Translational control by TOR and TAP42 through dephosphorylation of eIF2α kinase GCN2

Genes and Development

Volumn 17, Issue 7, 2003, Pages 859-872

  Cherkasova, Vera A ^a   Hinnebusch, Alan G ^a  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

Author keywords

EIF2 kinase; GCN2; TAP42; TOR; Translational control

Indexed keywords

ALANINE; INITIATION FACTOR 2; PROTEIN; PROTEIN KINASE; PROTEIN KINASE GCN2; PROTEIN TAP42; RAPAMYCIN; SERINE; TARGET OF RAPAMYCIN KINASE; TRANSCRIPTION FACTOR GCN4; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; DEPHOSPHORYLATION; ENZYME ACTIVITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN MALNUTRITION; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; TRANSLATION REGULATION; YEAST CELL;

1-PHOSPHATIDYLINOSITOL 3-KINASE; EIF-2 KINASE; GENE EXPRESSION REGULATION, FUNGAL; PHOSPHORYLATION; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); PROTEIN BIOSYNTHESIS; PROTEIN KINASES; PROTEIN-SERINE-THREONINE KINASES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SIROLIMUS;

EID: 0037382865     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.1069003     Document Type: Article

References (46)

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. Beck, T. and Hall, M.N. 1999. The TOR signalling pathway controls nuclear localization of nutrient-regulated transcription factors. Nature 402: 689-692.
3. Berlanga, J.J., Santoyo, J., and De Haro, C. 1999. Characterization of a mammalian homolog of the GCN2 eukaryotic initiation factor 2alpha kinase. Eur. J. Biochem. 265: 754-762.
4. Berset, C., Trachsel, H., and Altmann, M. 1998. The TOR (target of rapamycin) signal transduction pathway regulates the stability of translation initiation factor eIF4G in the yeast Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. 95: 4264-4269.
5. Cardenas, M.E., Cutler, N.S., Lorenz, M.C., Di Como, C.J., and Heitman, J. 1999. The TOR signaling cascade regulates gene expression in response to nutrients. Genes & Dev. 13: 3271-3279.
6. Cooper, T. 2002. Transmitting the signal of excess nitrogen in Saccharomyces cerevisiae from the Tor proteins to the GATA factors: Connecting the dots. FEMS Microbiol. Rev. 26: 223-238.
7. Cosentino, G.P., Schmelzle, T., Haghighat, A., Helliwell, S.B., Hall, M.N., and Sonenberg, N. 2000. Eaplp, a novel eukaryotic translation initiation factor 4E-associated protein in Saccharomyces cerevisiae. Mol. Cell. Biol. 20: 4604-4613.
8. Crespo, J.L., Powers, T., Fowler, B., and Hall, M.N. 2002. The TOR-controlled transcription activators GLN3, RTG1, and RTG3 are regulated in response to intracellular levels of glutamine. Proc. Natl. Acad. Sci.99: 6784-6789.
9. Dever, T.E., Feng, L., Wek, R.C., Cigan, A.M., Donahue, T.D., and Hinnebusch, A.G. 1992. Phosphorylation of initiation factor 2a by protein kinase GCN2 mediates gene-specific translational control of GCN4 in yeast. Cell 68: 585-596.
10. 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.
11. Dong, J., Qiu, H., Garcia-Barrio, M., Anderson, J., and Hinnebusch, A.G. 2000. Uncharged tRNA activates GCN2 by displacing the protein kinase moiety from a bipartite tRNA-binding domain. Mol. Cell 6: 269-279.
12. Garcia-Barrio, M., Dong, J., Ufano, S., and Hinnebusch, A.G. 2000. Association of GCN1/GCN20 regulatory complex with the conserved N-terminal domain of eIF2a kinase GCN2 is required for GCN2 activation in vivo. EMBO J. 19: 1887-1899.
