Acidic di-leucine motif essential for AP-3-dependent sorting and restriction of the functional specificity of the Vam3p vacuolar t-SNARE

Journal of Cell Biology

Volumn 142, Issue 4, 1998, Pages 913-922

  Darsow, Tamara ^a   Burd, Christopher G ^a   Emr, Scott D ^a,b  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

AP 3; Di leucine; Saccharomyces cerevisiae; SNARE; Vacuole

Indexed keywords

ALKALINE PHOSPHATASE; CARBOXYPEPTIDASE; CARBOXYPEPTIDASE C; LEUCINE; PROTEIN PEP12P; PROTEIN VAM3P; SNARE PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR AP 3; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL SELECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN TARGETING; SIGNAL TRANSDUCTION;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; ALKALINE PHOSPHATASE; BIOLOGICAL TRANSPORT; CARBOXYPEPTIDASE C; CARBOXYPEPTIDASES; ENDOSOMES; FUNGAL PROTEINS; LEUCINE; MEMBRANE PROTEINS; MONOMERIC CLATHRIN ASSEMBLY PROTEINS; MUTATION; NERVE TISSUE PROTEINS; PHOSPHOPROTEINS; QA-SNARE PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SNARE PROTEINS; VESICLE-ASSOCIATED MEMBRANE PROTEIN 3; VESICULAR TRANSPORT PROTEINS;

EID: 0032563630     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.142.4.913     Document Type: Article

References (47)

