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 Journal

Volumn 17, Issue 17, 1998, Pages 4930-4942

  Wurmser, Andrew E ^a   Emr, Scott D ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Endocytosis; Endosome; Phosphatidylinositol 3 kinase; Proteinase; VPS34

Indexed keywords

HYDROLASE; INOSITOL TRISPHOSPHATE; PHOSPHATASE; PHOSPHATIDYLINOSITIDE; TRIACYLGLYCEROL LIPASE;

ARTICLE; CELL VACUOLE; CONTROLLED STUDY; ENDOSOME; ENZYME ACTIVITY; GENE MUTATION; MEMBRANE TRANSPORT; NONHUMAN; PHOSPHOINOSITIDE METABOLISM; PRIORITY JOURNAL;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ALKALINE PHOSPHATASE; BIOLOGICAL TRANSPORT; CELL COMPARTMENTATION; ENDOCYTOSIS; FUNGAL PROTEINS; GTP PHOSPHOHYDROLASES; GTP-BINDING PROTEINS; HYDROLASES; MEMBRANE PROTEINS; PHOSPHATIDYLINOSITOL PHOSPHATES; QA-SNARE PROTEINS; RAB GTP-BINDING PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SIGNAL TRANSDUCTION; SNARE PROTEINS; VACUOLES; VESICULAR TRANSPORT PROTEINS;

EID: 0032168684     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/17.17.4930     Document Type: Article

References (69)

