Protein kinase activity and identification of a toxic effector domain of the target of rapamycin TOR proteins in yeast

Molecular Biology of the Cell

Volumn 10, Issue 8, 1999, Pages 2531-2546

  Alarcon, Clara M ^a   Heitman, Joseph ^a   Cardenas, Maria E ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHOLIPASE C; PROTEIN DERIVATIVE; PROTEIN KINASE; RAPAMYCIN; WORTMANNIN;

AMINO ACID SEQUENCE; ARTICLE; CELL CYCLE G1 PHASE; CELL GROWTH; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME SUBSTRATE; GENE DELETION; GENE OVEREXPRESSION; GROWTH INHIBITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN INTERACTION; YEAST;

FUNGI; MAMMALIA;

EID: 0032802378     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.10.8.2531     Document Type: Article

References (60)

1. Alani, E., Cao, L., and Kleckner, N. (1987). A method for gene disruption that allows repeated use of URA3 selection in the construction of multiply disruption yeast strains. Genetics 116, 541-545.
2. Alarcon, C.M., Cardenas, M.E., and Heitman, J. (1996). Mammalian RAFT1 kinase domain provides rapamycin-sensitive TOR function in yeast. Genes Dev. 10, 279-288.
3. Barbet, N.C., Schneider, U., Helliwell, S.B., Stansfield, I., Tuite, M.F., and Hall, M.N. (1996). TOR controls translation initiation and early G1 progression in yeast. Mol. Biol. Cell 7, 25-42.
4. Barlow, C., et al. (1996). Atm-deficient mice: a paradigm of ataxia telangiectasia. Cell 86, 159-171.
5. Brown, E.J., Albers, M.W., Shin, T.B., Ichikawa, K., Keith, C.T., Lane, W.S., and Schreiber, S.L. (1994). A mammalian protein targeted by G1-arresting rapamycin-receptor complex. Nature 369, 756-759.
6. Brown, E.J., Beal, P.A., Keith, C.T., Chen, J., Shin, T.B., and Schreiber, S.L. (1995). Control of p70 S6 kinase by kinase activity of FRAP in vivo. Nature 377, 441-446.
7. Brown, E.J., and Schreiber, S.L. (1996). A signaling pathway to translational control. Cell 86, 517-520.
8. Brunn, G.J., Hudson, C.C., Sekulic, A., Williams, J.M., Hosoi, J., Houghton, P.J., Lawrence, J.C., and Abraham, R.T. (1997). Phosphorylation of the translational repressor PHAS-I by the mammalian target of rapamycin. Science 277, 99-101.
9. Brunn, G.J., Williams, J., Sabers, C., Wiederrecht, G., Lawrence, J.C., Jr., and Abraham, R.T. (1996). Direct inhibition of the signal functions of the mammalian target of rapamycin by the phosphoinositide 3-kinase inhibitors, wortmannin and LY294002. EMBO J. 15, 5256-5267.
10. 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.
11. Cafferkey, R., Young, P.R., McLaughlin, M.M., Bergsma, D.J., Koltin, Y., Sathe, G.M., Faucette, L., Eng, W.-K., Johnson, R.K., and Livi, G.P. (1993). Dominant missense mutations in a novel yeast protein related to mammalian phosphatidylinositol 3-kinase and VPS34 abrogate rapamycin cytotoxicity. Mol. Cell. Biol. 13, 6012-6023.
12. Cardenas, M.E., Hemenway, C., Muir, R.S., Ye, R., Fiorentino, D., and Heitman, J. (1994a). Immunophilins interact with calcineurin in the absence of exogenous immunosuppressive ligands. EMBO J. 13, 5944-5957.
13. Cardenas, M.E., and Heitman, J. (1995). FKBP12-rapamyein target TOR2 is a vacuolar protein with an associated phosphatidylinositol-4 kinase activity. EMBO J. 14, 5892-5907.
14. Cardenas, M.E., Lorenz, M., Hemenway, C., and Heitman, J. (1994b). Yeast as model-T cells. Perspect. Drug Discov. Des. 2, 103-126.
15. Chen, J., Zheng, X.-F., Brown, E.J., and Schreiber, S.L. (1995). Identification of an 11-kDa FKBP12-rapamycin-binding domain within the 289-kDa FKBP12-rapamycin-associated protein and characterization of a critical serine residue. Proc. Natl. Acad. Sci. USA 92, 4947-4951.
16. Chiu, M.I., Katz, H., and Berlin, V. (1994). RAPT1, a mammalian homolog of yeast Tor, interacts with the FKBP12/rapamycin complex. Proc. Natl. Acad. Sci. USA 92, 12574-12578.
17. Choi, J., Chen, J., Schreiber, S.L., and Clardy, J. (1996). Structure of the FKBP12-rapamycin complex interacting with the binding domain of human FRAP. Science 273, 239-242.