1. Babst, M., T.K. Sato, L.M. Banta, and S.E. Emr. 1997. Endosomal transport function in yeast requires a novel AAA-type ATPase, Vps4p. EMBO (Eur. Mol. Biol. Organ.) J. 16:1820-1831.
2. Babst, M., B. Wendland, E.J. Estepa, and S.D. Emr. 1998. The Vps4p AAA ATPase regulates membrane association of a Vps protein complex required for normal endosomal function. EMBO (Eur. Mol. Biol. Organ.) J. 17:2982-2993.
3. Banfield, D.K., M.J. Lewis, C. Rabouille, G. Warren, and H.R. Pelham. 1994. Localization of Sed5, a putative vesicle targeting molecule, to the cis-Golgi network involves both its transmembrane and cytoplasmic domains. J. Cell Biol. 127:357-371.
4. Becherer, K.A., S. Reider, S.D. Emr. and E.W. Jones. 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.
5. Bennett, M.K., and R.H. Scheller. 1993. The molecular machinery for secretion is conserved from yeast to neurons. Proc. Natl. Acad. Sci. USA. 90:2559-2563.
6. Bennett, M.K., J.E. Garcia-Arraras, L.A. Elferink, K. Peterson, A.M. Fleming, C.D. Hazuka, and R.H. Scheller. 1993. The syntaxin family of vesicular transport receptors. Cell. 74:863-873.
7. Burd, C.G., M. Peterson, C.R. Cowles, and S.D. Emr. 1997. A novel Sec18p/NSF-dependent complex required for Golgi-to-endosome transport in yeast. Mol. Biol. Cell. 8:1089-1104.
8. Chen, W.J., J.L. Goldstein, and M.S. Brown. 1990. NPXY, a sequence often found in cytoplasmic tails, is required for coated pit-mediated internalization of the low density lipoprotein receptor. J. Biol. Chem. 265:3116-3123.
9. Cowles, C.R., S.D. Emr, and B.F. Horazdovsky. 1994. Mutations in the VPS45 gene, a SEC1 homologue, result in vacuolar protein sorting defects and accumulation of membrane vesicles. J. Cell Sci. 107:3449-3459.
10. Cowles, C.R., G. Odorizzi, G.S. Payne, and S.D. Emr. 1997a. The AP-3 adaptor complex is essential for cargo-selective transport to the yeast vacuole. Cell. 91:109-118.
11. Cowles, C.R., W.B. Snyder, C.G. Burd, and S.D. Emr. 1997b. An alternative Golgi to vacuole delivery pathway in yeast: identification of a sorting determinant and required transport component. EMBO (Eur. Mol. Biol. Organ.) J. 16:2769-2782.
12. Darsow, T., S.E. Rieder, and S.D. Emr. 1997. A multispecificity syntaxin homologue, Vam3p, essential for autophagic and biosynthetic protein transport to the vacuole. J. Cell Biol. 138:517-529.
13. Dell' Angelica, E.C., H. Ohno, C.E. Ooi, E. Rabinovich, K.W. Roche, and J.S. Bonifacino. 1997. AP-3: an adaptor-like protein complex with ubiquitous expression. EMBO (Eur. Mol. Biol. Organ.) J. 16:917-928.
14. Dietrich, J., J. Kastrup, B.L. Nielsen, N. Odum, and C. Geisler. 1997. Regulation and function of the CD3gamma DxxxLL motif: A binding site for adaptor protein-1 and adaptor protein-2 in vitro. J. Cell Biol. 138:271-281.
15. Gaynor, E.C., S. te Heesen, T.R. Graham, M. Aebi, and S.D. Emr. 1994. Signal-mediated retrieval of a membrane protein from the Golgi to the ER in yeast. J. Cell Biol. 127:653-665.
16. Gotte, M., and D. Gallwitz. 1997. High expression of the yeast syntaxin-related Vam3 protein suppresses the protein transport defects of pep12 null mutant. FEBS (Fed. Eur. Biochem. Soc.) Lett. 411:48-52.
17. Hanahan, D. 1983. Studies on transformation of Escherichia coli with plasmids. J. Mol. Biol. 166:557-580.
18. Heilker, R., U. Manning-Krieg, J.F. Zuber, and M. Spiess. 1996. In vitro binding of clathrin adaptors to sorting signals correlates with endocytosis and basolateral sorting. EMBO (Eur. Mol. Biol. Organ.) J. 15:2893-2899.
19. Honing, S., I.V. Sandoval, and K. von Figura. 1998. A di-leucine-based motif in the cytoplasmic tail of LIMP-II and tyrosinase mediates selective binding of AP-3. EMBO (Eur. Mol. Biol. Organ.) J. 17:1304-1314.
20. Horazdovsky, B.F., G.R. Busch, and S.D. Emr. 1994. VPS21 encodes a rab5-like GTP binding protein that is required for the sorting of yeast vacuolar proteins. EMBO (Eur. Mol. Biol. Organ.) J. 13:1297-1309.
21. Ito, H., Y. Fukuda, K. Murata, and A. Kimura. 1983. Transformation of intact yeast cells treated with alkali cations. J. Bacteriol. 153:163-168.
22. Klionsky, D.J., and S.D. Emr. 1989. Membrane protein sorting: biosynthesis, transport and processing of yeast vacuolar alkaline phosphatase. EMBO (Eur. Mol. Biol. Organ.) J. 8:2241-2250.
