Suppressors of YCK-encoded yeast casein kinase 1 deficiency define the four subunits of a novel clathrin AP-like complex

EMBO Journal

Volumn 16, Issue 14, 1997, Pages 4194-4204

  Panek, Heather R ^a   Stepp, J David ^b   Engle, Holly M ^c   Marks, Kim M ^a   Tan, Philip K ^d,e   Lemmon, Sandra K ^b   Robinson, Lucy C ^a  

^a LOUISIANA STATE UNIV MEDICAL CENTER   (United States)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c MORAVIAN COLLEGE   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Casein kinase 1; Clathrin adaptors; Vesicular trafficking

Indexed keywords

CASEIN KINASE I; CLATHRIN; FUNGAL PROTEIN; PROTEIN SUBUNIT;

ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; ENDOCYTOSIS; ENZYME DEFICIENCY; FUNGUS GROWTH; FUNGUS MUTANT; NONHUMAN; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE; SUPPRESSOR GENE; YEAST;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; BLOTTING, WESTERN; CASEIN KINASE I; CASEIN KINASES; CELL DIVISION; CLATHRIN; DNA MUTATIONAL ANALYSIS; ENDOCYTOSIS; ENDOSOMES; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; MONOMERIC CLATHRIN ASSEMBLY PROTEINS; MORPHOGENESIS; NERVE TISSUE PROTEINS; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN CONFORMATION; PROTEIN KINASES; RECEPTORS, CELL SURFACE; RECEPTORS, G-PROTEIN-COUPLED; RECEPTORS, MATING FACTOR; RECEPTORS, PHEROMONE; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SUPPRESSION, GENETIC;

FUNGI; SACCHAROMYCES CEREVISIAE;

EID: 0030743354     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/16.14.4194     Document Type: Article

References (55)

