A modulatory role for clathrin light chain phosphorylation in Golgi membrane protein localization during vegetative growth and during the mating response of Saccharomyces cerevisiae

Molecular Biology of the Cell

Volumn 10, Issue 3, 1999, Pages 713-726

  Chu, Diana S ^a,b,c   Pishvaee, Babak ^a   Payne, Gregory S ^a,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASEIN KINASE II; CLATHRIN; MATING HORMONE ALPHA FACTOR; MITOGEN ACTIVATED PROTEIN KINASE; PHEROMONE; SERINE;

AMINO ACID SEQUENCE; ARTICLE; CELL GROWTH; CONTROLLED STUDY; ENDOCYTOSIS; ENZYME ACTIVITY; FUNGUS GROWTH; GOLGI COMPLEX; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE; REGULATORY MECHANISM; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION;

FUNGI; SACCHAROMYCES CEREVISIAE;

EID: 0032935411     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.10.3.713     Document Type: Article

References (69)

1. Bar-Zvi, D., and Branton, D. (1986). Clathrin-coated vesicles contain two protein kinase activities. Phosphorylation of clathrin β-light chain by casein kinase II. J. Biol. Chem. 261, 9614-9621.
2. Bar-Zvi, D., Mosley, S.T., and Branton, D. (1988). In vivo phosphorylation of clathrin-coated vesicle proteins from rat reticulocytes. J. Biol. Chem. 163, 4408-4415.
3. Bidwai, A.P., Reed, J.C., and Glover, C.V. (1995). Cloning and disruption of CKB1, the gene encoding the 38-kDa β subunit of Saccharomyces cerevisiae casein kinase II (CKII). Deletion of CKII regulatory subunits elicits a salt-sensitive phenotype. J. Biol. Chem. 270, 10395-10404.
4. Boyle, W.J., van der Geer, P., and Hunter, T. (1991). Phosphopeptide mapping and phosphoamino acid analysis by two-dimensional separation on thin layer cellulose plates. Methods Enzymol. 201, 110-149.
5. Brodsky, F.M. (1997). New fashions in vesicle coats. Trends Cell Biol. 7, 175-179.
6. Brodsky, F.M., Hill, B.L., Acton, S.L., Nathke, I., Wong, D.H., Ponnambalam, S., and Parham, P. (1991). Clathrin light chains: arrays of protein motifs that regulate coated-vesicle dynamics. Trends Biochem. Sci. 16, 208-213.
7. Buehrer, B.M., and Errede, B. (1997). Coordination of the mating and cell integrity mitogen-activated protein kinase pathways in Saccharomyces cerevisiae. Mol. Cell. Biol. 17, 6517-6525.
8. Burnette, W.N. (1981). "Western blotting": electrophoretic transfer of proteins from SDS-polyacrylamide gels to unmodified nitrocellulose and radiographic detection with antibody and radioiodinated protein A. Anal. Biochem. 112, 195-203.
9. Cantournet, B., Creuzet, C., Komano, O., and Loeb, J. (1987). Clathrin β-light chain of rat liver coated vesicles is phosphorylated in vitro and in vivo. FEBS Lett. 220, 143-148.
10. Chan, R.K., and Otte, C.A. (1982). Physiological characterization of Saccharomyces cerevisiae mutants supersensitive to G1 arrest by a factor and a factor pheromones. Mol. Cell. Biol. 2, 21-29.
11. Chang, F., and Herskowitz, I. (1990). Identification of a gene necessary for cell cycle arrest by a negative growth factor of yeast: FAR1 is an inhibitor of a G1 cyclin, CLN2. Cell 63, 999-1011.
12. Chen-Wu, J.L., Padmanabha, R., and Glover, C.V. (1988). Isolation, sequencing, and disruption of the CKA1 gene encoding the α subunit of yeast casein kinase II. Mol. Cell. Biol. 8, 4981-4990.