18. Cliby, W.A., Roberts, C.J., Cimprich, K.A., Stringer, C.M., Lamb, J.R., Schreiber, S.L., and Friend, S.H. (1998). Overexpression of a kinase-inactive ATR protein causes sensitivity to DNA-damaging agents and defects in cell cycle checkpoints. EMBO J. 17, 159-169.
19. Cutler, N.S., Heitman, J., and Cardenas, M.E. (1997). STT4 is an essential phosphatidylinositol 4-kinase that is a target of wortmannin in Saccharomyces cerevisiae. J. Biol. Chem. 272, 27671-27677.
20. Dhand, R., Hiles, I., Panayotou, G., Roche, S., Fry, M.J., Gout, I., Totty, N.F., Truong, O., Vicendo, P., and Yonezawa, K. (1994). PI 3-kinase is a dual specificity enzyme: autoregulation by an intrinsic protein-serine kinase activity. EMBO J. 13, 522-533.
21. Di Como, C.J., and Arndt, K.T. (1996). Nutrients, via the Tor proteins, stimulate the association of Tap42 with type 2A phosphatases. Genes Dev. 10, 1904-1916.
22. Flick, J.S. (1998). An essential function of a phosphoinositide-specific phospholipase C is relieved by inhibition of a cyclin-dependent protein kinase in the yeast Saccharomyces cerevisiae. Genetics 148, 33-47.
23. Flick, J.S., and Thorner, J. (1993). Genetic and biochemical characterization of a phosphatidylinositol-specific phospholipase C in Saccharomyces cerevisiae. Mol. Cell. Biol. 23, 5861-5876.
24. Gingras, A.-C., Kennedy, S.G., O'Leary, M.A., Sonenberg, N., and Hay, N. (1998). 4E-BP1, a repressor of mRNA translation, is phosphorylated and inactivated by the Akt(PKB) signaling pathway. Genes Dev. 12, 502-513.
25. Graves, L.M., Bornfeldt, K.E., Argast, G.M., Krebs, E.G., Kong, X., Lin, T.A., and Lawrence, J.C., Jr. (1995). cAMP- and rapamycin-sensitive regulation of the association of eukaryotic initiation factor 4E and the translational regulator PHAS-I in aortic smooth muscle cells. Proc. Natl. Acad. Sci. USA 92, 7222-7226.
26. Hara, Yonezawa, K., Kozlowski, M.T., Sugimoto, T., Andrabi, K., Weng, Q.-P., Kasuga, M., Nishimoto, I., and Avruch, J. (1997). Regulation of eIF-4E BP1 phosphorylation by mTOR. J. Biol. Chem. 272, 26457-26463.
27. 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.
28. Heitman, J., Movva, N.R., and Hall, M.N. (1992). Proline isomerases at the crossroads of protein folding, signal transduction, and immunosuppression. New Biol. 4, 448-460.
29. Helliwell, S.B., Howald, I., Barbet, N., and Hall, M.N. (1998). TOR2 is part of two related signaling pathways coordinating cell growth in Saccharomyces cerevisiae. Genetics 248, 99-112.
30. Helliwell, S.B., Wagner, P., Kunz, J., Deuter-Reinhard, M., Henriquez, R., and Hall, M.N. (1994). TOR1 and TOR2 are structurally and functionally similar but not identical phosphatidylinositol kinase homologues in yeast. Mol. Biol. Cell 5, 105-118.
31. Ho, S.N., Hunt, H.D., Horton, R.M., Pullen, J.K., and Pease, L.R. (1989). Site-directed mutagenesis by overlap extension using the PCR. Gene 77, 51-59.
32. Koltin, Y., Faucette, L., Bergsma, D.J., Levy, M.A., Cafferkey, R., Koser, P.L., Johnson, R.K., and Livi, G.P. (1991). Rapamycin sensitivity in Saccharomyces cerevisiae is mediated by a peptidyl-prolyl cis-trans isomerase related to human FK506-binding protein. Mol. Cell. Biol. 11, 1718-1723.
33. 1 progression. Cell 73, 585-596.
34. Lawrence, J.C., Jr., and Abraham, R.T. (1997). PHAS/4E-BPs as regulators of mRNA translation and cell proliferation. Trends Biochem. Sci. 22, 345-349.
35. Lin, T.A., Kong, X., Saltiel, A.R., Blackshear, P.J., and Lawrence, J.C. (1995). Control of PHAS-I by insulin in 3T3-L1 adipocytes. Synthesis, degradation, and phosphorylation by a rapamycin-sensitive and mitogen-activated protein kinase-independent pathway. J. Biol. Chem. 270, 18531-18538.
36. Lorenz, M.C., and Heitman, J. (1995). TOR mutations confer rapamycin resistance by preventing interaction with FKBP12-rapamycin. J. Biol. Chem. 270, 27531-27537.
37. Morgan, S.E., Lovly, C., Pandita, T.K., Shiloh, Y., and Kastan, M.B. (1997). Fragments of ATM which have dominant-negative or complementing activity. Mol. Cell. Biol. 17, 2020-2029.
38. Noda, T., and Ohsumi, Y. (1998). Tor, a phosphatidylinositol kinase homologue, controls autophagy in yeast. J. Biol. Chem. 273, 3963-3966.
