Cyclin partners determine Pho85 protein kinase substrate specificity in vitro and in vivo: Control of glycogen biosynthesis by Pcl8 and Pcl10

Molecular and Cellular Biology

Volumn 18, Issue 6, 1998, Pages 3289-3299

  Huang, Dongqing ^a,b   Moffat, Jason ^b   Wilson, Wayne A ^a   Moore, Lynda ^b   Cheng, Christine ^a   Roach, Peter J ^a   Andrews, Brenda ^b  

^a INDIANA UNIVERSITY   (United States)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ACID PHOSPHATASE; CYCLIN DEPENDENT KINASE; CYCLINE; GLYCOGEN; GLYCOGEN SYNTHASE;

ARTICLE; CELL GROWTH; CELL STRUCTURE; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; GENE CONTROL; GENE DISRUPTION; GENE EXPRESSION REGULATION; GLYCOGEN SYNTHESIS; NONHUMAN; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE;

SACCHAROMYCES CEREVISIAE;

EID: 0031844386     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.18.6.3289     Document Type: Article

References (81)

1. Aerne, B. L., A. L. Johnson, J. H. Toyn, and L. H. Johnston. 1998. Swi5 controls a novel wave of cyclin synthesis in late mitosis. Mol. Biol. Cell 9:945-956.
2. Bai, C., and S. Elledge. 1997. Gene identification using the yeast two-hybrid system. Methods Enzymol. 283:141-156.
3. Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
4. Cannon, J. F., J. R. Pringle, A. Fiechter, and M. Khalil. 1994. Characterization of glycogen-deficient glc mutants of Saccharomyces cerevisiae. Genetics 136:485-503.
5. Cheng, C., D. Huang, and P. J. Roach. 1997. Yeast PIG genes: PIG1 encodes a putative type 1 phosphatase subunit that interacts with the yeast glycogen synthase Gsy2p. Yeast 13:1-8.
6. Cheng, C., J. Mu, I. Farkas, D. Huang, M. G. Goebl, and P. J. Roach. 1995. Requirement of the self-glucosylating initiator proteins Glg1p and Glg2p for glycogen accumulation in Saccharomyces cerevisiae. Mol. Cell. Biol. 15:6632-6640.
7. Cheng, C., and P. J. Roach. 1998. Unpublished results.
8. Chien, C. T., P. L. Bartel, R. Sternglanz, and S. Fields. 1991. The two-hybrid system: a method to identify and clone genes for proteins that interact with a protein of interest. Proc. Natl. Acad. Sci. USA 88:9578-9582.
9. Christianson, T. W., R. S. Sikorski, M. Dante, J. H. Shero, and P. Hieter. 1992. Multifunctional yeast high-copy-number shuttle vectors. Gene 110: 119-122.
10. Coche, T., D. Prozzi, M. Legrain, F. Hilger, and J. Vandenhaute. 1990. Nucleotide sequence of the PHO81 gene involved in the regulation of the repressible acid phosphatase gene in Saccharomyces cerevisiae. Nucleic Acids Res. 18:2176.
11. Creasy, C. L., S. L. Madden, and L. W. Bergman. 1993. Molecular analysis of the PHO81 gene of Saccharomyces cerevisiae. Nucleic Acids Res. 21:1975-1982.
12. Durfee, T., K. Becherer, P. L. Chen, S. H. Yeh, Y. Yang, A. E. Kilburn, W. H. Lee, and S. J. Elledge. 1993. The retinoblastoma protein associates with the protein phosphatase type 1 catalytic subunit. Genes Dev. 7:555-569.
13. Dynlacht, B. D., O. Flores, J. A. Lees, and E. Harlow. 1994. Differential regulation of E2F transactivation by cyclin/cdk2 complexes. Genes Dev. 8:1772-1786.
14. Espinoza, F. H., J. Ogas, I. Herskowitz, and D. O. Morgan. 1994. Cell cycle control by a complex of the cyclin HCS26 (PCL1) and the kinase PHO85. Science 266:1388-1391.
15. Farkas, I., T. A. Hardy, A. A. DePaoli-Roach, and P. J. Roach. 1990. Isolation of the GSY1 gene encoding yeast glycogen synthase and evidence for the existence of a second gene. J. Biol. Chem. 265:20879-20886.
16. Farkas, I., T. A. Hardy, M. G. Goebl, and P. J. Roach. 1991. Two glycogen synthase isoforms in Saccharomyces cerevisiae are coded by distinct genes that are differentially controlled. J. Biol. Chem. 266:15602-15607.
17. Feng, Z. H., S. E. Wilson, Z. Y. Peng, K. K. Schlender, E. M. Reimann, and R. J. Trumbly. 1991. The yeast GLC7 gene required for glycogen accumulation encodes a type 1 protein phosphatase. J. Biol. Chem. 266:23796-23801.
