A role for the lumenal domain in Golgi localization of the Saccharomyces cerevisiae guanosine diphosphatase

Molecular Biology of the Cell

Volumn 9, Issue 6, 1998, Pages 1351-1365

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

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GUANOSINE DIPHOSPHATE; PHOSPHATASE;

ARTICLE; ENZYME LOCALIZATION; GOLGI COMPLEX; LIPID BILAYER; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SACCHAROMYCES CEREVISIAE;

FUNGI; SACCHAROMYCES CEREVISIAE;

EID: 0031815063     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.9.6.1351     Document Type: Article

References (68)

1. Abeijon, C., Orlean, P., Robbins, P.W., and Hirschberg, C.B. (1989). Topography of glycosylation in yeast: characterization of GDPmannose transport and lumenal guanosine diphosphatase activities in Golgi-like vesicles. Proc Natl Acad Sci USA 86, 6935-6939.
2. Abeijon, C., Yanagisawa, K., Mandon, E.C., Hausler, A., Moremen, K., Hirschberg, C.B., and Robbins, 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.
3. Berninsone, P., Lin, Z.-Y., Kempner, E., and Hirschberg, C.B. (1995). Regulation of yeast Golgi glycosylation. J. Biol. Chem. 270, 14564-14567.
4. Bowser, R., and Novick, P. (1991). Sec15 protein, an essential component of the exocytotic apparatus, is associated with the plasma membrane and with a soluble 19.5s particle. J. Cell Biol. 112, 1117-1131.
5. Bretscher, M.S., and Munro, S. (1993). Cholesterol and the Golgi apparatus. Science 261, 1280-1281.
6. Bryant, N.J., and Boyd, A. (1993). Immunoisolation of Kex2p-containing organelles from yeast demonstrates colocalisation of three processing proteinases to a single Golgi compartment. J. Cell Sci. 106, 815-822.
7. Chapman, R.E., and Munro, S. (1994). The functioning of the yeast Goigi 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.
8. Colley, K.J. (1997). Golgi localization of glycosyltransferases: more questions than answers. Glycobiology 7, 1-13.
9. Colley, K.J., Lee, E.U., and Paulson, J.C. (1992). The signal anchor and stem regions of the β-galactoside α-2,6,-sialyltransferase may each act to localize the enzyme to the Golgi apparatus. J. Biol. Chem. 267, 7784-7793.
10. Cooper, A., and Bussey, H. (1992). Yeast Kex1p is a Golgi-associated membrane protein: deletions in a cytoplasmic targeting domain result in mislocalization to the vacuolar membrane. J. Cell Biol. 229, 1459-1468.
11. Cowles, C.R., Snyder, W.B., Burd, C.G. and Emr, S.D. (1997). Novel Golgi to vacuole delivery pathway in yeast: identification of a sorting determinant and required transport component. EMBO J. 16, 2769-2782.
12. Cunningham, K.W., and Wickner, W.T. (1989). Yeast KEX2 protease and mannosyltransferase I are localized to distinct compartments of the secretory pathway. Yeast 5, 25-33.
13. Dahdal, R.Y., and Colley, K.J. (1993). Specific sequences in the signal anchor of the β-galactoside α-2,6-sialyltransferase are not essential for Golgi localization. J. Biol. Chem. 268, 26310-26319.
14. Franzusoff, A., Redding, K., Crosby, J., Fuller, R.S., and Schekman, R. (1991). Localization of components involved in protein transport and processing through the yeast Golgi apparatus. J. Cell Biol. 112, 27-37.
15. Franzusoff, A., and Schekman, R. (1989). Functional compartments of the yeast Golgi apparatus are defined by the sec7 mutation. EMBO J. 8, 2695-2702.
16. 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.
17. 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.
18. Graham, T.R., and Krasnov, V.A. (1995). Sorting of yeast α1,3 mannosyltransferase is mediated by a lumenal domain interaction, and a transmembrane domain signal that can confer clathrin-dependent Golgi localization to a secreted protein. Mol. Biol. Cell 6, 809-824.