13. Garcia-Barrio, M., Dong, J., Cherkasova, V.A., Zhang, X., Zhang, F., Ufano, S., Lai, R., Qin, J., and Hinnebusch, A.G. 2002. Serine-577 is phosphorylated and inhibits the tRNA binding and eIF2 alpha kinase activities of GCN2. J. Biol. Chem. 227: 30675-30683.
14. Gingras, A.C., Raught, B., and Sonenberg, N. 2001. Regulation of translation initiation by FRAP/mTOR. Genes & Dev. 15: 807-826.
15. Goossens, A., Dever, T.E., Pascual-Ahuir, A., and Serrano, R. 2001. The protein kinase Gcn2p mediates sodium toxicity in yeast. J. Biol. Chem. 276: 30753-30760.
16. Harding, H., Calfon, M., Urano, F., Novoa, I., and Ron, D. 2002. Transcription and translational control in the mammalian unfolded protein response. Annu. Rev. Cell Dev. Biol. 18: 575-599.
17. Hinnebusch, A.G. 1985. A hierarchy of trans-acting factors modulate translation of an activator of amino acid biosynthetic genes in Saccharomyces cerevisiae. Mol. Cell. Biol. 5: 2349-2360.
18. -. 1996. Translational control of GCN4: Gene-specific regulation by phosphorylation of eIF2. In Translational control (eds. J.W.B. Hershey, M.B. Mathews, and N. Sonenberg), pp. 199-244. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
19. -. 2000. Mechanism and regulation of initiator methionyl0-tRNA binding to ribosomes. In Translational control of gene expression (eds. N. Sonenberg, J.W.B. Hershey, and M.B. Mathews), pp. 185-243. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
20. Hinnebusch, A.G. and Natarajan, K. 2002. Gcn4p, a master regulator of gene expression, is controlled at multiple levels by diverse signals of starvation and stress. Eukaryot. Cell 1: 22-32.
21. Hughes, T.R., Marton, M.J., Jones, A.R., Roberts, C.J., Stoughton, R., Armour, C.D., Bennett, H.A., Coffey, E., Dai, H., He, Y.D., et al. 2000. Functional discovery via a compendium of expression profiles. Cell 102: 109-126.
22. Jacinto, E., Guo, B., Arndt, K.T., Schmelzle, T., and Hall, M.N. 2001. TIP41 interacts with TAP42 and negatively regulates the TOR signaling pathway. Mol. Cell 8: 1017-1026.
23. Jiang, Y. and Broach, J.R. 1999. Tor proteins and protein phosphatase 2A reciprocally regulate Tap42 in controlling cell growth in yeast. EMBO J. 18: 2782-2792.
24. 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.
25. Lorenz, M.C. and Heitman, J. 1997. Yeast pseudohyphal growth is regulated by GPA2, a G protein alpha homolog. EMBO J. 16: 7008-7018.
26. Marton, M.J., Crouch, D., and Hinnebusch, A.G. 1993. GCN1, a translational activator of GCN4 in S. cerevisiae, is required for phosphorylation of eukaryotic translation initiation factor 2 by protein kinase GCN2. Mol. Cell. Biol. 13: 3541-3556.
27. Moehle, C.M. and Hinnebusch, A.G. 1991. Association of RAP1 binding sites with stringent control of ribosomal protein gene transcription in Saccharomyces cerevisiae. Mol. Cell. Biol. 11: 2723-2735.
28. Mueller, P.P. and Hinnebusch, A.G. 1986. Multiple upstream AUG codons mediate translational control of GCN4. Cell 45: 201-207.
29. Natarajan, K., Meyer, M.R., Jackson, B.M., Slade, D., Roberts, C., Hinnebusch, A.G., and Marton, M.J. 2001. Transcriptional profiling shows that Gcn4p is a master regulator of gene expression during amino acid starvation in yeast. Mol. Cell. Biol. 21: 4343-4368.