18. François, J. M., J. Blazquez, J. Arino, and C. Gancedo. 1997. Storage carbohydrates in the yeast Saccharomyces cerevisiae, p. 285-311. In F. K. Zimmermann and K.-D. Entian (ed.), Yeast sugar metabolism: biochemistry, genetics, biotechnology. Technomic, Lancaster, Pa.
19. Francois, J. M., S. Thompson-Jaeger, J. Skroch, U. Zellenka, W. Spevak, and K. Tatchell. 1992. GAC1 may encode a regulatory subunit for protein phosphatase type 1 in Saccharomyces cerevisiae. EMBO J. 11:87-96.
20. Gibbs, E., Z. Q. Pan, H. Niu, and J. Hurwitz. 1996. Studies on the in vitro phosphorylation of HSSB-p34 and -p107 by cyclin-dependent kinases. Cyclin-substrate interactions dictate the efficiency of phosphorylation. J. Biol. Chem. 271:22847-22854.
21. Gilliquet, V., and G. Berben. 1993. Positive and negative regulators of the Saccharomyces cerevisiae 'PHO system' participate in several cell functions. FEMS Microbiol. Lett. 108:333-339.
22. Guthrie, C., and R. Fink. 1991. Methods in enzymology, vol. 194. Guide to yeast genetics and molecular biology. Academic Press, New York, N.Y.
23. Hardy, T. A., D. Huang, and P. J. Roach. 1994. Interactions between cAMP-dependent and SNF1 protein kinases in the control of glycogen accumulation in Saccharomyces cerevisiae. J. Biol. Chem. 269:27907-27913.
24. Hardy, T. A., and P. J. Roach. 1993. Control of yeast glycogen synthase-2 by COOH-terminal phosphorylation. J. Biol. Chem. 268:23799-23805.
25. Harper, J. W., G. R. Adami, N. Wei, K. Keyomarsi, and S. J. Elledge. 1993. The p21 Cdk-interacting protein Cip1 is a potent inhibitor of G1 cyclin-dependent kinases. Cell 75:805-816.
26. Higashi, H., I. Suzuki-Takabashi, Y. Taya, K. Segawa, S. Nishimura, and M. Kitagawa. 1995. Differences in substrate specificity between Cdk2-cyclin A and Cdk2-cyclin E in vitro. Biochem. Biophys. Res. Commun. 216:520-525.
27. Higuchi, R. 1990. Recombinant PCR, p. 177-83. In M. A. Innis, D. H. Gelfand, J. J. Sninsky, and T. J. White (ed.), PCR protocols: a guide to methods and applications. Academic Press, San Diego, Calif.
28. Hirst, K., F. Fisher, P. C. McAndrew, and C. R. Goding. 1994. The transcription factor, the Cdk, its cyclin and their regulator: directing the transcriptional response to a nutritional signal. EMBO J. 13:5410-5420.
29. Hoffmann, I., P. R. Clarke, M. J. Marcote, E. Karsenti, and G. Draetta. 1993. Phosphorylation and activation of human cdc25-C by cdc2-cyclin B and its involvement in the self-amplification of MPF at mitosis. EMBO J. 12:53-63.
30. Holmes, J. K., and M. J. Solomon. 1996. A predictive scale for evaluating cyclin-dependent kinase substrates. A comparison of p34cdc2 and p33cdk2. J. Biol. Chem. 271:25240-25246.
31. Horton, L. E., and D. J. Templeton. 1997. The cyclin box and C-terminus of cyclins A and E specify CDK activation and substrate specificity. Oncogene 14:491-498.
32. Huang, D., K. T. Chun, M. G. Goebl, and P. J. Roach. 1996. Genetic interactions between REG1/HEX2 and GLC7, the gene encoding the protein phosphatase type 1 catalytic subunit in Saccharomyces cerevisiae. Genetics 143:119-127.
33. Huang, D., I. Farkas, and P. J. Roach. 1996. Pho85p, a cyclin-dependent protein kinase, and the Snf1p protein kinase act antagonistically to control glycogen accumulation in Saccharomyces cerevisiae. Mol. Cell. Biol. 16:4357-4365.
34. Huang, D., V. Measday, P. J. Roach, and B. Andrews. 1997. Unpublished results.
35. Huang, D., and P. J. Roach. 1997. Unpublished results.
36. Huang, D., W. A. Wilson, and P. J. Roach. 1997. Glucose-6-P control of glycogen synthase phosphorylation in yeast. J. Biol. Chem. 272:22495-22501.
37. Johnston, M., and M. Carlson. 1992. Regulation of carbon and phosphate utilization, p. 193-281. In E. W. Jones, J. R. Pringle, and J. R. Broach (ed.), The molecular biology of the yeast Saccharomyces. Gene expression, vol. 2. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