39. Orr-Weaver, T.L., Szostak, J.W., and Rothstein, R.J. (1981). Yeast transformation: a model system for the study of recombination. Proc. Natl. Acad. Sci. USA 78, 6354-6358.
40. Sabatini, D.M., Erdjument-Bromage, H., Lui, M., Tempst, P., and Snyder, S.H. (1994). RAFT1: a mammalian protein that binds to FKBP12 in a rapamycin-dependent manner and is homologous to yeast TORs. Cell 78, 35-43.
41. Sabatini, D.M., Pierchala, B.A., Barrow, R.K., Schell, M.J., and Snyder, S.H. (1995). The rapamycin and FKBP12 target (RAFT) displays phosphatidylinositol 4-kinase activity. J. Biol. Chem. 270, 20875-20878.
42. Sabers, C.J., Martin, M.M., Brunn, G.J., Williams, J.M., Dumont, F.J., Wiederrecht, G., and Abraham, R.T. (1995). Isolation of a protein target of the FKBP12-rapamycin complex in mammalian cells. J. Biol. Chem. 270, 815-822.
43. Schiestl, R.H., Manivasakam, P., Woods, R.A., and Gietz, R.D. (1993). Introducing DNA into yeast by transformation. Methods 5, 79-85.
44. Schmidt, A., Bickle, M., Beck, T., and Hall, M.N. (1997). The yeast phosphatidylinositol kinase homolog TOR2 activates RHO1 and RHO2 via the exchange factor ROM2. Cell 88, 531-542.
45. Schmidt, A., Kunz, J., and Hall, M.N. (1996). TOR2 is required for organization of the actin cytoskeleton in yeast. Proc. Natl. Acad. Sci. USA 93, 13780-13785.
46. Schreiber, S.L., and Crabtree, G.R. (1992). The mechanism of action of cyclosporin A and FK506. Immunol. Today 13, 136-142.
47. Schu, P.V., Takegawa, K., Fry, M.J., Stack, J.H., Waterfield, M.D., and Emr, S.D. (1993). Phosphatidylinositol 3-kinase encoded by yeast VPS34 gene essential for protein sorting. Science 260, 88-91.
48. Sherman, F. (1991). Getting started with yeast. In: Methods in Enzymology, vol. 194, ed. C. Guthrie and G.R. Fink, San Diego, CA: Academic Press, 3-21.
49. Stan, R., McLaughlin, M.M., Cafferkey, R.T., Johnson, R.K., Rosenberg, M., and Livi, G.P. (1994). Interaction between FKBP12-rapamycin and TOR involves a conserved serine residue. J. Biol. Chem. 269, 32027-32030.
50. Taylor, S.S., Knighton, D.R., Zheng, J., Sowadski, J.M., Gibbs, C.S., and Zoller, M.J. (1993). A template for the protein kinase family. Trends Biochem. Sci. 28, 84-89.
51. s6k pathway and is independent of mitogen-activated protein kinase. Proc. Natl. Acad. Sci. USA 93, 4076-4080.
52. Wach, A., Brachat, A., Pohlmann, R., and Philippsen, P. (1994). New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae. Yeast 10, 1793-1808.
53. Weisman, R., Choder, M., and Koltin, Y. (1997). Rapamycin specifically interferes with the developmental response of fission yeast to starvation. J. Bacteriol. 179, 6325-6334.
54. Withers, D.J., Ouwens, D.M., Nave, B.T., van der Zon, G.C., Alarcon, C.M., Cardenas, M.E., Heitman, J., Maassen, J.A., and Shepherd, P.R. (1997). Expression, enzyme activity, and subcellular localization of mammalian target of rapamycin in insulin-responsive cells. Biochem. Biophys. Res. Commun. 241, 704-709.
55. Xu, Y., Ashley, T., Brainerd, E.E., Bronson, R.T., Meyn, M.S., and Baltimore, D. (1996). Targeted disruption of ATM leads to growth retardation, chromosomal fragmentation during meiosis, immune defects, and thymic lymphoma. Genes Dev. 10, 2411-2422.
56. Xu, Y., and Baltimore, D. (1996). Dual roles of ATM in the cellular response to radiation and in cell growth control. Genes Dev. 10, 2401-2410.
57. Yoshida, S., Ohya, Y., Goebl, M., Nakano, A., and Anraku, Y. (1994a). A novel gene, STT4, encodes a phosphatidylinositol 4-kinase in the PKC1 protein kinase pathway of Saccharomyces cerevisiae. J. Biol. Chem. 269, 1166-1171.
58. Yoshida, S., Ohya, Y., Nakano, A., and Anraku, Y. (1994b). Genetic interactions among genes involved in the STT4-PKC1 pathway of Saccharomyces cerevisiae. Mol. Gen. Genet. 242, 631-640.
59. Zheng, X.-F., Fiorentino, D., Chen, J., Crabtree, G.R., and Schreiber, S.L. (1995). TOR kinase domains are required for two distinct functions, only one of which is inhibited by rapamycin. Cell 82, 121-130.
60. Zheng, X.F., and Schreiber, S.L. (1997). Target of rapamycin proteins and their kinase activities are required for meiosis. Proc. Natl. Acad. Sci. USA 94, 3070-3075.