30. Olsen, D.S., Jordan, B., Chen, D., Wek, R.C., and Cavener, D.R. 1998. Isolation of the gene encoding the Drosophila melanogaster homolog of the Saccharomyces cerevisiae GCN2 eIF-2a kinase. Genetics 149: 1495-1509.
31. Patil, C. and Walter, P. 2001. Intracellular signaling from the endoplasmic reticulum to the nucleus: The unfolded protein response in yeast and mammals. Cell Biol. 13: 349-356.
32. Powers, T. and Walter, P. 1999. Regulation of ribosome biogenesis by the rapamycin-sensitive TOR-signaling pathway in Saccharomyces cerevisiae. Mol. Biol. Cell 10: 987-1000.
33. Qiu, H., Hu, C., Dong, J., and Hinnebusch, A.G. 2002. Mutations that bypass tRNA binding activate the intrinsically defective kinase domain in GCN2. Genes & Dev. 16: 1271-1280.
34. Rolfes, R.J. and Hinnebusch, A.G. 1993. Translation of the yeast transcriptional activator GCN4 is stimulated by purine limitation: Implications for activation of the protein kinase GCN2. Mol. Cell. Biol. 13: 5099-5111.
35. Romano, P.R., Garcia-Barrio, M.T., Zhang, X., Wang, Q., Taylor, D.R., Zhang, F., Herring, C., Mathews, M.B., Qin, J., and Hinnebusch, A.G. 1998. Autophosphorylation in the activation loop is required for full kinase activity in vivo of human and yeast eukaryotic initiation factor 2a kinases PKR and GCN2. Mol. Cell. Biol. 18: 2282-2297.
36. Schmelzle, T. and Hall, M.N. 2000. TOR, a central controller of cell growth. Cell 103: 253-262.
37. Schmidt, A., Beck, T., Koller, A., Kunz, J., and Hall, M.N. 1998. The TOR nutrient signalling pathway phosphorylates NPR1 and inhibits turnover of the tryptophan permease. EMBO J. 17: 6924-6931.
38. Sherman, F., Fink, G.R., and Lawrence, C.W. 1974. Methods in yeast genetics, pp. 61-64. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
39. Tzamarias, D., Roussou, I., and Thireos, G. 1989. Coupling of GCN4 mRNA translational activation with decreased rates of polypeptide chain initiation. Cell 57: 947-954.
40. Valášek, L., Phan, L., Schoenfeld, L.W., Valásková, V., and Hinnebusch, A.G. 2001. Related eIF3 subunits TIF32 and HCR1 interact with an RNA recognition motif in PRT1 required for eIF3 integrity and ribosome binding. EMBO J. 20: 891-904.
41. Valenzuela, L., Aranda, C., and Gonzalez, A. 2001. TOR modulates GCN4-dependent expression of genes turned on by nitrogen limitation. J. Bacteriol. 183: 2331-2334.
42. Vazquez de Aldana, C.R., Wek, R.C., San Segundo, P., Truesdell, A.G., and Hinnebusch, A.G. 1994. Multicopy tRNA genes functionally suppress mutations in yeast eIF-2a kinase GCN2: Evidence for separate pathways coupling GCN4 expression to uncharged tRNA. Mol. Cell. Biol. 14: 7920-7932.
43. Wek, R.C., Cannon, J.F., Dever, T.E., and Hinnebusch, A.G. 1992. Truncated protein phosphatase GLC7 restores translational activation of GCN4 expression in yeast mutants defective for the eIF-2a kinase GCN2. Mol. Cell. Biol. 12: 5700-5710.
44. Wek, S.A., Zhu, S., and Wek, R.C. 1995. The histidyl-tRNA synthetase-related sequence in the eIF-2a protein kinase GCN2 interacts with tRNA and is required for activation in response to starvation for different amino acids. Mol. Cell. Biol. 15: 4497-4506.
45. Yang, R., Wek, S.A., and Wek, R.C. 2000. Glucose limitation induces GCN4 translation by activation of Gcn2 protein kinase. Mol. Cell. Biol. 20: 2706-2717.
46. Zhu, S., Sobolev, A.Y., and Wek, R.C. 1996. Histidyl-tRNA synthetase-related sequences in GCN2 protein kinase regulate in vitro phosphorylation of eIF-2. J. Biol. Chem. 271: 24989-24994.