23. Letourneur, F., and R.D. Klausner. 1992. A novel di-leucine motif and a tyrosine-based motif independently mediate lysosomal targeting and endocytosis of CD3 chains. Cell. 69:1143-1157.
24. Marks, M.S., H. Ohno, T. Kirchhausen, and J.S. Bonifacino. 1997. Protein sorting by tyrosine-based signals. Trends Cell Biol. 7:124-128.
25. Motta, A., B. Bremnes, M.A. Morelli, R.W. Frank, G. Saviano, and O. Bakke. 1995. Structure-activity relationship of the leucine-based sorting motifs in the cytosolic tail of the major histocompatibility complex-associated invariant chain. J. Biol. Chem. 270:27165-27171.
26. Muhlrad, D., R. Hunter, and R. Parker. 1992. A rapid method for localized mutagenesis of yeast genes. Yeast. 8:79-82.
27. Novick, P., and P. Brennwald. 1993. Friends and family: the role of Rab GTP-ases in vesicular traffic. Cell. 75:597-601.
28. Odorizzi, G., C.R. Cowles, and S.D. Emr. 1998. The AP-3 complex: a coat of many colors. Trends Cell Biol. 8:282-287.
29. Paravicini, G., B.F. Horazdovsky, and S.D. Emr. 1992. Alternative pathways for the sorting of soluble vacuolar proteins in yeast: a vps35 null mutant missorts and secretes only a subset of vacuolar hydrolases. Mol. Biol. Cell. 3:415-427.
30. Phan, H.L., J.A. Finlay, D.S. Chu, P.K. Tan, T. Kirchhausen, and G.S. Payne. 1994. The Saccharomyces cerevisiae APS1 gene encodes a homolog of the small subunit of the mammalian clathrin AP-1 complex: evidence for functional interaction with clathrin at the Golgi complex. EMBO (Eur. Mol. Biol. Organ.) J. 13:1706-1717.
31. Piper, R.C., N.J. Bryant, and T.H. Stevens. 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.
32. Pond, L., L.A. Kuhn, L. Teyton, M.P. Schutze, J.A. Tainer, M.R. Jackson, and P.A. Peterson. 1995. A role for acidic residues in di-leucine motif-based targeting to the endocytic pathway. J. Biol. Chem. 270:19989-19997.
33. Rapoport, I., Y.C. Chen, P. Cupers, S.E. Shoelson, and T. Kirchhausen. 1998. Dileucine-based sorting signals bind to the beta chain of AP1 at a site distinct and regulated differently from the tyrosine-based motif-binding site. EMBO (Eur. Mol. Biol. Organ.) J. 17:2148-2155.
34. Rayner, J.C., and H.R. Pelham. 1997. Transmembrane domain-dependent sorting of proteins to the ER and plasma membrane in yeast. EMBO (Eur. Mol. Biol. Organ.) J. 16:1832-1841.
35. Rieder, S.E., L.M. Banta, K. Kohrer, J.M. McCaffery, and S.D. Emr. 1996. Multilamellar endosome like compartment accumulates in the yeast vps28. Mol. Biol. Cell. 7:985-999.
36. Robinson, M.S. 1994. The role of clathrin, adaptors, and dynamin in endocytosis. Curr. Opin. Cell Biol. 6:538-544.
37. Robinson, M.S. 1997. Coats and vesicle budding. Trends Cell Biol. 7:99-102.
38. Rothman, J.E. 1994. Mechanisms of intracellular protein transport. Nature. 372: 55-63.
39. Sato, T.K., T. Darsow, and S.D. Emr. 1998. Vam7p, a SNAP-25-like molecule, and Vam3p, a syntaxin homologue function together in vacuolar protein trafficking. Mol. Cell. Biol. In press.
40. Sikorski, R.S., and P. Hieter. 1989. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics. 122:19-27.
41. Simpson, F., A.A. Peden, L. Christopoulou, and M.S. Robinson. 1997. Characterization of the adaptor-related protein complex, AP-3. J. Cell Biol. 137: 835-845.
42. Sollner, T., S.W. Whiteheart, M. Brunner, H. Erdjument-Bromage, S. Geromanos, P. Tempst, and J.E. Rothman. 1993. SNAP receptors implicated in vesicle targeting and fusion. Nature. 362:318-324.
43. Stack, J.H., and S.D. Emr. 1993. Genetic and biochemical studies of protein sorting to the yeast vacuole. Curr. Opin. Cell. Biol. 5:641-646.
44. Stepp, J.D., A. Pellicena-Palle, S. Hamilton, T. Kirchhausen, and S.K. Lemmon. 1995. A late Golgi sorting function for Saccharomyces cerevisiae Apm1p, but not for Apm2p, a second yeast clathrin AP medium chainrelated protein. Mol. Biol. Cell. 6:41-58.
45. Stepp, J.D., K. Huang, and S.K. Lemmon. 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.
46. Vida, T. A., and S.D. Emr. 1995. A new vital stain for visualizing vacuolar membrane dynamics and endocytosis in yeast. J. Cell Biol. 128:779-792.
47. Vowels, J.J., and G.S. Payne. 1998. A dileucine-like sorting signal directs transport into an AP-3-dependent, clathrin-independent pathway to the yeast vacuole. EMBO (Eur. Mol. Biol. Organ.) J. 17:2482-2493.