Schizosaccharomyces pombe AGC family kinase Gad8p forms a conserved signaling module with TOR and PDK1-like kinases

EMBO Journal

Volumn 22, Issue 12, 2003, Pages 3073-3083

  Matsuo, Tomohiko ^a   Kubo, Yoshiya ^a   Watanabe, Yoshinori ^b   Yamamoto, Masayuki ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

AGC family kinase; PDK1 like kinase; Sexual development; Stress response; TOR kinase

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC GMP DEPENDENT PROTEIN KINASE; PHOSPHOINOSITIDE DEPENDENT KINASE 1; PROTEIN KINASE C; PROTEIN SERINE THREONINE KINASE; SERINE; TARGET OF RAPAMYCIN KINASE; THREONINE; UNCLASSIFIED DRUG;

ARTICLE; CELL GROWTH; ENZYME ACTIVITY; EUKARYOTE; FUNGUS GROWTH; GENE DISRUPTION; HYDROPHOBICITY; NONHUMAN; PHENOTYPE; PHOSPHORYLATION; PRIORITY JOURNAL; SCHIZOSACCHAROMYCES POMBE; SEXUAL DEVELOPMENT; SIGNAL TRANSDUCTION; STRESS;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; HUMANS; MUTATION; PHOSPHORYLATION; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); PROTEIN KINASES; PROTEIN-SERINE-THREONINE KINASES; SACCHAROMYCES CEREVISIAE PROTEINS; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS; SERINE; SIGNAL TRANSDUCTION;

EUKARYOTA; FUNGI; MAMMALIA; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE;

EID: 0037600512     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/cdg298     Document Type: Article

References (51)

