The TOR nutrient signalling pathway phosphorylates NPR1 and inhibits turnover of the tryptophan permease

EMBO Journal

Volumn 17, Issue 23, 1998, Pages 6924-6931

  Schmidt, Anja ^a   Beck, Thomas ^a   Koller, Antonius ^a,b   Kunz, Jeannette ^a,c   Hall, Michael N ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

p70(s6k); Rapamycin; Signal transduction; Starvation; TAP42

Indexed keywords

PERMEASE; RAPAMYCIN; TRYPTOPHAN;

ARTICLE; CELL CYCLE G0 PHASE; CELL CYCLE G1 PHASE; CELL GROWTH; CELL VACUOLE; CONTROLLED STUDY; DEPHOSPHORYLATION; ENZYME METABOLISM; NONHUMAN; NUTRIENT; PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN TARGETING; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; STARVATION;

FUNGI; MAMMALIA; SACCHAROMYCES CEREVISIAE;

EID: 0032403058     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/17.23.6924     Document Type: Article

References (45)

1. 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.
2. Begum, N. and Ragolia, L. (1996) cAMP counter-regulates insulin-mediated protein phosphatase-2A inactivation in rat skeletal muscle cells. J. Biol. Chem., 271, 31166-31171.
3. Beretta, L., Gingras, A.C., Svitkin, Y.V., Hall, M.N. and Sonenberg, N. (1996) Rapamycin blocks the phosphorylation of 4E-BP1 and inhibits cap-dependent initiation of translation. EMBO J., 15, 658-664.
4. Bickle, M., Delley, P.-A., Schmidt, A. and Hall, M.N. (1998) Cell wall integrity modulates RHO1 activity via the exchange factor ROM2. EMBO J., 17, 2235-2245.
5. Brunn, G.J., Hudson, C.C., Sekulic, A., Williams, J.M., Hosoi, H., Houghton, P.J., Lawrence, J.C.,Jr and Abraham, R.T. (1997) Phosphorylation of the translational repressor PHAS-I by the mammalian target of rapamycin. Science, 211, 99-101.
6. 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.
7. Cafferkey, R., McLaughlin, M.M., Young, P.R., Johnson, R.K. and Livi, G.P. (1994) Yeast TOR (DRR) proteins: amino-acid sequence alignment and identification of structural motifs. Gene, 141, 133-136.
8. Chen, J., Peterson, R.T. and Schreiber, S.L. (1998) α4 associates with protein phosphatases 2A, 4 and 6. Biochem. Biophys. Res. Commun., 247, 827-832.
9. 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.
10. Gietz, R.D. and Sugino, A. (1988) New yeast-Escherichia coli shuttle vectors constructed with in vitro mutagenized yeast genes lacking six-base pair restriction sites. Gene, 74, 527-534.
11. Grenson, M. (1983a) Inactivation-reactivation process and repression of permease formation regulate several ammonia-sensitive permeases in the yeast Saccharomyces cerevisiae. Eur. J. Biochem., 133, 135-139.
12. Grenson, M. (1983b) Study of the positive control of the general amino-acid permease and other ammonia-sensitive uptake systems by the product of the NPR1 gene in the yeast Saccharomyces cerevisiae. Eur. J. Biochem., 133, 141-144.
13. Guthrie, J. and Fink, G.R. (1991) Guide to Yeast Genetics and Molecular Biology. Academic Press, San Diego, CA.
14. Hara, K., Yonezawa, K., Weng, Q.P., Kozlowski, M.T., Belham, C. and Avruch, J. (1998) Amino acid sufficiency and mTOR regulate p70 S6 kinase and eIF-4E BP1 through a common effector mechanism. J. Biol. Chem., 273, 14484-14494.
15. Hein, C., Springael, J.Y., Volland, C., Haguenauer-Tsapis, R. and Andre, B. (1995) NP11, an essential yeast gene involved in induced degradation of Gap1 and Fur4 permeases, encodes the Rsp5 ubiquitin-protein ligase. Mol. Microbiol., 18, 77-87.
16. Heitman, J., Movva, N.R. and Hall, M.N. (1991a) Targets for cell cycle arrest by the immunosuppressant rapamycin in yeast. Science, 253, 905-909.
17. Heitman, J., Movva, N.R., Hiestand, P.C. and Hall, M.N. (1991b) FK 506-binding protein proline rotamase is a target for the immunosuppressive agent FK 506 in Saccharomyces cerevisiae. Proc. Natl Acad. Sci. USA, 88, 1948-1952.
18. Heitman, J., Koller, A., Kunz, J., Henriquez, R., Schmidt, A., Movva, N.R. and Hall, M.N. (1993) The immunosuppressant FK506 inhibits amino acid import in Saccharomyces cerevisiae. Mol. Cell. Biol., 13, 5010-5019.