13. Chu, D.S., Pishvaee, B., and Payne, G.S. (1996). The light chain subunit is required for clathrin function in Saccharomyces cerevisiae. J. Biol. Chem. 271, 33123-33130.
14. Cole, G.M., Stone, D.E., and Reed, S.I. (1990). Stoichiometry of G protein subunits affects the Saccharomyces cerevisiae mating pheromone signal transduction pathway. Mol. Cell. Biol. 10, 510-517.
15. Cook, J.G., Bardwell, L., and Thorner, J. (1997). Inhibitory and activating functions for MAPK Kss1 in the S. cerevisiae filamentous-growth signaling pathway. Nature 390, 85-88.
16. Corvera, S., and Capocasale, R.J. (1990). Enhanced phosphorylation of a coated vesicle polypeptide in response to insulin stimulation of rat adipocytes. J. Biol. Chem. 265, 15963-15969.
17. Elion, E.A., Brill, J.A., and Fink, G.R. (1991a). Functional redundancy in the yeast cell cycle: FUS3 and KSS1 have both overlapping and unique functions. Cold Spring Harbor Symp. Quant. Biol. 56, 41-49.
18. Elion, E.A., Brill, J.A., and Fink, G.R. (1991b). FUS3 represses CLN1 and CLN2 and in concert with KSS1 promotes signal transduction. Proc. Natl. Acad. Sci. USA 88, 9392-9396.
19. Fuller, R.S., Sterne, R.E., and Thorner, J. (1988). Enzymes required for yeast prohormone processing. Annu. Rev. Physiol. 50, 345-362.
20. Gietz, R.D., and Schiestl, R.H. (1995). Transforming Yeast with DNA. Methods Mol. Cell. Biol. 5, 255-269.
21. Glover, C.V., Bidwai, A.P., and Reed, J.C. (1994). Structure and function of Saccharomyces cerevisiae casein kinase II. Cell. & Mol. Biol. Res. 40, 481-488.
22. Hanna, D.E., Rethinaswamy, A., and Glover, C.V. (1995). Casein kinase II is required for cell cycle progression during G1 and G2/M in Saccharomyces cerevisiae. J. Biol. Chem. 270, 25905-25914.
23. Hanson, V.G., Schook, W.J., and Puszkin, S. (1990). Novel regulatory role of phosphorylated clathrin light chain β in bovine brain coated vesicles. J. Neurochem. 54, 46-50.
24. Hill, B.L., Drickamer, K., and Brodsky, F.M. (1988). Identification of the phosphorylation sites of clathrin light chain LCb. J. Biol. Chem. 263, 5499-5501.
25. Huang, K.M., Gullberg, L., Nelson, K.K., Stefan, C.J., Blumer, K., and Lemmon, S.K. (1997). Novel functions of clathrin light chains: clathrin heavy chain trimerization is defective in light chain-deficient yeast. J. Cell Sci. 110, 899-910.
26. Ito, H., Fukada, Y., Murata, K., and Kimura, A. (1982). Transformation of intact yeast cells with alkali cations. J. Bacteriol. 153, 63-168.
27. Keen, J.H., and Black, M.M. (1986). The phosphorylation of coated membrane proteins in intact neurons. J. Cell Biol. 102, 1325-1333.
28. Kemp, B.E., Graves, D.J., Benjamini, E., and Drebs, E.G. (1977). Role of multiple basic residues in determining the substrate specificity of cyclic AMP-dependent protein kinases. J. Biol. Chem. 252, 4888-4894.
29. Kennelly, P.J. (1994). Identification of sites of serine and threonine phosphorylation via site-directed mutagenesis - site transformation versus site elimination. Anal. Biochem. 219, 384-386.
30. Kirchhausen, T., and Harrison, S.C. (1981). Protein organization in clathrin trimers. Cell 23, 755-761.
31. Kunkel, T.A., Roberts, J.D., and Zakour, R.A. (1987). Rapid and efficient site-specific mutagenesis without phenotypic selection. Methods Enzymol. 154, 367-382.