38. Kaffman, A., I. Herskowitz, R. Tjian, and E. K. O'Shea. 1994. Phosphorylation of the transcription factor PHO4 by a cyclin-CDK complex, PHO80-PHO85. Science 263:1153-1156.
39. Kellogg, D. R., A. Kikuchi, T. Fujii-Nakata, C. W. Turck, and A. W. Murray. 1995. Members of the NAP/SET family of proteins interact specifically with B-type cyclins. J. Cell Biol. 130:661-673.
40. Kennelly, P. J., and E. G. Krebs. 1991. Consensus sequences as substrate specificity determinants for protein kinases and protein phosphatases. J. Biol. Chem. 266:15555-15558.
41. Kitagawa, M., H. Higashi, H. K. Jung, I. Suzuki-Takahashi, M. Ikeda, K. Tamai, J. Kato, K. Segawa, E. Yoshida, S. Nishimura, and Y. Taya. 1996. The consensus motif for phosphorylation by cyclin D1-Cdk4 is different from that for phosphorylation by cyclin A/E-Cdk2. EMBO J. 15:7060-7069.
42. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
43. Lenburg, M. E., and E. K. O'Shea. 1996. Signaling phosphate starvation. Trends Biochem. Sci. 21:383-387.
44. Madden, S. L., C. L. Creasy, V. Srinivas, W. Fawcett, and L. W. Bergman. 1988. Structure and expression of the PHO80 gene of Saccharomyces cerevisiae. Nucleic Acids Res. 16:2625-2637.
45. Measday, V., and B. Andrews. 1998. The cyclin family of budding yeast: abundant use of a good idea. Trends Genet. 14:66-72.
46. Measday, V., L. Moore, J. Ogas, M. Tyers, and B. Andrews. 1994. The PCL2 (ORFD)-PHO85 cyclin-dependent kinase complex: a cell cycle regulator in yeast. Science 266:1391-1395.
47. Measday, V., L. Moore, R. Retnakaran, J. Lee, M. Donoviel, A. M. Neiman, and B. Andrews. 1997. A family of cyclin-like proteins that interact with the Pho85 cyclin-dependent kinase. Mol. Cell. Biol. 17:1212-1223.
48. Moore, L., and B. Andrews. 1992. Mutational analysis of a DNA sequence involved in linking gene expression to the cell cycle. Biochem. Cell Biol. 70:1073-1080.
49. Morgan, D. O. 1996. The dynamics of cyclin dependent kinase structure. Curr. Opin. Cell Biol. 8:767-772.
50. Morgan, D. O. 1995. Principles of CDK regulation. Nature 374:131-134.
51. Nasmyth, K. 1993. Control of the yeast cell cycle by the Cdc28 protein kinase. Curr. Opin. Cell Biol. 5:166-179.
52. Nigg, E. A. 1995. Cyclin-dependent protein kinases: key regulators of the eukaryotic cell cycle. Bioessays 17:471-480.
53. O'Neill, E. M., A. Kaffman, E. R. Jolly, and E. K. O'Shea. 1996. Regulation of PHO4 nuclear localization by the PHO80-PHO85 cyclin-CDK complex. Science 271:209-212.
54. Oshima, Y. 1982. Regulatory circuits for gene expression: the metabolism of galactose and phosphate, p. 159-180. In J. N. Strathern, E. W. Jones, and J. R. Broach (ed.), The molecular biology of the yeast Saccharomyces cerevisiae: metabolism and gene expression. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
55. Pearson, R. B., and B. E. Kemp. 1991. Protein kinase phosphorylation site sequences and consensus specificity motifs: tabulations. Methods Enzymol. 200:62-81.
56. Peeper, D. S., L. L. Parker, M. E. Ewen, M. Toebes, F. L. Hall, M. Xu, A. Zantema, A. J. van der Eb, and H. Piwnica-Worms. 1993. A-and B-type cyclins differentially modulate substrate specificity of cyclin-cdk complexes. EMBO J. 12:1947-1954.
57. Peng, Z. Y., R. J. Trumbly, and E. M. Reimann. 1990. Purification and characterization of glycogen synthase from a glycogen-deficient strain of Saccharomyces cerevisiae. J. Biol. Chem. 265:13871-13877.
58. Pinna, L. A., and M. Ruzzene. 1996. How do protein kinases recognize their substrates? Biochim. Biophys. Acta 1314:191-225.
59. Platt, T., B. Muller-Hill, and J. H. Miller. 1972. Assay of β-galactosidase, p. 352-355. In J. H. Miller (ed.), Experiments in molecular genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
60. Ronne, H. 1995. Glucose repression in fungi. Trends Genet. 11:12-17.