1. Attree, O., Olivos, I.M., Okabe, I., Bailey, L.C., Nelson, D.L., Lewis, R.A., McInnes, R.R. and Nussbaum, R.L. (1992) The Lowe's oculocerebrorenal syndrome gene encodes a protein highly homologous to inositol polyphosphate-5-phosphatase. Nature, 358, 239-242.
2. 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.
3. Banta, L.M., Robinson, J.S., Klionsky, D.J. and Emr, S.D. (1988) Organelle assembly in yeast: characterization of yeast mutants defective in vacuolar biogenesis and protein sorting. J. Cell Biol., 107, 1369-1383.
4. Banta, L.M., Vida, T.A., Herman, P.K. and Emr, S.D. (1990) Characterization of yeast Vps33p, a protein required for vacuolar protein sorting and vacuole biogenesis. Mol. Cell. Biol., 10, 638-4649.
5. Brown, W.J., DeWald, D.B., Emr, S.D., Plutner, H. and Balch, W.E. (1995) Role for phosphatidylinositol 3-kinase in the sorting and transport of newly synthesized lysosomal enzymes in mammalian cells. J. Cell Biol., 130, 781-796.
6. Browne, B.L., McClendon, V. and Bedwell, D.M. (1996) Mutations within the first LSGGQ motif of Ste6p cause defects in a-factor transport and mating in Saccharomyces cerevisiae. J. Bacteriol., 178, 1712-1719.
7. 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.
8. Caldwell, K.K., Lips, D.L., Bansal, V.S. and Majerus, P.W. (1991) Isolation and characterization of two 3-phosphatases that hydrolyze both phosphatidylinositol 3-phosphate and inositol, 1,3-bisphosphate. J. Biol. Chem., 266, 18378-18386.
9. Cowles, C.R., Odorizzi, G., Payne, G.S. and Emr, S.D. (1997a) The AP-3 adaptor complex is essential for cargo-selective transport to the yeast vacuole. Cell, 91, 109-118.
10. 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.
11. Darsow, T., Rieder, S.E. and Emr, S.D. (1997) A multispecificity syntaxin homologue, Vam3p, essential for autophagic and biosynthetic protein transport to the vacuole. J. Cell Biol., 138, 517-529.
12. Davidson, H.W. (1995) Wortmannin causes mistargeting of procathepsin D. evidence for the involvement of a phosphatidylinositol 3-kinase in vesicular transport to lysosomes. J. Cell Biol., 130, 797-805.
13. Dove, S.K., Cooke, F.T., Douglas, M.R., Sayers, L.G., Parker, P.J. and Michell, R.H. (1997) Osmotic stress activates phosphatidylinositol-3,5-bisphosphate synthesis. Nature, 390, 187-192.
14. Felder, S., Miller, K., Moehren, G., Ullrich, A., Schlessinger, J. and Hopkins, C.R. (1990) Kinase activity controls the sorting of the epidermal growth factor receptor within the multivesicular body. Cell, 61, 623-634.
15. Franke, T.F., Kaplan, D.R., Cantley, L.C. and Toker, A. (1997) Direct regulation of the Akt proto-oncogene product by phosphatidylinositol-3,4-bisphosphate. Science, 275, 665-668.
16. Futter, C.E., Pearse, A., Hewlett, L.J. and Hopkins, C.R. (1996) Multivesicular endosomes containing internalized EGF-EGF receptor complexes mature and then fuse directly with lysosomes. J. Cell Biol., 132, 1011-1023.
17. Gruenberg, J. and Maxfield, F.R. (1995) Membrane transport in the endocytic pathway. Curr. Opin. Cell Biol., 7, 552-563.
18. Hanahan, D. (1983) Studies on transformation of Escherichia coli with plasmids. J. Mol. Biol., 166, 557-580.
19. Herman, P.K. and Emr, S.D. (1990) Characterization of VPS34, a gene required for vacuolar protein sorting and vacuole segregation in Saccharomyces cerevisiae. Mol. Cell. Biol., 10, 6742-6754.
20. Herman, P.K., Stack, J.H., DeModena, J.A. and Emr, S.D. (1991) A novel protein kinase homolog essential for protein sorting to the yeast lysosome-like vacuole. Cell, 64, 425-437.
21. Hirsch, H.H., Schiffer, H.H. and Wolf, D.H. (1992) Biogenesis of the yeast vacuole (lysosome). Proteinase yscB contributes molecularly and kinetically to vacuolar hydrolase-precursor maturation. Eur. J. Biochem., 207, 867-876.
22. Ho, M.N., Hill, K.J., Lindorfer, M.A. and Stevens, T.H. (1993) Isolation of vacuolar membrane H (+)-ATPase-deficient yeast mutants; the VMA5 and VMA4 genes are essential for assembly and activity of the vacuolar H (+)-ATPase. J. Biol. Chem., 268, 221-227.
23. Horazdovsky, B.F., Busch, G.R. and Emr, S.D. (1994) VPS21 encodes a rab5-like GTP binding protein that is required for the sorting of yeast vacuolar proteins. EMBO J., 13, 1297-1309.
24. Ito, H., Fukuda, Y., Murata, K. and Kimura, A. (1983) Transformation of intact yeast cells treated with alkali cations. J. Bacteriol., 153, 163-168.
25. Kean, L.S., Fuller, R.S. and Nichols, J.W. (1993) Retrograde lipid traffic in yeast: identification of two distinct pathways for internalization of fluorescent-labeled phosphatidylcholine from the plasma membrane. J. Cell Biol., 123, 1403-1419.
26. 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.
27. 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.
28. Klionsky, D.J., Herman, P.K. and Emr, S.D. (1990) The fungal vacuole: composition, function and biogenesis. Microbiol. Rev., 54, 266-292.
29. Kobayashi, T., Stang, E., Fang, K.S., de Moerloose, P., Parton, R.G. and Gruenberg, J. (1998) A lipid associated with the antiphospholipid syndrome regulates endosome structure and function. Nature, 392, 193-197.
30. Kolling, R. and Hollenberg, C.P. (1994) The ABC-transporter Ste6 accumulates in the plasma membrane in a ubiquitinated form in endocytosis mutants. EMBO J., 13, 3261-3271.
31. Li, G., D'Souza-Schorey, C., Barbieri, M.A., Roberts, R.L., Klippel, A., Williams, L.T. and Stahl, P.D. (1995) Evidence for phosphatidylinositol 3-kinase as a regulator of endocytosis via activation of Rab5. Proc. Natl Acad. Sci. USA, 92, 10207-10211.
32. Maniatis, T., Fritsch, E.F. and Sambrook, J. (1982) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
33. McPherson, P.S. et al. (1996) A presynaptic inositol-5-phosphatase. Nature, 379, 353-357.
34. Morano, K.A. and Klionsky, D.J. (1994) Differential effects of compartment deacidification on the targeting of membrane and soluble proteins to the vacuole in yeast. J. Cell Sci., 107, 2813-2824.
