The Vps4p AAA ATPase regulates membrane association of a Vps protein complex required for normal endosome function

EMBO Journal

Volumn 17, Issue 11, 1998, Pages 2982-2993

  Babst, Markus ^a   Wendland, Beverly ^a   Estepa, Eden J ^a   Emr, Scott D ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

ATPase; Endosome; Transport; Vacuole

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; DIMER; MEMBRANE PROTEIN;

ARTICLE; CELL STRUCTURE; CONTROLLED STUDY; DELETION MUTANT; ENDOSOME; HYDROLYSIS; IMMUNOFLUORESCENCE; MEMBRANE TRANSPORT; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; SACCHAROMYCES CEREVISIAE;

ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; DIMERIZATION; ENDOSOMES; ENZYME ACTIVATION; FUNGAL PROTEINS; INTRACELLULAR MEMBRANES; MACROMOLECULAR SUBSTANCES; NUCLEAR PROTEINS; NUCLEOTIDES; POLYMERS; PROTEIN BINDING; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SUBCELLULAR FRACTIONS;

SACCHAROMYCES CEREVISIAE;

EID: 0032101334     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/17.11.2982     Document Type: Article

References (55)

1. Arlt, H., Tauer, R., Feldmann, H., Neupert, W. and Langer, T. (1996) The YTA10-12 complex, an AAA protease with chaperone-like activity in the inner membrane of mitochondria. Cell, 85, 875-885.
2. Babst, M., Sato, T.K., Banta, L.M. and Emr, S.E. (1997) Endosomal transport function in yeast requires a novel AAA-type ATPase, Vps4p. EMBO J., 16, 1820-1831.
3. Becherer, K.A., Reider, S., 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.
4. Beckers, C.J., Block, M.R., Glick, B.S., Rothman, J.E. and Balch, W.E. (1989) Vesicular transport between the endoplasmic reticulum and the Golgi stack requires the NEM-sensitive fusion protein. Nature, 339, 397-398.
5. Beyer, A. (1997) Sequence analysis of the AAA protein family. Protein Sci., 6, 2043-2058.
6. Bock, J.B., Klumperman, J., Davanger, S. and Scheller, R.H. (1997) Syntaxin 6 functions in trans-Golgi network vesicle trafficking. Mol. Biol. Cell, 8, 1261-1271.
7. Burd, C.G., Mustol, P.A., Schu, P.V. and Emr, S.D. (1996) A yeast protein related to a mammalian Ras-binding protein, Vps9p, is required for localization of vacuolar proteins. Mol. Cell. Biol., 16, 2369-2377.
8. Burd, C.G., Peterson, M., Cowles, C.R. and Emr, S.D. (1997) A novel Sec18p/NSF-dependent complex required for Golgi-to-endosome transport in yeast. Mol. Biol. Cell, 8, 1089-1104.
9. Cereghino, J.L., Marcusson, E.G. and Emr, S.D. (1995) The cytoplasmic tail domain of the vacuolar sorting receptor Vps10p and a subset of VPS gene products regulate receptor stability, function and localization. Mol. Biol. Cell, 6, 1089-1102.
10. Christianson, T.W., Sikorski, R.S., Dante, M., Shero, J.H. and Hieter, P. (1992) Multifunctional yeast high-copy-number shuttle vectors. Gene, 110, 119-122.
11. Confalonieri, F. and Duguet, M. (1995) A 200-amino acid ATPase module in search of a basic function. BioEssays, 17, 639-650.
12. Daro, E., Sheff, D., Gomez, M., Kreis, T. and Mellman, I. (1997) Inhibition of endosome function in CHO cells bearing a temperature-sensitive defect in the coatomer (COPI) component epsilon-COP. J. Cell Biol., 139, 1747-1759.
13. Dieckmann, C.L. and Tzagoloff, A. (1985) Assembly of the mitochondrial membrane system. CBP6, a yeast nuclear gene necessary for synthesis of cytochrome b. J. Biol. Chem., 260, 1513-1520.
