TOR controls transcriptional and translational programs via Sap-Sit4 protein phosphatase signaling effectors

Molecular and Cellular Biology

Volumn 24, Issue 19, 2004, Pages 8332-8341

  Rohde, John R ^a,c   Campbell, Susan ^b   Zurita Martinez, Sara A ^a   Cutler, N Shane ^a,d   Ashe, Mark ^b   Cardenas, Maria E ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

^c INSERM   (France)

^d UNIVERSITY OF UTAH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; INITIATION FACTOR 2; PHOSPHOPROTEIN PHOSPHATASE; POSTSYNAPTIC DENSITY PROTEIN 95; PROTEIN SAP155; PROTEIN SAP185; PROTEIN SIT4; PROTEIN SUBUNIT; PROTEIN TAP42; RAPAMYCIN; REGULATOR PROTEIN; SIGNALING LYMPHOCYTE ACTIVATION MOLECULE ASSOCIATED PROTEIN; TARGET OF RAPAMYCIN KINASE; UNCLASSIFIED DRUG;

ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; DRUG SENSITIVITY; DRUG TARGETING; ENZYME ACTIVITY; ENZYME MECHANISM; ENZYME SUBUNIT; GENE DELETION; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; TRANSLATION INITIATION; TRANSLATION REGULATION; YEAST;

1-PHOSPHATIDYLINOSITOL 3-KINASE; GENE EXPRESSION REGULATION; GENES, REPORTER; PHOSPHOPROTEIN PHOSPHATASE; PHOSPHOPROTEINS; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); PROTEIN BIOSYNTHESIS; PROTEIN KINASES; PROTEIN-SERINE-THREONINE KINASES; RIBONUCLEOPROTEIN, U2 SMALL NUCLEAR; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC;

EUKARYOTA; SACCHAROMYCES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCETALES; TOR;

EID: 4544333055     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.24.19.8332-8341.2004     Document Type: Article

References (54)