61. Rowen, D. W., M. Meinke, and D. C. LaPorte. 1992. GLC3 and GHA1 of Saccharomyces cerevisiae are allelic and encode the glycogen branching enzyme. Mol. Cell. Biol. 12:22-29.
62. Russo, A. A., P. D. Jeffrey, A. K. Patten, J. Massague, and N. P. Pavletich. 1996. Crystal structure of the p27Kip1 cyclin-dependent-kinase inhibitor bound to the cyclin A-Cdk2 complex. Nature 382:325-331.
63. Schneider, K. R., R. L. Smith, and E. K. O'Shea. 1994. Phosphate-regulated inactivation of the kinase PHO80-PHO85 by the CDK inhibitor PHO81. Science 266:122-126.
64. 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.
65. Skurat, A. V., and P. J. Roach. 1995. Regulation of glycogen biosynthesis, p. 213-222. In D. LeRoith, J. E. Olefsky, and S. Taylor (ed.), Diabetes mellitus: a fundamental and clinical text. J. B. Lippincott Company, Philadelphia, Pa.
66. Songyang, Z., S. Blechner, N. Hoagland, M. F. Hoekstra, H. Piwnica-Worms, and L. C. Cantley. 1994. Use of an oriented peptide library to determine the optimal substrates of protein kinases. Curr. Biol. 4:973-982.
67. Songyang, Z., K. P. Lu, Y. T. Kwon, L.-H. Tsai, O. Filhol, C. Cochet, D. A. Brickey, T. R. Soderling, C. Bartleson, D. J. Graves, A. J. DeMaggio, M. F. Hoekstra, J. Blenis, T. Hunter, and L. C. Cantley. 1996. A structural basis for substrate specificities of protein Ser/Thr kinases: primary sequence preference of casein kinases I and II, NIMA, phosphorylase kinase, calmodulin-dependent kinase II, CDK5, and Erkl. Mol. Cell. Biol. 16:6486-6493.
68. Stuart, J. S., D. L. Frederick, C. M. Varner, and K. Tatchell. 1994. The mutant type 1 protein phosphatase encoded by glc7-1 from Saccharomyces cerevisiae fails to interact productively with the GAC1-encoded regulatory subunit. Mol. Cell. Biol. 14:896-905.
69. 14C]glucose. Biochim. Biophys. Acta 582:543-547.
70. Taya, Y. 1997. RB kinases and RB-binding proteins: new points of view. Trends Biochem. Sci. 22:14-17.
71. Tennyson, C., J. Lee, and B. Andrews. A role for the Pc19-Pho85 cyclin-cdk complex at the M/G1 boundary in S. cerevisiae. Mol. Microbiol., in press.
72. 14C-glucose. Anal. Biochem. 25:486-499.
73. Thompson-Jaeger, S., J. Francois, J. P. Gaughran, and K. Tatchell. 1991. Deletion of SNF1 affects the nutrient response of yeast and resembles mutations which activate the adenylate cyclase pathway. Genetics 129:697-706.
74. Thon, V. J., C. Vigneron-Lesens, T. Marianne-Pepin, J. Montreuil, A. Decq, C. Rachez, S. G. Ball, and J. F. Cannon. 1992. Coordinate regulation of glycogen metabolism in the yeast Saccharomyces cerevisiae. Induction of glycogen branching enzyme. J. Biol. Chem. 267:15224-15228.
75. Timblin, B. K., K. Tatchell, and L. W. Bergman. 1996. Deletion of the gene encoding the cyclin-dependent protein kinase Pho85 alters glycogen metabolism in Saccharomyces cerevisiae. Genetics 143:57-66.
76. Toh-e, A., K. Tanaka, Y. Uesono, and R. B. Wickner. 1988. PHO85, a negative regulator of the PHO system, is a homolog of the protein kinase gene, CDC28, of Saccharomyces cerevisiae. Mol. Gen. Genet. 214:162-164.
77. Torriani, A. 1960. Influence of organic phosphate on the formation of acid phosphatases by Escherichia coli. Biochim. Biophys. Acta 38:460-469.
78. Tyers, M., G. Tokiwa, R. Nash, and B. Futcher. 1992. The Cln3-Cdc28 kinase complex of S. cerevisiae is regulated by proteolysis and phosphorylation. EMBO J. 11:1773-1784.
79. Uesono, Y., K. Tanaka, and A. Toh-e. 1987. Negative regulators of the PHO system in Saccharomyces cerevisiae: isolation and structural characterization of PHO85. Nucleic Acids Res. 15:10299-10309.
80. Uesono, Y., M. Tokai, K. Tanaka, and A. Toh-e. 1992. Negative regulators of the PHO system of Saccharomyces cerevisiae: characterization of PHO80 and PHO85. Mol. Gen. Genet. 231:426-432.
81. Zarkowska, T., and S. Mittnacht. 1997. Differential phosphorylation of the retinoblastoma protein by G1/S cyclin-dependent kinases. J. Biol. Chem. 272:12738-12746.