14. Finken-Eigen, M., Rohricht, R.A. and Kohrer, K. (1997) The VPS4 gene is involved in protein transport out of a yeast pre-vacuolar endosome-like compartment. Curr. Genet., 31, 469-480.
15. Frohlich, K.U., Fries, H.W., Peters, J.M. and Mecke, D. (1995) The ATPase activity of purified CDC48p from Saccharomyces cerevisiae shows complex dependence on ATP-, ADP-, and NADH-concentrations and is completely inhibited by NEM. Biochim. Biophys. Acta, 1253, 25-32.
16. Graham, T.R. and Emr, S.D. (1991) Compartmental organization of Golgi-specific protein modification and vacuolar protein sorting events defined in a yeast sec18 (NSF) mutant. J. Cell Biol., 114, 207-218.
17. Gruenberg, J. and Maxfield, F. (1995) Membrane transport in the endocytic pathway. Curr. Opin. Cell Biol., 7, 552-563.
18. Hanson, P.I., Roth, R., Morisaki, H., Jahn, R. and Heuser, J.E. (1997) Structure and conformational changes in NSF and its membrane receptor complexes visualized by quick-freeze/deep-etch electron microscopy. Cell, 90, 523-535.
19. Harlow, E. and Lane, D.L. (1988) Antibodies: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
20. Hay, J.C. and Scheller, R.H. (1997) SNAREs and NSF in targeted membrane fusion. Curr. Opin. Cell Biol., 9, 505-512.
21. Hicke, L., Zanolari, B., Pypaert, M., Rohrer, J., Riezman, H., TerBush, D.R., Maurice, T., Roth, D. and Novick, P. (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.
22. Horazdovsky, B.F. and Emr, S.D. (1993) The VPS16 gene product associates with a sedimentable protein complex and is essential for vacuolar protein sorting in yeast. J. Biol. Chem., 268, 4953-4962.
23. Ito, H., Fukuda, Y., Murata, K. and Kimura, A. (1983) Transformation of intact yeast cells treated with alkali cations. J. Bacteriol., 153, 163-168.
24. Jones, E.W. (1977) Proteinase mutants of Saccharomyces cerevisiae. Genetics, 85, 23-33.
25. Komada, M. and Kitamura, N. (1994) Regulatory role of major tyrosine autophosphorylation site of kinase domain of c-Met receptor (scatter factor/hepatocyte growth factor receptor). J. Biol. Chem., 269, 16131-16136.
26. Komada, M., Masaki, R., Yamamoto, A. and Kitamura, N. (1997) Hrs, a tyrosine kinase substrate with a conserved double zinc ringer domain, is localized to the cytoplasmic surface of early endosomes. J. Biol. Chem., 272, 20538-20544.
27. Lenhard, J.M., Kahn, R.A. and Stahl, P.D. (1992) Evidence for ADP-ribosylation factor (ARF) as a regulator of in vitro endosome-endosome fusion. J. Biol. Chem., 267, 13047-13052.
28. Lupas, A., Van Dyke, M. and Stock, J. (1991) Predicting coiled coils from protein sequences. Science, 252, 1162-1164.
29. Miller, J. (1972) Experiments in Molecular Genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
30. Muhlberg, A.B., Warnock, D.E. and Schmid, S.L. (1997) Domain structure and intramolecular regulation of dynamin GTPase. EMBO J., 16, 6676-6683.
31. Mukhopadhyay, A., Funato, K. and Stahl, P.D. (1997) Rab7 regulates transport from early to late endocytic compartments in Xenopus oocytes. J. Biol. Chem., 272, 13055-13059.
32. Nagiec, E.E., Bernstein, A. and Whiteheart, S.W. (1995) Each domain of the N-ethylmaleimide-sensitive fusion protein contributes to its transport activity. J. Biol. Chem., 270, 29182-29188.
33. Novick, P. and Zerial, M. (1997) The diversity of Rab proteins in vesicle transport. Curr. Opin. Cell Biol., 9, 496-504.