19. Graham, T.R., Seeger, M., Payne, G.S., MacKay, V.L., and Emr, S.D. (1994). Clathrin-dependent localization of α1,3 mannosyltransferase to the Golgi complex of Saccharomyces cerevisiae. J. Cell Biol. 227 667-678.
20. Harris, S.L., and Waters, M.G. (1996). Localization of a yeast early Golgi mannosyltransferase, Och1p, involves retrograde transport. J. Cell Biol. 132, 985-998.
21. Herscovics, A., and Orlean, P. (1993). Glycoprotein biosynthesis in yeast. FASEB J. 7, 540-550.
22. Ito, H., Fukuda, Y., Murata, K., and Kimura, A. (1983). Transformation of intact yeast cells treated with alkali cations. J. Bacteriol. 153, 163-168.
23. Jones, E.W. (1991). Tackling the protease problem in Saccharomyces cerevisiae. Methods Enzymol. 194, 428-453.
24. Jungmann, J., and Munro, S. (1998). Multi-protein complexes in the cis Golgi of Saccharomyces cerevisiae with α-1,6-mannoxyltransferase activity. EMBO J. 17, 423-434.
25. Kaneko, Y., Hayashi, N., Toh-e, A., Banno, I., and Oshima, Y. (1987). Structural characteristics of the PHO8 gene encoding repressible alkaline phosphatase in Saccharomyces cerevisiae. Gene 58, 137-148.
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., and Emr, S.D. (1990). A new class of lysosomal/ vacuolar protein sorting signals. J. Biol. Chem. 265, 5349-5352.
28. Laemmli, U.K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
29. Lupashin, V.V., Hamamoto, S., and Schekman, R.W. (1996). Biochemical requirements for the targeting and fusion of ER-derived transport vesicles with purified yeast Golgi membranes. J. Cell Biol. 132, 277-289.
30. Lussier, M., Sdicu, A.-M., Ketela, T., and Bussey, H. (1995). Localization and targeting of the Saccharomyces cerevisiae Kre2p/Mrrt1p medial-Golgi compartment. J. Cell Biol. 131, 913-927.
31. Machamer, C.E. (1993). Targeting and retention of Golgi membrane proteins. Curr. Opin. Cell Biol. 5, 606-612.
32. Masibay, A.S., Balaji, P.V., Boeggeman, E.E., and Qasba, P.K. (1993). Mutational analysis of the Golgi retention signal of bovine β-1,4-galactosyltransferase. J. Biol. Chem. 268, 9908-9916.
33. McClary, J.A., Witney, F., and Geisselsoder, J. (1989). Efficient site-directed in vitro mutagenesis using phagemid vectors. BioTechniques 7, 282-287.
34. Mellman, I., and Simons, K. (1992). The Golgi complex: in vitro veritas? Cell 68, 829-840.
35. Munro, S. (1991). Sequences within and adjacent to the transmembrane segment of α-2,6-sialyltransferase specify Golgi retention. EMBO J. 10, 3577-3588.
36. Munro, S. (1995). An investigation of the role of transmembrane domains in Golgi protein retention. EMBO J. 14, 4695-4704.
37. Nakanishi-Shindo, Y., Nakayama, K.-I., Tanaka, A., Toda, Y., and Jigami, Y. (1993). Structure of the N-linked oligosaccharides that show the complete loss of α-1,6-polymannose outer chain from och1, och1 mnn1, and och1 mnn1 alg3 mutants of Saccharomyces cerevisiae. J. Biol. Chem. 268, 26338-26345.
38. Nakayama, K., Nakanishi-Shindo, Y., Tanaka, A., Haga-Toda, Y., and Jigami, Y. (1997). Substrate specificity of alpha-1,6-mannosyltransferase that initiates N-linked mannose outer chain elongation in Saccharomyces cerevisiae. FEBS Lett. 412, 547-550.
39. Nakayama, K.-I., Nagasu, T., Shimma, Y.-I., Kuromitsu, J.-R., and Jigami, Y. (1992). OCH1 encodes a novel membrane bound mannosyltransferase: outer chain elongation of asparagine-linked oligosaccharides. EMBO J. 11, 2511-2519.
40. Nilsson, T., Hoe, M.H., Slusarewicz, P., Rabouille, C., Watson, R., Hunte, F., Watzele, G., Berger, E.G., and Warren, G. (1994). Kin recognition between medial Golgi enzymes in HeLa cells. EMBO J. 13, 562-574.