1. Altschul, S.F., Gish, W., Miller, W., Myers, E.W. and Lipman, D.J. (1990) Basic local alignment search tool. J. Mol. Biol., 215, 403-410.
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., 263, 4408-4415.
3. Brockman, J.L., Gross, S.D., Sussman, M.R. and Anderson, R.A. (1992) Cell cycle-dependent localization of casein kinase I to mitotic spindles. Proc. Natl Acad. Sci. USA, 89, 9454-9458.
4. Chuang, J.S. and Schekman, R.W. (1996) Differential trafficking and timed localization of two chitin synthase proteins, Chs2p and Chs3p. J. Cell Biol., 135, 597-610.
5. Cukierman, E., Huber, I., Rotman, M. and Cassel, D. (1995) The ARF1 GTPase-activating protein: zinc tinger motif and Golgi complex localization. Science, 270, 1999-2002.
6. Davis, N.G., Horecka, J.L. and Sprague, J.G.F., III (1993) Cis- and transacting functions required for endocytosis of the yeast pheromone receptors. J. Cell Biol., 122, 53-65.
7. Dell'Angelica, E.C., Ohno, H., Ooi, C.E., Rabinovich, E., Roche, K.W. and Bonifacino, J.S. (1997) An adaptor-like complex with ubiquitous expression. EMBO J., 5, 917-928.
8. DeMaggio, A.J., Lindberg, R.A., Hunter, T. and Hoekstra, M.F. (1992) The budding yeast HRR25 gene product is a casein kinase I isoform. Proc. Natl Acad. Sci. USA, 89, 7008-7012.
9. Feldmann, H., Aigle, M. and Aljinovic, G. (1994) Complete DNA sequence of yeast chromosome II. EMBO J., 13, 5795-5809.
10. Fish, K.J., Cegielska, A., Getman, M.E., Landes, G.M. and Virshup, D.M. (1995) Isolation and characterization of human casein kinase Iε (CKI), a novel member of the CKI gene family. J. Biol. Chem., 270, 14875-14883.
11. Givan, S.A. and Sprague, G.F., Jr (1997) The ankyrin repeat-containing protein Akr1p is required for the endocytosis of yeast pheromone receptors. Mol. Biol. Cell, in press.
12. Graves, P.R., Haas, D.W., Hagedorn, C.H., DePaoli-Roach, A.A. and Roach, P.J. (1993) Molecular cloning, expression, and characterization of a 49-kilodalton casein kinase I isoform from rat testis. J. Biol. Chem., 268, 6394-6401.
13. Gross, S.D., Hoffman, D.P., Fisette, P.L., Baas, P. and Anderson, R.A. (1995) A phosphatidylinositol 4,5 bis phosphate-sensitive casein kinase Iα associates with synaptic vesicles and phosphorylates a subset of vesicle proteins. J. Cell Biol., 130, 711-724.
14. Hicke, L. and Riezman, H. (1996) Ubiquitination of a yeast plasma membrane receptor signals its ligand-stimulated endocytosis. Cell, 84, 277-287.
15. Hoekstra, M.F., Liskay, R.M., Ou, A.C., DeMaggio, A.J., Burbee, D.J. and Heffron, F. (1991) HRR25, a putative protein kinase from budding yeast: association with repair of damaged DNA. Science, 253, 1031-1034.
16. Hoffman, C.S. and Winston, F. (1987) A ten-minute DNA preparation from yeast efficiently releases autonomous plasmids for transformation of Escherichia coli. Gene, 57, 267-272.
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. Kirchhausen, T. (1990) Identification of a putative yeast homolog of the mammalian beta chains of the clathrin-associated protein complexes. Mol. Cell. Biol., 10, 6089-6090.
19. Kirchhausen, T., Davis, A.C., Frucht, S., Greco, B.O., Payne, G.S, and Tubb, B. (1991) AP17 and AP19, the mammalian small chains of the clathrin-associated protein complexes, show homology to Yap17p, their putative homolog in yeast. J. Biol. Chem., 266, 11153-11157.
20. Maniatis, T., Fritsch, E.F. and Sambrook, J. (1982) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
21. Nakayama, Y., Goebl, M., O'Brine, B.G., Lemmon, S., Chow, E.P. and Kirchhausen, T. (1991) The medium chains of the mammalian clathrin-associated proteins have a homolog in yeast. Eur. J. Biochem., 202, 569-574.
22. 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.
23. Page, L.J. and Robinson, M.S. (1995) Targeting signals and subunit interactions in coated vesicle adaptor complexes. J. Cell Biol., 131, 619-630.
24. Pauloin, A. and Thurieau, C. (1994) The 50 kDa protein subunit of assembly polypeptide (AP) AP-2 adapter from clathrin-coated vesicles is phosphorylated on threonine-156 by AP-1 and a soluble AP50 kinase which co-purifies with the assembly polypeptides. Biochem. J., 296, 409-415.
25. Pearse, B.M.F. and Robinson, M.S. (1990) Clathrin, adaptors, and sorting. Annu. Rev. Cell Biol., 6, 151-171.
26. 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.
27. Poon, P.P., Wang, X.M., Rotman, M., Huber, I., Cukierman, E., Cassel, D., Singer, R.A. and Johnston, G.C. (1996) Saccharomyces cerevisiae Gcs1 is an ADP-ribosylation factor GTPase-activating protein. Proc. Natl Acad. Sci. USA, 93, 10074-10077.
28. Rad, M.R., Phan, H.L., Kirchrath, L., Tan, P.K., Kirchhausen, T., Hollenberg, C.P. and Payne, G.S. (1995) Saccharomyces cerevisiae Ap12p, a homologue of the mammalian clathrin AP β subunit, plays a role in clathrin-dependem Golgi functions. J. Cell Sci., 108, 1605-1615.
29. Roach, P.J. (1990) Control of glycogen synthase by hierarchical protein phosphorylation. FASEB J., 4, 2961-2968.