34. Patel, S. and Latterich, M. (1998) The AAA team: related ATPases with diverse functions. Trends Cell Biol., 8, 65-71.
35. Perier, F. Coulter, K.L., Liang, H., Radeke, C.M., Gaber, R.F. and Vandenberg, C.A. (1994) Identification of a novel mammalian member of the NSF/CDC48p/Pas1p/TBP-1 family through heterologous expression in yeast. FEBS Lett., 351, 286-290.
36. Peters, J.M., Walsh, M.J. and Franke, W.W. (1990) An abundant and ubiquitous homo-oligomeric ring-shaped ATPase particle related to the putative vesicle fusion proteins Sec18p and NSF. EMBO J., 9, 1757-1767.
37. Piper, R.C., Cooper, A.A., Yang, H. and Stevens, T.H. (1995) VPS27 controls vacuolar and endocytic traffic through a prevacuolar compartment in Saccharomyces cerevisiae. J. Cell. Biol., 131, 603-618.
38. Raymond, C.K., Howald-Stevenson, I., Vater, C.A. and 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.
39. 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. Mol. Biol. Cell, 7, 985-999.
40. 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.
41. Robinson, L.J., Aniento, F. and Gruenberg, J. (1997) NSF is required for transport from early to late endosomes. J. Cell Sci., 110, 2079-2087.
42. Rodriguez, L., Stirling, C.J. and Woodman, P.G. (1994) Multiple N-ethylmaleimide-sensitive components are required for endosomal vesicle fusion. Mol. Biol. Cell, 5, 773-783.
43. Rothman, J.H., Howald, I. and Stevens, T.H. (1989) Characterization of genes required for protein sorting and vacuolar function in the yeast Saccharomyces cerevisiae. EMBO J., 8, 2057-2065.
44. Rybin, V., Ullrich, O., Rubino, M., Alexandrov, K., Simon, I., Seabra, C., Goody, R. and Zerial, M. (1996) GTPase activity of Rab5 acts as a timer for endocytic membrane fusion. Nature, 383, 266-269.
45. Sambrook, J., Fritsch, E.F. and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
46. 32P]ATP/dATP. J. Biol. Chem., 260, 13831-13837.
47. 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.
48. Shirahama, K., Noda, T. and Ohsumi, Y. (1997) Mutational analysis of Csc1/Vps4p: involvement of endosome in regulation of autophagy in yeast. Cell Struct. Funct., 22, 501-509.
49. Sudhof, T.C. (1995) The synaptic vesicle cycle: a cascade of protein-protein interactions. Nature, 375, 645-653.
50. Takei, K., McPherson, P.S., Schmid, S.L. and De Camilli, P. (1995) Tubular membrane invaginations coated by dynamin rings are induced by GTP-γ S in nerve terminals. Nature, 374, 186-190.
51. Tu, J., Vallier, L.G. and Carlson, M. (1993) Molecular and genetic analysis of the SNF7 gene in Saccharomyces cerevisiae. Genetics, 135, 17-23.
52. Ullrich, O., Reinsch, S., Urbe, S., Zerial, M. and Parton, R.G. (1996) Rab11 regulates recycling through the pericentriolar recycling endosome. J. Cell Biol., 135, 913-924.
53. Warnock, D.E., Hinshaw, J.E. and Schmid, S.L. (1996) Dynamin self-assembly stimulates its GTPase activity. J. Biol. Chiem., 271, 22310-22314.
54. Whiteheart, S.W., Rossnagel, K., Buhrow, S.A., Brunner, M., Jaenicke, R. and Rothman, J.E. (1994) N-ethylmaleimide-sensitive fusion protein: a trimeric ATPase whose hydrolysis of ATP is required for membrane fusion. J. Cell Biol., 126, 945-954.
55. Whitney, J.A., Gomez, M., Sheff, D., Kreis, T.E. and Mellman, I. (1995) Cytoplasmic coat proteins involved in endosome function. Cell, 83, 703-713.