A dileucine-like sorting signal directs transport into an AP-3-dependent, clathrin-independent pathway to the yeast vacuole

EMBO Journal

Volumn 17, Issue 9, 1998, Pages 2482-2493

  Vowels, Jennifer J ^a   Payne, Gregory S ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

ALP sorting signal; AP 3 pathway; Dileucine like signal; Vacuolar transport

Indexed keywords

ADAPTOR PROTEIN; ALKALINE PHOSPHATASE; CHIMERIC PROTEIN; CLATHRIN; LEUCINE; PROTEIN SUBUNIT; VALINE;

ARTICLE; CELL VACUOLE; CONTROLLED STUDY; GENETIC CONSERVATION; LYSOSOME; MEMBRANE TRANSPORT; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; YEAST;

ALKALINE PHOSPHATASE; AMINO ACID SEQUENCE; CLATHRIN; DNA-BINDING PROTEINS; GENOTYPE; GOLGI APPARATUS; INTRACELLULAR MEMBRANES; LEUCINE; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PYROPHOSPHATASES; RECOMBINANT FUSION PROTEINS; SACCHAROMYCES CEREVISIAE; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; VACUOLES; VALINE;

EUKARYOTA; MAMMALIA;

EID: 0032079666     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/17.9.2482     Document Type: Article

References (64)