41. Nilsson, T., Rabouille, C., Hui, N., Watson, R., and Warren, G. (1996). The role of the membrane-spanning domain and stalk region of N-acetylglucosaminyltransferase I in retention, kin recognition and structural maintenance of the Golgi apparatus in HeLa cells. J. Cell Sci. 109, 1975-1989.
42. Nilsson, T., Slusarewicz, P., Hoe, M.H., and Warren, G. (1993). Kin recognition: a model for the retention of Golgi enzymes. FEBS Lett. 330, 1-4.
43. Nilsson, T., and Warren, G. (1994). Retention and retrieval in the endoplasmic reticulum and the Golgi apparatus. Curr. Opin. Cell Biol. 6, 517-521.
44. Nothwehr, S.F., Roberts, C.J., and Stevens, T.H. (1993). Membrane protein retention in the yeast Golgi apparatus: dipeptidyl amino-peptidase A is retained by a cytoplasmic signal containing aromatic residues. J. Cell Biol. 121, 1197-1209.
45. Novick, P., Ferro, S., and Schekman, R. (1981). Order of events in the yeast secretory pathway. Cell 25, 461-469.
46. Pelham, H.R., and Munro, S. (1993). Sorting of membrane proteins in the secretory pathway. Cell 75, 603-605.
47. 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.
48. Preuss, D., Mulholland, J., Franzusoff, A., Segev, N., and Botstein, D. (1992). Characterization of the Saccharomyces Golgi complex through the cell cycle by immunoelectron microscopy. Mol. Biol. Cell 3, 789-803.
49. Rayner, J.C., and Pelham, H.R.B. (1997). Transmembrane domain-dependent sorting of proteins to the ER and plasma membrane in yeast. EMBO J. 16, 1832-1841.
50. 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.
51. 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.
52. Roberts, C.J., Raymond, C.K., Yamashiro, C.T., and Stevens, T.H. (1991). Methods for studying the yeast vacuole. Methods Enzymol. 194, 644-661.
53. 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.
54. Rothstein, R. (1991). Targeting, disruption, replacement, and allele rescue: integrative DNA transformation in yeast. Methods Enzymol. 194, 281-301.
55. 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.
56. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989). Molecular cloning: a laboratory manual, 2nd ed., Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
57. Sanger, F., Nicklen, S., and Coulson, A.R. (1977). DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74, 5463-5467.
58. 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.
59. 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.
60. 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.
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. Tang, B.L., Low, S.H., Wong, S.H., and Hong, W. (1995). Cell type differences in Golgi retention signals for transmembrane proteins. Eur. J. Cell Biol. 66, 365-374.
63. Teasdale, R.D., Matheson, F., and Gleeson, P.A. (1994). Post-translational modifications distinguish cell surface from Golgi-retained β1,4 galactosyltransferase molecules. Golgi localization involves active retention. Glycobiology 4, 917-928.
64. Vowels, J.J., and Payne, G.S. (1998). A dileucine-like sorting signal directs transport into an AP-3-dependent, clathrin-independent pathway to the yeast vacuole. EMBO J. (in press).
65. Whitters , E.A., McGee, T.P., and Bankaitis, V.A. (1994). Purification and characterization of a late Golgi compartment from Saccharomyces cerevisiae. J. Biol. Chem. 269, 28106-28117.
66. 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.
67. Wilsbach, K., and Payne, G.S. (1993). Dynamic retention of TGN membrane proteins in Saccharomyces cerevisiae. Trends Cell Biol. 3, 426-431.
68. Yip, C.L., Welch, S.K., Klebl, F., Gilbert, T., Seidel, P., Grant, F.J., O'Hara, P.J., and MacKay, V.L. (1994). Cloning and analysis of the Saccharomyces cerevisiae MNN9 and MNN1 genes required for complex glycosylation of secreted proteins. Proc Natl Acad Sci USA 91, 2723-2727.