1. Ai, W., P. G. Bertram, C. K. Tsang, T. F. Chan, and X. F. Zheng. 2002. Regulation of subtelomeric silencing during stress response. Mol. Cell 10:1295-1305.
2. Ashe, M. P., S. K. De Long, and A. B. Sachs. 2000. Glucose depletion rapidly inhibits translation initiation in yeast. Mol. Biol. Cell 11:833-848.
3. Backman, S., V. Stambolic, and T. Mak. 2002. PTEN function in mammalian cell size regulation. Curr. Opin. Neurobiol. 12:516-522.
4. 1 progression in yeast. Mol. Biol. Cell 7:25-42.
5. Beck, T., and M. N. Hall. 1999. The TOR signalling pathway controls nuclear localization of nutrient-regulated transcription factors. Nature 402:689-692.
6. Bertram, P. G., J. H. Choi, J. Carvalho, W. Ai, C. Zeng, T. F. Chan, and X. F. Zheng. 2000. Tripartite regulation of Gln3p by TOR, Ure2p, and phosphatases. J. Biol. Chem. 275:35727-35733.
7. Cardenas, M. E., N. S. Cutler, M. C. Lorenz, C. J. Di Como, and J. Heitman. 1999. The TOR signaling cascade regulates gene expression in response to nutrients. Genes Dev. 13:3271-3279.
8. Chen, E. J., and C. A. Kaiser. 2003. LST8 negatively regulates amino acid biosynthesis as a component of the TOR pathway. J. Cell Biol. 161:333-347.
9. Cherkasova, V. A., and A. G. Hinnebusch. 2003. Translational control by TOR and TAP42 through dephosphorylation of eIF2α kinase GCN2. Genes Dev. 17:859-872.
10. Cutler, N. S., X. Pan, J. Heitman, and M. E. Cardenas. 2001. The TOR signal transduction cascade controls cellular differentiation in response to nutrients. Mol. Biol. Cell 12:4103-4113.
11. Di Como, C. J., and K. T. Arndt. 1996. Nutrients, via the Tor proteins, stimulate the association of Tap42 with type 2A phosphatases. Genes Dev. 10:1904-1916.
12. Duvel, K., A. Santhanam, S. Garrett, L. Schneper, and J. R. Broach. 2003. Multiple roles of Tap42 in mediating rapamycin-induced transcriptional changes in yeast. Mol. Cell 11:1467-1478.
13. Garber, K. 2001. Rapamycin's resurrection: a new way to target the cancer cell cycle. J. Natl. Cancer Inst. 93:1517-1519.
14. Garber, K. 2002. Synthetic lethality: killing cancer with cancer. J. Natl. Cancer Inst. 94:1666-1668.
15. Garcia-Barrio, M., J. Dong, V. A. Cherkasova, X. Zhang, F. Zhang, S. Ufano, R. Lai, J. Qin, and A. G. Hinnebusch. 2002. Serine 577 is phosphorylated and negatively affects the tRNA binding and eIF2α kinase activities of GCN2. J. Biol. Chem. 277:30675-30683.
16. Goldstein, A. L., and J. H. McCusker. 1999. Three new dominant drug resistance cassettes for gene disruption in Saccharomyces cerevisiae. Yeast 15:1541-1553.
17. Hardwick, J. S., F. G. Kuruvilla, J. K. Tong, A. F. Shamji, and S. L. Schreiber. 1999. Rapamycin-modulated transcription defines the subset of nutrient-sensitive signaling pathways directly controlled by the Tor proteins. Proc. Natl. Acad. Sci. USA 96:14866-14870.
18. Hinnebusch, A. 2000. Mechanism and regulation of initiator methionyl-tRNA binding to ribosomes, p. 185-243. In N. Sonenberg, J. W. B. Hershey, and M. B. Mathews (ed.), Translational control of gene expression. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
19. Hinnebusch, A. G. 1985. A hierarchy of trans-acting factors modulates translation of an activator of amino acid biosynthetic genes in Saccharomyces cerevisiae. Mol. Cell. Biol. 5:2349-2360.
20. Hinnebusch, A. G. 1990. Involvement of an initiation factor and protein phosphorylation in translational control of GCN4 mRNA. Trends Biochem. Sci. 15:148-152.
21. Hinnebusch, A. G., and K. Natarajan. 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.
22. Ho, Y., A. Gruhler, A. Heilbut, G. D. Bader, L. Moore, S. L. Adams, A. Millar, P. Taylor, K. Bennett, K. Boutilier, L. Yang, C. Wolting, I. Donaldson, S. Schandorff, J. Shewnarane, M. Vo, J. Taggart, M. Goudreault, B. Muskat, C. Alfarano, D. Dewar, Z. Lin, K. Michalickova, A. R. Willems, H. Sassi, P. A. Nielsen, K. J. Rasmussen, J. R. Andersen, L. E. Johansen, L. H. Hansen, H. Jespersen, A. Podtelejnikov, E. Nielsen, J. Crawford, V. Poulsen, B. D. Sorensen, J. Matthiesen, R. C. Hendrickson, F. Gleeson, T. Pawson, M. F. Moran, D. Durocher, M. Mann, C. W. Hogue, D. Figeys, and M. Tyers. 2002. Systematic identification of protein complexes in Saccharomyces cerevisiae by mass spectrometry. Nature 415:180-183.