1. Alessi, D.R. (2001) Discovery of PDK1, one of the missing links in insulin signal transduction. Colworth Medal Lecture. Biochem. Soc. Trans, 29, 1-14.
2. Alessi, D.R., Kozlowski, M.T., Weng, Q.P., Morrice, N. and Avruch, J. (1998) 3-Phosphoinositide-dependent protein kinase 1 (PDK1) phosphorylates and activates the p70 S6 kinase in vivo and in vitro. Curr. Biol., 8, 69-81.
3. Bahler, J., Wu, J.Q., Longtine, M.S., Shah, N.G., McKenzie, A.,III, Steever, A.B., Wach, A., Philippsen, P. and Pringle, J.R. (1998) Heterologous modules for efficient and versatile PCR-based gene targeting in Schizosaccharomyces pombe. Yeast, 14, 943-951.
4. Biondi, R.M., Kieloch, A., Currie, R.A., Deak, M. and Alessi, D.R. (2001) The PIF-binding pocket in PDK1 is essential for activation of S6K and SGK, but not PKB. EMBO J., 20, 4380-4390.
5. Burnett, P.E., Barrow, R.K., Cohen, N.A., Snyder, S.H. and Sabatini, D.M. (1998) RAFT1 phosphorylation of the translational regulators p70 S6 kinase and 4E-BP1. Proc. Natl Acad. Sci. USA, 95, 1432-1437.
6. Casamayor, A., Torrance, P.D., Kobayashi, T., Thorner, J. and Alessi, D.R. (1999) Functional counterparts of mammalian protein kinases PDK1 and SGK in budding yeast. Curr. Biol., 9, 186-197.
7. Chen, P., Lee, K.S. and Levin, D.E. (1993) A pair of putative protein kinase genes (YPK1 and YPK2) is required for cell growth in Saccharomyces cerevisiae. Mol. Gen. Genet., 236, 443-447.
8. Chung, J., Kuo, C.J., Crabtree, G.R. and Blenis, J. (1992) Rapamycin-FKBP specifically blocks growth-dependent activation of and signaling by the 70 kd S6 protein kinases. Cell, 69, 1227-1236.
9. Cross, D.A., Alessi, D.R., Cohen, P., Andjelkovich, M. and Hemmings, B.A. (1995) Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature, 378, 785-789.
10. deHart, A.K., Schnell, J.D., Allen, D.A. and Hicke, L. (2002) The conserved Pkh-Ypk kinase cascade is required for endocytosis in yeast. J. Cell Biol., 156, 241-248.
11. Friant, S., Lombardi, R., Schmelzle, T., Hall, M.N. and Riezman, H. (2001) Sphingoid base signaling via Pkh kinases is required for endocytosis in yeast. EMBO J., 20, 6783-6792.
12. Frodin, M., Jensen, C.J., Merienne, K. and Gammeltoft, S. (2000) A phosphoserine-regulated docking site in the protein kinase RSK2 that recruits and activates PDK1. EMBO J., 19, 2924-2934.
13. Frodin, M., Antal, T.L., Dummler, B.A., Jensen, C.J., Deak, M., Gammeltoft, S. and Biondi, R.M. (2002) A phosphoserine/threonine-binding pocket in AGC kinases and PDK1 mediates activation by hydrophobic motif phosphorylation. EMBO J., 21, 5396-5407.
14. Gelperin, D., Horton, L., DeChant, A., Hensold, J. and Lemmon, S.K. (2002) Loss of ypkl function causes rapamycin sensitivity, inhibition of translation initiation and synthetic lethality in 14-3-3-deficient yeast. Genetics, 161, 1453-1464.
15. Gingras, A.-C., Raught, B. and Sonenberg, N. (2001) Regulation of translation initiation by FRAP/mTOR. Genes Dev., 15, 807-826.
16. Guan, K.L. and Dixon, J.E. (1991) Eukaryotic proteins expressed in Escherichia coli: an improved thrombin cleavage and purification procedure of fusion proteins with glutathione S-transferase. Anal. Biochem., 192, 262-267.
17. Gutz, H., Heslot, H., Leupold, U. and Loprieno, N. (1974) Schizosaccharomyces pombe. In Handbook of Genetics, Vol. 1. Plenum Publishing Corporation, New York, NY, pp. 395-446.
18. Heitman, J., Movva, N.R. and Hall, M.N. (1991) Targets for cell cycle arrest by the immunosuppressant rapamycin in yeast. Science, 253, 905-909.
19. Higuchi, T., Watanabe, Y. and Yamamoto, M. (2002) Protein kinase A regulates sexual development and gluconeogenesis through phosphorylation of the Zn finger transcriptional activator Rst2p in fission yeast. Mol. Cell. Biol., 22, 1-11.
20. Hirota, K., Tanaka, K., Watanabe, Y. and Yamamoto, M. (2001) Functional analysis of the C-terminal cytoplasmic region of the M-factor receptor in fission yeast. Genes Cells, 6, 201-214.
21. Inagaki, M., Schmelzle, T., Yamaguchi, K., Irie, K., Hall, M.N. and Matsumoto, K. (1999) PDK1 homologs activate the Pkc1-mitogen-activated protein kinase pathway in yeast. Mol. Cell. Biol., 19, 8344-8352.
22. Isotani, S., Hara, K., Tokunaga, C., Inoue, H., Avruch, J. and Yonezawa, K. (1999) Immunopurified mammalian target of rapamycin phosphorylates and activates p70 S6 kinase alpha in vitro. J. Biol. Chem., 274, 34493-34498.
23. Kanoh, J., Watanabe, Y., Ohsugi, M., Iino, Y. and Yamamoto, M. (1996) Schizosaccharomyces pombe gad7+ encodes a phosphoprotein with a bZIP domain, which is required for proper G1 arrest and gene expression under nitrogen starvation. Genes Cells, 1, 391-408.
24. Kawai, M., Nakashima, A., Ueno, M., Ushimaru, T., Aiba, K., Doi, H. and Uritani, M. (2001) Fission yeast torl functions in response to various stresses including nitrogen starvation, high osmolarity and high temperature. Curr. Genet., 39, 166-174.