32. Lemmon, S.K., Pellicena-Palle, A., Conley, K., and Freund, C.L. (1991). Sequence of clathrin heavy chain from Saccharomyces cerevisae and requirement of the COOH terminus for clathrin function. J. Cell Biol. 112, 65-80.
33. Ma, D., Cook, J.G., and Thorner, J. (1995). Phosphorylation and localization of Kss1, a MAP kinase of the Saccharomyces cerevisiae pheromone response pathway. Mol. Biol. Cell 6, 889-909.
34. MacKay, V.L., Welch, S.K., Insley, M.Y., Manney, T.R., Holly, J., Saari, G.C., and Parker, M.L. (1988). The Saccharomyces cerevisiae BAR1 gene encodes an exported protein with homology to pepsin. Proc. Natl. Acad. Sci. USA 85, 55-59.
35. Madhani, H.D., Styles, C.A., and Fink, G.R. (1997). MAP kinases with distinct inhibitory functions impart signaling specificity during yeast differentiation. Cell 91, 673-684.
36. Merrese, S., Ludwig T., Frank, R., and Hoflack, B. (1990). Phosphorylation of the cytoplasmic domain of the bovine cation-independent mannose 6-phosphate receptor. J. Biol. Chem. 265, 18833-18842.
37. Mooibroek, M.J., Michiel, D.F., and Wang, J.H. (1992). Differential in vitro phosphorylation of clathrin light chains by the epidermal growth factor receptor-associated protein tyrosine kinase and a pp60c-src-related spleen tyrosine kinase. Arch. Biochem. Biophys. 292, 448-455.
38. Nathke, I., Parham, P., and Brodsky, F.M. (1988). The calcium binding site of clathrin light chains. J. Biol. Chem. 265, 18621-18627.
39. Nomoto, S., Nakayama, N., Arai, K., and Matsumoto, K. (1990). Regulation of the yeast pheromone response pathway by G protein subunits. EMBO J. 9, 691-696.
40. Nothwehr, S.F., and Stevens, T.H. (1994). Sorting of membrane proteins in the yeast secretary pathway. J. Biol. Chem. 269, 10185-10188.
41. Padmanabha, R., Chen-Wu, J.L., Hanna, D.E., and Glover, C.V. (1990). Isolation, sequencing, and disruption of the yeast CKA2 gene: casein kinase II is essential for viability in Saccharomyces cerevisiae. Mol. Cell. Biol. 10, 4089-4099.
42. Payne, G., and Schekman, R. (1985). A test of clathrin function in protein secretion and cell growth. Science 230, 1009-1014.
43. Payne, G.S., and Schekman, R. (1989). Clathrin: a role in the intracellular retention of a Golgi membrane protein. Science 245, 1358-1365.
44. Pearse, B.M.F., and Robinson, M.S. (1990). Clathrin, adaptors, and sorting. Annu. Rev. Cell Biol. 6, 151-171.
45. Peter, M., Gartner, A., Horecka, J., Ammerer, G., and Herskowitz, I. (1993). FAR1 links the signal transduction pathway to the cell cycle machinery in yeast. Cell 73, 747-760.
46. Pishvaee, B., Munn, A., and Payne, G.S. (1997). A novel structural model for regulation of clathrin function. EMBO J. 16, 2227-2239.
47. Posas, F., and Saito, H. (1997). Osmotic activation of the HOG MAPK pathway via Ste11p MAPKKK: scaffold role of Pbs2p MAPKK. Science 276, 1702-1705.
48. Redding, K., Brickner, J., Marschall, L.G., Nichols, J.W., and Fuller, R.S. (1996a). Allele-specific suppression of a defective trans-Golgi network (TGN) localization signal in Kex2p identifies three genes involved in localization of TGN transmembrane proteins. Mol. Cell. Biol. 16, 6206-6217.
49. Redding, K., Seeger, M., Payne, G., and Fuller, R.S. (1996b). 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.