1. Abeijon,C., Yanagisawa,K., Mandon,E.C, Hausler,A., Moremen,K., Hirschberg,C.B. and Robhins,P.W. (1993) Guanosine diphosphatase is required for protein and sphingolipid glycosylation in the Golgi lumen of Saccharomyces cerevisiae. J. Cell Biol., 122, 307-323.
2. Amigorena,S. et al. (1992) Cytoplasmic domain heterogeneity and functions of IgG receptors in B lymphocytes. Science, 256. 1808-1812.
3. 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.
4. 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.
5. Berninsone,P., Lin,Z.-Y., Kempner,E. and Hirschberg,C.B. (1995) Regulation of yeast Golgi glycosylation. J. Biol. Chem., 270, 14564-14567.
6. Brickner,J.H. and Fuller,R.S. (1997) SOII encodes a novel, conserved protein that promotes TGN-endosomal cycling of Kex2p and other membrane proteins by modulating the function of two TGN localization signals. J. Cell Biol., 139, 23-36.
7. Bryant,N.J. and Stevens,T.H. (1997) Vacuole biogenesis in Saccharomyces cerevisiae: protein transport pathways to the yeast vacuole. Microbiol. Mol. Biol. Rev., 62, 230-247.
8. Chapman,R.E. and Munro,S. (1994) The functioning of the yeast Golgi apparatus requires an ER protein encoded by ANP1, a member of a new family of genes affecting the secretory pathway. EMBO J., 13, 4896-4907.
9. Cowles,C.R., Emr,S.D. and Horazdovsky,B.F. (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., 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.
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. Dell'Angelica,E.C., Ohno,H., Ooi,C.E., Rabinovich,E., Roche,K. and Bonifacino,J.S. (1997a) AP-3: an adaptor-like protein complex with ubiquitous expression. EMBO J., 16, 917-928.
13. Dell'Angelica,E.C., Ooi,C.E. and Bonifacino,J.S. (1997b) β3A-adaptin, a subunit of the adaptor-like complex AP-3. J. Biol. Chem., 212, 15078-15084.
14. Dietrich,J., Kastrup,J., Nielsen,B.L., Odum,N. and Geisler,C. (1997) Regulation and function of the CD3γ 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., te Heesen,S., Graham,T.R., Aebi,M. and Emr,S.D. (1994) Signal-mediated retrieval of a membrane protein from the Golgi to the ER in yeast. J. Cell Biol., 127, 653-665.
16. Heilker,R., Manning-Krieg,U., Zuber,J.-F. and Spiess,M. (1996) In vitro binding of clathrin adaptors to sorting signals correlates with endocytosis and basolateral sorting. EMBO J., 15, 2893-2899.
17. Ito,H., Fukuda,Y., Murata,K. and Kimura,A. (1983) Transformation of intact yeast cells treated with alkali cations. J. Bacteriol., 153, 163-168.
18. Jones,E.W. (1991) Tackling the protease problem in Saccharomyces cerevisiae. Methods Enzymol., 194, 428-453.
19. Kirchhausen,T. (1993) Coated pits and coated vesicles - sorting it all out. Curr. Opin. Struct. Biol., 3, 182-188.
20. Kirchhausen,T., Bonifacino,J.S. and Riezman,H. (1997) Linking cargo to vesicle formation: receptor tail interactions with coat proteins. Curr. Opin. Cell Biol., 9, 488-195.
21. 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.
22. Klionsky,D.J. and Emr,S.D. (1990) A new class of lysosomal/vacuolar protein sorting signals. J. Biol. Chem., 265, 5349-5352.
23. Kornfeld,S. and Mellman,J. (1989) The biogenesis of lysosomes. Annu. Rev. Cell Biol., 5, 483-525.
24. Marks,M.S., Ohno,H., Kirchhausen,T. and Bonifacino,J.S. (1997) Protein sorting by tyrosine-based signals: adapting to the Ys and wherefores. Trends Cell Biol., 7, 124-128.
25. Mauxion,F. Le Borgne,R., Munier-Lehmann,H. and Hoftack,B. (1996) A casein kinase II phosphorylation site in the cytoplasmic domain of the cation-dependent mannose 6-phosphate receptor determines the high affinity interaction of the AP-1 Golgi assembly proteins with membranes. J. Biol. Chem., 271, 2171-2178.
26. McClary,J.A., Witney,F. and Geisselsoder,J. (1989) Efficient site-directed in vitro mutagenesis using phagemid vectors. BioTechniques, 7, 282-287.
27. Mellman,I. (1996) Endocytosis and molecular sorting. Annu. Rev. Cell Dev. Biol., 12, 575-625.
28. Miettinen,H.M., Rose,J.K. and Mellman,J. (1989) Fc receptor isoforms exhibit distinct abilities for coated pit localization as a result of cytoplasmic domain heterogeneity. Cell, 58, 317-327.
29. Motta,A., Bremnes,B., Morelli,M.A., Frank,R.W., Saviano,G. and Bakke,O. (1995) Structure-activity of the major histocompatibility complex-associated invariant chain. J. Biol. Chem., 270, 27165-27171.
30. Newman,L.S., McKeever,M.O., Okano,H.J. and Darnell,R.B. (1995) β-NAP, a cerebellar degeneration antigen, is a neuron-specific vesicle coat protein. Cell, 82, 773-783.
31. Nothwehr,S.F. and Stevens,T.H. (1994) Sorting of membrane proteins in the yeast secretory pathway. J. Biol. Chem., 269, 10185-10188.
32. Nothwehr,S.F., Conibear,E. and Stevens,T.H. (1995) Golgi and vacuolar membrane proteins reach the vacuole in vps1 mutant yeast cells via the plasma membrane. J. Cell Biol., 129, 35-46.
33. Nothwehr,S.F., Bryant,N.J. and Stevens,T.H. (1996) The newly identified yeast GRD genes are required for retention of late-Golgi membrane proteins. Mol. Cell Biol., 16, 2700-2707.