25. Kunitomo, H., Higuchi, T., Iino, Y. and Yamamoto, M. (2000) A zinc-finger protein, Rst2p, regulates transcription of the fission yeast stel1(+) gene, which encodes a pivotal transcription factor for sexual development. Mol. Biol. Cell, 11, 3205-3217.
26. Kunkel, T.A. (1985) Rapid and efficient site-specific mutagenesis without phenotypic selection. Proc. Natl Acad. Sci. USA, 82, 488-492.
27. Kunz, J., Henriquez, R., Schneider, U., Deuter-Reinhard, M., Movva, N.R. and Hall, M.N. (1993) Target of rapamycin in yeast, TOR2, is an essential phosphatidylinositol kinase homolog required for G1 progression. Cell, 73, 585-596.
28. Matsuyama, A., Yabana, N., Watanabe, Y. and Yamamoto, M. (2000) Schizosaccharomyces pombe Ste7p is required for both promotion and withholding of the entry to meiosis. Genetics, 155, 539-549.
29. Maurer, R.A. (1988) Isolation of a yeast protein kinase gene by screening with a mammalian protein kinase cDNA. DNA, 7, 469-474.
30. Moreno, S., Klar, A. and Nurse, P. (1990) Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol., 194, 795-826.
31. Moser, B.A., Dennis, P.B., Pullen, N., Pearson, R.B., Williamson, N.A., Wettenhall, R.E., Kozma, S.C. and Thomas, G. (1997) Dual requirement for a newly identified phosphorylation site in p70s6k. Mol. Cell. Biol., 17, 5648-5655.
32. Newton, A.C. (2001) Protein kinase C: structural and spatial regulation by phosphorylation, cofactors and macromolecular interactions. Chem. Rev., 101, 2353-2364.
33. Niederberger, C. and Schweingruber, M.E. (1999) A Schizosaccharomyces pombe gene, ksg1, that shows structural homology to the human phosphoinositide-dependent protein kinase PDK1, is essential for growth, mating and sporulation. Mol. Gen. Genet., 261, 177-183.
34. Oldham, S., Montagne, J., Radimerski, T., Thomas, G. and Hafen, E. (2000) Genetic and biochemical characterization of DTOR, the Drosophila homolog of the target of rapamycin. Genes Dev., 14, 2689-2694.
35. Pearson, R.B., Dennis, P.B., Han, J.W., Williamson, N.A., Kozma, S.C., Wettenhall, R.E. and Thomas, G. (1995) The principal target of rapamycin-induced p70s6k inactivation is a novel phosphorylation site within a conserved hydrophobic domain. EMBO J., 14, 5279-5287.
36. Price, D.J., Grove, J.R., Calvo, V., Avruch, J. and Bierer, B.E. (1992) Rapamycin-induced inhibition of the 70-kilodalton S6 protein kinase. Science, 257, 973-977.
37. Pullen, N., Dennis, P.B., Andjelkovic, M., Dufner, A., Kozma, S.C., Hemmings, B.A. and Thomas, G. (1998) Phosphorylation and activation of p70s6k by PDK1. Science, 279, 707-710.
38. Radimerski, T., Montagne, J., Rintelen, F., Stocker, H., van der Kaay, J., Downes, C.P., Hafen, E. and Thomas, G. (2002) dS6K-regulated cell growth is dPKB/dPI(3)K-independent, but requires dPDK1. Nat. Cell. Biol., 4, 251-255.
39. Rintelen, F., Stocker, H., Thomas, G. and Hafen, E. (2001) PDK1 regulates growth through Akt and S6K in Drosophila. Proc. Natl Acad. Sci. USA, 98, 15020-15025.
40. Roelants, F.M., Torrance, P.D., Bezman, N. and Thorner, J. (2002) Pkh1 and pkh2 differentially phosphorylate and activate ypk1 and ykr2 and define protein kinase modules required for maintenance of cell wall integrity. Mol. Biol. Cell, 13, 3005-3028.
41. Saitoh, M., Pullen, N., Brennan, P., Cantrell, D., Dennis, P.B. and Thomas, G. (2002) Regulation of an activated S6 kinase 1 variant reveals a novel mammalian target of rapamycin phosphorylation site. J. Biol. Chem., 277, 20104-20112.
42. Schmelzle, T. and Hall, M.N. (2000) TOR, a central controller of cell growth. Cell, 103, 253-262.
43. Schmelzle, T., Helliwell, S.B. and Hall, M.N. (2002) Yeast protein kinases and the RHO1 exchange factor TUS1 are novel components of the cell integrity pathway in yeast. Mol. Cell. Biol., 22, 1329-1339.
44. Sherman, F., Fink, G. and Hicks, J. (1986) Methods in Yeast Genetics: Laboratory Course Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, NY.
45. Sun, Y., Taniguchi, R., Tanoue, D., Yamaji, T., Takematsu, H., Mori, K., Fujita, T., Kawasaki, T. and Kozutsumi, Y. (2000) Sli2 (Ypk1), a homologue of mammalian protein kinase SGK, is a downstream kinase in the sphingolipid-mediated signaling pathway of yeast. Mol. Cell. Biol., 20, 4411-4419.
46. Toker, A. and Newton, A.C. (2000) Cellular signaling: pivoting around PDK-1. Cell, 103, 185-188.
47. Wang, Y., Xu, H.P., Riggs, M., Rodgers, L. and Wigler, M. (1991) byr2, a Schizosaccharomyces pombe gene encoding a protein kinase capable of partial suppression of the ras1 mutant phenotype. Mol. Cell. Biol., 11, 3554-3563.
48. Weisman, R. and Choder, M. (2001) The fission yeast TOR homolog, tor1+, is required for the response to starvation and other stresses via a conserved serine. J. Biol. Chem., 276, 7027-7032.
49. Wood, V. et al. (2002) The genome sequence of Schizosaccharomyces pombe. Nature, 415, 871-880.
50. Yamamoto, M. (1996) The molecular control mechanisms of meiosis in fission yeast. Trends Biochem. Sci., 21, 18-22.
51. Zhang, H., Stallock, J.P., Ng, J.C., Reinhard, C. and Neufeld, T.P. (2000) Regulation of cellular growth by the Drosophila target of rapamycin dTOR. Genes Dev., 14, 2712-2724.