30. Robinson, L.C. et al. (1992) Yeast casein kinase I homologues: an essential gene pair. Proc. Natl. Acad. Sci. USA, 89, 28-32.
31. Robinson, L.C., Menold, M.M., Garrett, S. and Culbertson, M.R. (1993) Casein kinase I-like protein kinases encoded by YCK1 and YCK2 are required for yeast morphogenesis. Mol. Cell. Biol., 13, 2870-2880.
32. Rose, M.D., Novick, P. Thomas, J.H., Botstein, D. and Fink, G.R. (1987) A Saccharomyces cerevisiae genomic plasmid bank based on a centromere-containing shuttle vector. Gene, 60, 237-243.
33. Roth, A.F. and Davis, N.G. (1996) Ubiquitination of the yeast a-factor receptor. J. Cell Biol., 134, 661-674.
34. Rothstein, R.J. (1983) One-step gene disruption in yeast. Methods Enzymol., 101, 202-210.
35. Rowles, J., Slaughter, C., Moomaw, C., Hsu, J. and Cobb, M.H. (1991) Purification of casein kinase I and isolation of cDNAs encoding multiple casein kinase I-like enzymes. Proc. Natl Acad. Sci. USA, 88, 9548-9552.
36. Sambrook, J., Fritsch, E.F. and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
37. Seaman, N.J., Sowerby, P.J. and Robinson, M.S. (1996) Cytosolic and membrane-associated proteins involved in the recruitment of AP-1 adaptors onto the trans-Golgi network. J. Biol. Chem., 271, 25446-25451.
38. Seeger, M. and Payne, G.S. (1992) Selective and immediate effects of clathrin heavy chain mutations on Golgi membrane protein retention in Saccharomyces cerevisiae. J. Cell Biol., 118, 531-540.
39. Sherman, F., Fink, G.R. and Hicks, J.B. (1986) Methods in Yeast Genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
40. 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.
41. Simpson, F., Peden, A.A., Christopolou, L. and Robinson, M.S. (1997) Characterization of the adaptor-related protein complex, AP-3. J. Cell Biol., 137, 835-845.
42. Stamnes, M.A. and Rothman, J.E. (1993) The binding of AP-1 clathrin adaptor particles to Golgi membranes requires ADP-ribosylation factor, a small GTP-binding protein. Cell, 73, 999-1005.
43. Stepp, J.D., Pellicena-Palle, A., Hamilton, S., Kirchhausen, T. and Lemmon, S.K. (1995) A late Golgi sorting function for Saccharomyces cerevisiae Apm1p, but not for Apm2p, a second yeast clathrin AP medium chain-related protein. Mol. Biol. Cell, 6, 41-58.
44. Sullivan, M.A., Cannon, J.F., Webb, F.H. and Bock, R.M. (1985) Antisuppressor mutation in Escherichia coli defective in biosynthesis of 5-methylaminomethyl-2-thiouridine. J. Bacteriol., 161, 368-376.
45. Traub, L.M., Ostrom, J.A. and Kornfeld, S. (1993) Biochemical dissection of AP-1 recruitment onto Golgi membranes. J. Cell Biol., 123, 561-573.
46. Tuazon, P.T. and Traugh, J.A. (1991) Casein kinase I and II-multipotential serine kinases: structure, function and regulation. Adv. Second Messenger Phosphoprotein Res., 23, 123-164.
47. Vancura, A., O'Connor, A., Patterson, S.D., Mirza, U., Chait, B.T. and Kuret, J. (1993) Isolation and properties of YCK2, a Saccharomyces cerevisiae homolog of casein kinase I. Arch. Biochem. Biophys., 305, 47-53.
48. Vancura, A., Sessler, A., Leichus, B. and Kuret, J. (1994) A prenylation motif is required for plasma membrane localization and biochemical function of casein kinase I in budding yeast. J. Biol. Chem., 269, 19271-19278.
49. Wang, P.-C., Vancura, A., Mitcheson, T.G. and Kuret, J. (1992) Two genes in Saccharomyces cerevisiae encode a membrane bound form of casein kinase-1. Mol. Biol. Cell, 3, 275-286.
50. Wang, X., Hoekstra, M.F., DeMaggio, A.J., Dhillon, N., Vancura, A., Kuret, J., Johnston, G.C. and Singer, R.A. (1996) Prenylated isoforms of yeast casein kinase I, including the novel Yck3p, suppress the gcs1 blockage of cell proliferation from stationary phase. Mol. Cell. Biol., 16, 5375-5385.
51. Watanabe, T.K., Shimizu, F., Nagata, M., Takaichi, A., Fujiwara, T., Nakamura, Y., Takahashi, E. and Hirai, Y. (1996) Cloning, expression pattern and mapping to 12p13.2→p13.1 of CLAPS3, a gene encoding a novel clathrin-adaptor small chain. Cytogenet. Cell Genet., 73, 214-217.
52. Wilde, A. and Brodsky, F.M. (1996) In vivo phosphorylation of adaptors regulates their interaction with clathrin. J. Cell Biol., 135, 635-645.
53. Zanolari, B., Raths, S., Singer-Kruger, B. and Riezman, H. (1992) Yeast pheromone receptor endocytosis and hyperphosphorylation are independent of G protein-mediated signal transduction. Cell, 71, 755-763.
54. Zhai, L., Graves, P.R., Robinson, L.C., Italiano, M., Culbertson, M.R., Rowles, J., Cobb, M.H., DePaoli-Roach, A.A. and Roach, P.J. (1995) Casein kinase Iγ subfamily: molecular cloning, expression and characterization of three mammalian isoforms, and complementation of defects in the Saccharomyces cerevisiae YCK genes. J. Biol. Chem., 270, 12717-12724.
55. Ziman, M., Chuang, J.S. and Schekman, R.W. (1996) Chs1p and Chs3p, two proteins involved in chitin synthesis, populate a compartment of the Saccharomyces cerevisiae endocytic pathway. Mol. Biol. Cell, 7, 1909-1919.