50. Reneke, J.E., Blumer, K.J., Courchesne, W.E., and Thorner, J. (1988). The carboxy-terminal segment of the yeast α-factor receptor is a regulatory domain. Cell 55, 221-234.
51. Rethinaswamy, A., Birnbaum, M.J., and Glover, C.V. (1998). Temperature-sensitive mutations of the CKA1 gene reveal a role for casein kinase II in maintenance of cell polarity in Saccharomyces cerevisiae. J. Biol. Chem. 273, 5869-5877.
52. Rubin, G.M. (1975). Preparation of RNA and ribosomes from yeast. Methods Cell Biol. 12, 45-64.
53. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual, Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
54. Schmid, S.L. (1997). Clathrin-coated vesicle formation and protein sorting: an integrated process. Annu. Rev. Biochem. 66, 511-548.
55. Schook, W.J., and Puszkin, S. (1985). Brain clathrin light chain 2 can be phosphorylated by a coated vesicle kinase. Proc. Natl. Acad. Sci. USA 82, 8039-8043.
56. Seeger, M., and Payne, G.S. (1992a). A role for clathrin in the sorting of vacuolar proteins in the Golgi complex of yeast. EMBO J. 11, 2811-2818.
57. Seeger, M., and Payne, G.S. (1992b). Selective and immediate effects of clathrin heavy chain mutations on Golgi membrane protein retention in Saccharomyces cerevisiae. J. Cell Biol. 118, 531-540.
58. Sherman, F., Fink, G., and Lawrence, C. (1974). Methods in Yeast Genetics, Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
59. 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.
60. Silveira, L.A., Wong, D.H., Masiarz, F.R., and Schekman, R. (1990). Yeast clathrin has a distinctive light chain that is important for cell growth. J. Cell Biol. 111, 1437-1449.
61. Sprague, G.F., and Thorner, J.W. (1992). Pheromone response and signal transduction during the mating process of Saccharomyces cerevisiae. In: The Molecular and Cellular Biology of the Yeast Saccharomyces, ed. E.W. Jones, J.R. Pringle, and J.R. Broach, Cold Spring Harbor, NY: Cold Spring Harbor Laboratory, 657-774.
62. Tedford, K., Kim, S., Sa, D., Stevens, K., and Tyers, M. (1997). Regulation of the mating pheromone and invasive growth responses in yeast by two MAP kinase substrates. Curr. Biol. 7, 228-238.
63. Tuazon, P.T., and Traugh, J.A. (1991). Casein kinase I and II-multiple serine protein kinases: structure, function, and regulation. Adv. Second Messenger Phoshoprotein Res. 23, 123-164.
64. Ungewickell, E., and Branton, D. (1981). Assembly units of clathrin coats. Nature 289, 420-422.
65. Usami, M., Takahashi, A., Kadota, T., and Katoda, K. (1985). Phosphorylation of a clathrin light chain of coated vesicles in the presence of histones. J. Biochem. 97, 1819-1822.
66. Whiteway, M., Hougan, L., and Thomas, D.Y. (1990). Overexpression of the STE4 gene leads to mating response in haploid Saccharomyces cerevisiae. Mol. Cell. Biol. 10, 217-222.
67. Wilde, A., and Brodsky, F.M. (1996). In vivo phosphorylation of adaptors regulates their interaction with clathrin. J. Cell Biol. 135, 635-645.
68. Wilsbach, K., and Payne, G.S. (1993a). Dynamic retention of TGN proteins in Saccharomyces cerevisiae. Trends Cell Biol. 3, 426-431.
69. Wilsbach, K., and Payne, G.S. (1993b). Vps1p, a member of the dynamin GTPase family, is necessary for Golgi membrane protein retention in S. cerevisiae. EMBO J. 8, 3049-3059.