35. Munn, A.L. and Riezman, H. (1994) Endocytosis is required for the growth of vacuolar H (+)-ATPase-defective yeast: identification of six new END genes. J. Cell Biol., 127, 373-386.
36. Novick, P., Field, C. and Schekman, R. (1980) Identification of 23 complementation groups required for post-translational events in the yeast secretory pathway. Cell, 21, 205-215.
37. Patki, V., Virbasius, J., Lane, W.S., Toh, B.H., Shpetner, H.S. and Corvera, S. (1997) Identification of an early endosomal protein regulated by phosphatidylinositol 3-kinase. Proc. Natl Acad. Sci. USA, 94, 7326-7330.
38. Piper, R.C., Bryant, N.J. and 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.
39. 3 interacts with SH2 domains and modulates PI 3-kinase association with tyrosine-phosphorylated proteins. Cell, 83, 821-830.
40. Rapoport, I., Miyazaki, M., Boll, W., Duckworth, B., Cantley, L.C., Shoelson, S. and Kirchhausen, T. (1997) Regulatory interactions in the recognition of endocytic sorting signals by AP-2 complexes. EMBO J., 16, 2240-2250.
41. Raths, S., Rohrer, J., Crausaz, F. and Riezman, H. (1993) end3 and end4: two mutants defective in receptor-mediated and fluid-phase endocytosis in Saccharomyces cerevisiae. J. Cell Biol., 120, 55-65.
42. 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.
43. Rhee, S.G. (1991) Inositol phospholipids-specific phospholipase C: interaction of the gamma l isoform with tyrosine kinase. Trends Biochem, Sci., 16, 297-301.
44. 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.
45. 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.
46. Sandhoff, K. and Kolter, T. (1996) Topology of glycosphingolipid degradation. Trends Cell Biol., 6, 98-103.
47. Schimmoller, F. and Riezman, H. (1993) Involvement of Ypt7p, a small GTPase, in traffic from late endosome to the vacuole in yeast. J. Cell Sci., 106, 823-830.
48. Schu, P.V., Takegawa, K., Fry, M.J., Stack, J.H., Waterfield, M.D. and Emr, S.D. (1993) Phosphatidylinositol 3-kinase encoded by yeast VPS34 gene essential for protein sorting. Science, 260, 88-91.
49. Serunian, L.A., Haber, M.T., Fukui, T., Kim, J.W., Rhee, S.G., Lowenstein, J.M. and Cantley, L.C. (1989) Polyphosphoinositides produced by phosphatidylinositol 3-kinase are poor substrates for phospholipases C from rat liver and bovine brain. J. Biol. Chem., 264, 17809-17815.
50. Sikorski, R.S. and Hieter, P. (1989) A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics, 122, 19-27.
51. Singer-Kruger, B., Stenmark, H., Dusterhoft, A., Philippsen, P. Yoo, J.S., Gallwitz, D. and Zerial, M. (1994) Role of three rab5-like GTPases, Ypt51p, Ypt52p and Ypt53p, in the endocytic and vacuolar protein sorting pathways of yeast. J. Cell Biol., 125, 283-298.
52. Sorensen, S.O., van den Hazel, H.B., Kielland-Brandt, M.C. and Winther, J.R. (1994) pH-dependent processing of yeast procarboxy-peptidase Y by proteinase A in vivo and in vitro. Eur. J. Biochem., 220, 19-27.
53. Spormann, D.O., Heim, J. and Wolf, D.H. (1991) Carboxypeptidase yscS: gene structure and function of the vacuolar enzyme. Eur. J. Biochem., 197, 399-405.
54. Stack, J.H., Herman, P.K., Schu, P.V. and 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.
55. Stack, J.H., DeWald, D.B., Takegawa, K. and Emr, S.D. (1995) Vesicle-mediated protein transport: regulatory interactions between the Vps15 protein kinase and the Vps34 PtdIns 3-kinase essential for protein sorting to the vacuole in yeast. J. Cell Biol., 129, 321-334.
56. Stephens, L. et al. (1998) Protein kinase B kinases that mediate phosphatidylinositol, 3,4,5-trisphosphate-dependent activation of protein kinase B. Science, 279, 710-714.
57. Sternweis, P.C. and Smrcka, A.V. (1992) Regulation of phospholipase C by G proteins. Trends Biochem. Sci., 17, 502-506.
58. Toker, A. and Cantley, L.C. (1997) Signalling through the lipid products of phosphoinositide-3-OH kinase. Nature, 387, 673-676.
59. van den Hazel, H.B., Kielland-Brandt, M.C. and Winther, J.R. (1992) Autoactivation of proteinase A initiates activation of yeast vacuolar zymogens. Eur. J. Biochem., 207, 277-283.
60. van den Hazel, H.B., Kielland-Brandt, M.C. and Winther, J.R. (1996) Review: biosynthesis and function of yeast vacuolar proteases. Yeast, 12, 1-16.
61. van Helvoort, A., Smith, A.J., Sprong, H., Fritzsche, I., Schinkel, A.H., Borst, P. and van Meer, G. (1996) MDR1 P-glycoprotein is a lipid translocase of broad specificity, while MDR3 P-glycoprotein specifically translocates phosphatidylcholine. Cell, 87, 507-517.
62. Vanhaesebroeck, B., Leevers, S.J., Panayotou, G. and Waterfield, M.D. (1997) Phosphoinositide 3-kinases: a conserved family of signal transducers. Trends Biochem. Sci., 22, 267-272.
63. Vida, T.A. and Emr, S.D. (1995) A new vital stain for visualizing vacuolar membrane dynamics and endocytosis in yeast. J. Cell Biol., 128, 779-792.
64. Vida, T.A., Huyer, 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.
65. Wada, Y. Nakamura, N., Ohsumi, Y. and Hirata, A. (1997) Vam3p, a new member of syntaxin related protein, is required for vacuolar assembly in the yeast Saccharomyces cerevisiae. J. Cell Sci., 110, 1299-1306.
66. Wendland, B., McCaffery, J.M., Xiao, Q. and Emr, S.D. (1996) A novel fluorescence-activated cell sorter-based screen for yeast endocytosis mutants identifies a yeast homologue of mammalian eps15. J. Cell Biol., 135, 1485-1500.
67. Wichmann, H., Hengst, L. and Gallwitz, D. (1992) Endocytosis in yeast: evidence for the involvement of a small GTP-binding protein (Ypt7p). Cell, 71, 1131-1142.
68. Woscholski, R. and Parker, P.J. (1997) Inositol lipid 5-phosphatases-traffic signals and signal traffic. Trends Biochem. Sci., 22, 427-431.
69. Woscholski, R., Waterfield, M.D. and Parker, P.J. (1995) Purification and biochemical characterization of a mammalian phosphatidylinositol, 3,4,5-trisphosphate 5-phosphatase. J. Biol. Chem., 270, 31001-31007.