34. Payne,G.S. and Schekman,R. (1989) Clathrin: a role in the intracellular retention of a Golgi membrane protein. Science, 245, 1358-1365.
35. Phan,H.L., Finlay,J.A., Chu,D.S., Tan,P.K., Kirchhausen,T. and Payne,G.S. (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 J., 13, 1706-1717.
36. Piper,R.C., Whitters,E.A. and Stevens,T.H. (1994) Yeast Vps45p is a Seclp-like protein required for the consumption of vacuole-targeted, post-Golgi transport vesicle. Eur. J. Cell Biol., 65, 305-318.
37. 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.
38. Pond,L., Kuhn,L.A., Teyton,L., Schutze,M.P., Tainer,J.A., Jackson,M.R. and Peterson,P.A. (1995) A role for acidic residues in di-leucine motifbased targeting to the endocytic pathway. J. Biol. Chem., 270, 19989-19997.
39. Rad,M.R., Phan,H.L., Kirchrath,L., Tan,P.K., Kirchhausen,T., Hollenberg,C.P. and Payne,G.S. (1995) Saccharomyces cerevisiae Apl2p, a homologue of the mammalian clathrin AP β subunit, plays a role in clathrin-dependent Golgi functions. J. Cell Sci., 108, 1605-1615.
40. 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.
41. Redding,K., Seeger,M., Payne,G. and Fuller,R.S. (1996) The effects of clathrin inactivation on localization of Kex2 protease are independent of the TGN localization signal in the cytosolic tail of Kex2p. Mol. Biol. Cell, 7, 1667-1677.
42. Roberts,C.J., Pohlig,G., Rothman,J.H. and Stevens,T.H. (1989) Structure, biosynthesis, and localization of dipeptidyl aminopeptidase B, an integral membrane glycoprotein of the yeast vacuole. J. Cell Biol., 108, 1363-1373.
43. Roberts,C.J., Nothwehr,S.F. and Stevens,T.H. (1992) Membrane protein sorting in the yeast secretory pathway: evidence that the vacuole may be the default compartment. J. Cell Biol., 119, 69-83.
44. 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.
45. Robinson,M.S. (1994) The role of clathrin, adaptors and dynamin in endocytosis. Curr. Opin. Cell Biol., 6, 538-544.
46. Rothstein,R. (1991) Targeting, disruption, replacement, and allele rescue: integrative DNA transformation in yeast. Methods Enzymol., 194, 281-301.
47. Saiki,R.K., Gelfand,D.H., Stoffel,S., Scharf,S.J., Higuchi,R., Horn,G.T., Mullis,K.B. and Erlich,H.A. (1988) Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science, 239, 487-491.
48. Sambrook,J., Fritsch,E.F. and Maniatis,T. (1989) Molecular Cloning: A Laboratory Manual. 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
49. Sandoval,I. and Bakke,O. (1994) Targeting of membrane proteins to endosomes and lysosomes. Trends Cell Biol., 4, 292-297.
50. Sandoval,I.V., Arredondo,J.J., Alcalde,J., Noriega,A.G., Vandekerckhove, J., Jimenez,M.A. and Rico,M. (1994) The residues Leu(Ile)475-He(Leu, Val, Ala)476, contained in the extended carboxyl cytoplasmic tail, are critical for targeting of the resident lysosomal membrane protein LIMP II to lysosomes. J. Biol. Chem., 269, 6622-6631.
51. Sanger,F., Nicklen,S. and Coulson,A.R. (1977) DNA sequencing with chain-terminating inhibitors. Proc. Natl Acad. Sci. USA, 74, 5463-5467.
52. Schekman,R. and Orci,L. (1996) Coat proteins and vesicle budding. Science, 271, 1526-1532.
53. Seeger,M. and Payne,G. (1992a) Selective and immediate effects of clathrin heavy chain mutations on Golgi membrane protein retention in Saccharomyces cerevisiae. J. Cell Biol., 118, 531-540.
54. Seeger,M. and Payne,G.S. (1992b) A role for clathrin in the sorting of vacuolar proteins in the Golgi complex of yeast. EMBO J., 11, 2811-2818.
55. 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.
56. Simpson,F., Bright,N.A., West,M.A., Newman,L.S., Darnell,R.B. and Robinson,M.S. (1996) A novel adaptor-related protein complex. J. Cell Biol., 133, 749-760.
57. Simpson,F., Peden,A.A., Christopoulou,L. and Robinson,M.S. (1997) Characterization of the adaptor-related protein complex, AP-3. J. Cell Biol., 137, 835-845.
58. Stack,J.H., Horazdovsky,B. and Emr,S.D. (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.
59. Stepp,J.D., Pellicena-Palle,A., Hamilton,S., Kirchhausen,T. and Lemmon, S.K. (1995) A late Golgi sorting function for Saccharomyces cerevisiae Apmlp, but not for Apm2p, a second yeast clathrin AP medium chain-related protein. Mol. Biol. Cell, 6, 41-58.
60. Stepp,J.D., Huang,K. and Lemmon,S.K. (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.
61. Stevens,T., Esmon,B. and Schekman,R. (1982) Early stages in the yeast secretory pathway are required for transport of carboxypeptidase Y to the vacuole. Cell, 30, 439-448.
62. Tan,P.K., Davis,N.G., Sprague,G.F. and Payne,G.S. (1993) Clathrin facilitates the internalization of seven transmembrane segment receptors for mating pheromones in yeast. J. Cell Biol., 123, 1707-1716.
63. Vowels,J.J. and Payne,G.S. (1998) A role for the lumenal domain in Golgi localization of the Saccharomyces cerevisiae guanosine diphosphatase. Mol. Biol. Cell, 9, in press.
64. Wilcox,C.A., Redding,K., Wright,R. and Fuller,R.S. (1992) Mutation of a tyrosine localization signal in the cytosolic tail of yeast Kex2 protease disrupts Golgi retention and results in default transport to the vacuole. Mol. Biol. Cell, 3, 1353-1371.