke, L., Zanolari, B., Pypaert, M., Rohrer, J. and Riezmann, 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.
20. Holthuis, J.C.M., Nichols, B.J., Dhruvakumar, S. and Pelham, H.R.B. (1998) Two syntaxin homologs in the TGN/endosomal system of yeast. EMBO J., 17, 113-126.
21. Kim, J., Scott, S.V., Oda, M. and Klionsky, D.J. (1997) Transport of a large oligomeric protein by the cytoplasm to vacuole protein degradation pathway. J. Cell Biol., 137, 609-618.
22. Kim, J., Dalton, V.M., Eggerton, K.P., Scott, S.V. and Klionsky, D.J. (1999) Apg7p/Cvt2p is required for the Cvt, macroautophagy and peroxisomal degradation pathways. Mol. Biol. Cell, 10, 1337-1351.
23. Klionsky, D. (1998) Nonclassical protein sorting to the vacuole. J. Biol. Chem., 273, 10807-10810.
24. Klionsky, D.J. and Emr, S.D. (1989) Membrane protein sorting: biosynthesis, transport and processing of yeast vacuolar alkaline phosphatase. EMBO J., 8, 2241-2250.
25. Klionsky, D.J., Banta, L.M. and Emr, S.D. (1988) Intracellular sorting and processing of a yeast vacuolar hydrolase: proteinase A propeptide contains vacuolar targeting information. Mol. Cell. Biol., 8, 2105-2116.
26. Klionsky, D.J., Herman, P.K. and Emr, S.D. (1990) The fungal vacuole: composition, function and biogenesis. Microbiol. Rev., 54, 266-292.
27. Klionsky, D.J., Cueva, R. and Yaver, D.S. (1992) Aminopeptidase I of Saccharomyces cerevisiae is localized to the vacuole independent of the secretory pathway. J. Cell Biol., 119, 287-299.
28. Maniatis, T., Fritsch, E.F. and Sambrook, J. (1982) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
29. Miller, J. (1972) Experiments in Molecular Genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
30. Nichols, B.J., Ungermann, C., Pelham, H.R., Wickner, W.T. and Haas, A. (1997) Homotypic vacuolar fusion mediated by t- and v-SNAREs. Nature, 387, 199-202.
31. Nichols, B.J., Holthuis, J.C. and Pelham, H.R. (1998) The Sec1p homologue Vps45p binds to the syntaxin Tlg2p. Eur. J. Cell Biol., 77, 263-268.
32. Noda, T. and Ohsumi, Y. (1998) Tor, a phosphatidylinositol kinase homologue, controls autophagy in yeast. J. Biol. Chem., 273, 3963-3966.
33. Patel, S.K., Indig, F.E., Olivieri, N., Levine, N.D. and Latterich, M. (1998) Organelle membrane fusion: a novel function for the syntaxin homolog Ufe 1p in ER membrane fusion. Cell, 92, 611-620.
34. Pevsner, J., Hsu, S., Braun, J.E.A., Calakos, N., Ting, A.E., Bennet, M.K. and Scheller, R.H. (1994) Specificity and regulation of a synaptic vesicle docking complex. Neuron, 13, 353-361.
35. Pfeffer, S.R. (1996) Transport vesicle docking: SNAREs and associates. Annu. Rev. Cell Dev. Biol., 12, 441-461.
36. Rabouille, C., Kondo, H., Newman, R., Hui, N., Freemont, P. and Warren, G. (1998) Syntaxin 5 is a common component of the NSF- and p97-mediated reassembly pathways of Golgi cisternae from mitotic Golgi fragments in vitro. Cell, 92, 603-610.
37. Rieder, S.E., Banta, L.M., Kohrer, K., McCaffery, J.M. and Emr, S.D. (1996) Multilamellar endosome-like compartment accumulates in the yeast vps28 vacuolar protein sorting mutant. Mol. Biol. Cell, 7, 985-999.
38. Robinson, J.S., Klionsky, D.J., Banta, L.M. and Emr, S.D. (1988) Protein sorting in Saccharomyces cerevisiae: isolation of mutants defective in the delivery and processing of multiple vacuolar hydrolases. Mol. Cell. Biol., 8, 4936-4948.
39. Rothman, J.E. and Wieland, F.T. (1996) Protein sorting by transport vesicles. Science, 272, 227-234.
40. Scott, S.V. and Klionsky, D. (1995) In vitro reconstitution of cytoplasm to vacuole targeting in yeast. J. Cell Biol., 131, 1727-1735.
41. Scott, S.V., Hefner-Gravink, A., Morano, K.A., Noda, T., Ohsumi, Y. and Klionsky, D.J. (1996) Cytoplasm-to-vacuole targeting and autophagy employ the same machinery to deliver proteins to the yeast vacuole. Proc. Natl Acad. Sci. USA, 93, 12304-12308.
42. Scott, S.V., Baba, M., Ohsumi, Y. and Klionsky, D.J. (1997) Amino-peptidase I is targeted to the vacuole by a nonclassical vesicular mechanism. J. Cell Biol., 138, 37-44.
43. Seron, K. et al. (1998) A yeast t-SNARE involved in endocytosis. Mol. Biol. Cell, 9, 2873-2879.
44. Sherman, F., Fink, G.R. and Lawrence, L.W. (1979) Methods in Yeast Genetics: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
45. Sogaard, M., Tani, K., Ye, R.R., Geromanos, S., Tempst, P., Kirchhausen, T., Rothman, J.E. and Sollner, T. (1994) A rab protein is required for the assembly of SNARE complexes in the docking of transport vesicles. Cell, 78, 937-948.
46. Sollner, T., Whiteheart, S.W., Brunner, M., Erdjument-Bromage, H., Geromanos, S., Tempst, P. and Rothman, J.E. (1993) SNAP receptors implicated in vesicle targeting and fusion. Nature, 362, 318-324.
47. Takeshige, K., Baba, M., Tsuboi, S., Noda, T. and Ohsumi, Y. (1992) Autophagy in yeast demonstrated with proteinase-deficient mutants and conditions for its induction. J. Cell Biol., 119, 301-311.
48. Thumm, M., Egner, R., Koch, B., Schlumpberger, M., Straub, M., Veenhuis, M. and Wolf, D.H. (1994) Isolation of autophagocytosis mutants of Saccharomyces cerevisiae. FEBS Lett., 349, 275-280.
49. Tsukada, M. and Ohsumi, Y. (1993) Isolation and characterization of autophagy-defective mutants of Saccharomyces cerevisiae. FEBS Lett., 333, 169-174.
50. Ungermann, C., Sato, K. and Wickner, W. (1998) Defining the functions of trans-SNARE pairs. Nature, 396, 543-548.
51. Vida, T., Huyer, A.G. and Emr, S.D. (1993) Yeast vacuolar proenzymes are sorted in the late Golgi complex and transported to the vacuole via a prevacuolar endosome-like compartment. J. Cell Biol., 121, 1245-1256.
52. Weimbs, T., Hui Low, S., Chapin, S.J., Mostov, K.E., Bucher, P. and Hoffman, K. (1997) A conserved domain is present in different family members of vesicular fusion proteins: a new superfamily. Proc. Natl Acad. Sci. USA, 94, 3046-3051.
53. 0 program of transcriptional repression in yeast by interfering with the TOR signaling pathway. Mol. Cell. Biol., 18, 4463-4470.