19. 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.
20. Helliwell, S.B., Howald, I., Barbet, N. and Hall, M.N. (1998) Evidence for two related TOR2 signaling pathways coordinating cell growth in Saccharomyces cerevisiae. Genetics, 148, 99-112.
21. Hicke, L. (1997) Ubiquitin-dependent internalization and down-regulation of plasma membrane proteins. FASEB J., 11, 1215-1226.
22. Hicke, L. and Riezman, H. (1996) Ubiquitination of a yeast plasma membrane receptor signals its ligand-stimulated endocytosis. Cell, 84, 277-287.
23. 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.
24. Ito, H., Fukuda, Y., Murata, K. and Kimura, A. (1983) Transformation of intact yeast cells treated with alkali cations. J. Bacteriol., 153, 163-168.
25. Keith, C.T. and Schreiber, S.L. (1995) PIK-related kinases: DNA repair, recombination and cell cycle check points. Science, 270, 50-51.
26. Koller, A., Heitman, J. and Hall, M.N. (1996) Regional bivalent-univalent pairing versus trivalent pairing of a trisomic chromosome in Saccharomyces cerevisiae. Genetics, 144, 957-966.
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. Lane, D. (1998) Awakening angels. Nature, 394, 616-617.
29. Marchal, C., Haguenauer-Tsapis, R. and Urban-Grimal, D. (1998) A PEST-like sequence mediates phosphorylation and efficient ubiquitination of yeast uracil permease. Mol. Cell. Biol., 18, 314-321.
30. Murata, K., Wu, J. and Brautigan, D.L. (1997) B cell receptor-associated protein alpha4 displays rapamycin-sensitive binding directly to the catalytic subunit of protein phosphatase 2A. Proc. Natl Acad. Sci. USA, 94, 10624-10629.
31. Noda, T. and Ohsumi, Y. (1998) Tor, a phosphatidylinositol kinase homologue, controls autophagy in yeast. J. Biol. Chem., 273, 3963-3966.
32. Pullen, N. and Thomas, G. (1997) The modular phosphorylation and activation of p70s6k. FEBS Lett., 410, 78-82.
33. Sambrook, J., Fritsch, E.F. and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
34. Schmidt, A., Hall, M.N. and Koller, A. (1994) Two FK506 resistance-conferring genes in Saccharomyces cerevisiae, TAT1 and TAT2, encode amino acid permeases mediating tyrosine and tryptophan uptake. Mol. Cell. Biol., 14, 6597-6606.
35. 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.
36. Schmidt, A., Bickle, M., Beck, T. and Hall, M.N. (1997) The yeast phosphatidylinositol kinase homologTOR2 activates RHO1 and RHO2 via the exchange factor ROM2. Cell, 88, 531-542.
37. Sophianopoulou, V. and Diallinas, G. (1995) Amino acid transporters of lower eukaryotes: regulation, structure and topogenesis. FEMS Microbiol. Rev., 16, 53-75.
38. Springael, J.Y. and Andre, B. (1998) Nitrogen-regulated ubiquitination of the Gap1 permease of Saccharomyces cerevisiae. Mol. Biol. Cell, 9, 1253-1263.
39. Stan, R., McLaughlin, M.M., Cafferkey, R., 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.
40. Stanbrough, M. and Magasanik, B. (1995) Transcriptional and posttranslational regulation of the general amino acid permease of Saccharomyces cerevisiae. J. Bacteriol., 177, 94-102.
41. Thomas, G. and Hall, M.N. (1997) TOR signalling and control of cell growth. Curr. Opin. Cell Biol., 9, 782-787.
42. Vandenbol, M., Jauniaux, J.-C., Vissers, S. and Grenson, M. (1987) Isolation of the NPR1 gene responsible for the reactivation of ammonia-sensitive amino-acid permeases in Saccharomyces cerevisiae. Eur. J. Biochem., 164, 607-612.
43. Vandenbol, M., Jauniaux, J.C. and Grenson, M. (1990) The Saccharomyces cerevisiae NPR1 gene required for the activity of ammonia-sensitive amino acid permeases encodes a protein kinase homologue. Mol. Gen. Genet., 222, 393-399.
44. von Manteuffel, S.R., Gingras, A.C., Ming, X.F., Sonenberg, N. and Thomas, G. (1996) 4E-BP1 phosphorylation is mediated by the FRAP-p70s6k pathway and is independent of mitogen-activated protein kinase. Proc. Natl Acad. Sci. USA, 93, 4076-4080.
45. Zheng, X.F., Florentino, 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.