23. Jablonowski, D., A. R. Butler, L. Fichtner, D. Gardiner, R. Schaffrath, and M. J. Stark. 2001. Sit4p protein phosphatase is required for sensitivity of Saccharomyces cerevisiae to Kluyveromyces lactis zymocin. Genetics 159:1479-1489.
24. Jacinto, E., B. Guo, K. T. Arndt, T. Schmelzle, and M. N. Hall. 2001. TIP41 interacts with TAP42 and negatively regulates the TOR signaling pathway. Mol. Cell 8:1017-1026.
25. Jiang, Y., and J. R. Broach. 1999. Tor proteins and protein phosphatase 2A reciprocally regulate Tap42 in controlling cell growth in yeast. EMBO J. 18:2782-2792.
26. Kim, D. H., D. Sarbassov dos, S. M. Ali, R. R. Latek, K. V. Guntur, H. Erdjument-Bromage, P. Tempst, and D. M. Sabatini. 2003. GβL, a positive regulator of the rapamycin-sensitive pathway required for the nutrient-sensitive interaction between raptor and mTOR. Mol. Cell 11:895-904.
27. Komeili, A., K. P. Wedaman, E. K. O'Shea, and T. Powers. 2000. Mechanism of metabolic control. Target of rapamycin signaling links nitrogen quality to the activity of the Rtg1 and Rtg3 transcription factors. J. Cell Biol. 151:863-878.
28. Kubota, H., T. Obata, K. Ota, T. Sasaki, and T. Ito. 2003. Rapamycin-induced translational derepression of GCN4 mRNA involves a novel mechanism for activation of the eIF2α kinase GCN2. J. Biol. Chem. 278:20457-20460.
29. Li, Y., M. N. Corradetti, K. Inoki, and K. L. Guan. 2004. TSC2: filling the GAP in the mTOR signaling pathway. Trends Biochem. Sci. 29:32-38.
30. Loewith, R., E. Jacinto, S. Wullschleger, A. Lorberg, J. L. Crespo, D. Bonenfant, W. Oppliger, P. Jenoe, and M. N. Hall. 2002. Two TOR complexes, only one of which is rapamycin sensitive, have distinct roles in cell growth control. Mol. Cell 10:457-468.
31. Longtine, M. S., A. McKenzie III, D. J. Demarini, N. G. Shah, A. Wach, A. Brachat, P. Philippsen, and J. R. Pringle. 1998. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14:953-961.
32. Lorenz, M. C., and J. Heitman. 1997. Yeast pseudohyphal growth is regulated by GPA2, a G protein alpha homolog. EMBO J. 16:7008-7018.
33. Luke, M. M., F. Della Seta, C. J. Di Como, H. Sugimoto, R. Kobayashi, and K. T. Arndt. 1996. The SAP, a new family of proteins, associate and function positively with the SIT4 phosphatase. Mol. Cell. Biol. 16:2744-2755.
34. Natarajan, K., M. R. Meyer, B. M. Jackson, D. Slade, C. Roberts, A. G. Hinnebusch, and M. J. Marton. 2001. Transcriptional profiling shows that Gcn4p is a master regulator of gene expression during amino acid starvation in yeast. Mol. Cell. Biol. 21:4347-4368.
35. Neshat, M. S., I. K. Mellinghoff, C. Tran, B. Stiles, G. Thomas, R. Petersen, P. Frost, J. J. Gibbons, H. Wu, and C. L. Sawyers. 2001. Enhanced sensitivity of PTEN-deficient tumors to inhibition of FRAP/mTOR. Proc. Natl. Acad. Sci. USA 98:10314-10319.
36. +/- mice. Proc. Natl. Acad. Sci. USA 98:10320-10325.
37. Powers, T., and P. Walter. 1999. Regulation of ribosome biogenesis by the rapamycin-sensitive TOR-signaling pathway in Saccharomyces cerevisiae. Mol. Biol. Cell 10:987-1000.
38. Rohde, J., J. Heitman, and M. E. Cardenas. 2001. The TOR kinases link nutrient sensing to cell growth. J. Biol. Chem. 276:9583-9586.
39. Rohde, J. R., and M. E. Cardenas. 2003. The Tor pathway regulates gene expression by linking nutrient sensing to histone acetylation. Mol. Cell. Biol. 23:629-635.
40. Schiestl, R. H., and R. D. Gietz. 1989. High efficiency transformation of intact yeast cells using single stranded nucleic acids as a carrier. Curr. Genet. 16:339-346.
41. Shamji, A. F., F. G. Kuruvilla, and S. L. Schreiber. 2000. Partitioning the transcriptional program induced by rapamycin among the effectors of the Tor proteins. Curr. Biol. 10:1574-1581.
42. Sherman, F. 1991. Getting started with yeast. Methods Enzymol. 194:3-21.
43. Snyder, G. L., S. Galdi, A. A. Fienberg, P. Allen, A. C. Nairn, and P. Greengard. 2003. Regulation of AMPA receptor dephosphorylation by glutamate receptor agonists. Neuropharmacology 45:703-713.
44. Stark, M. J. 1996. Yeast protein serine/threonine phosphatases: multiple roles and diverse regulation. Yeast 12:1647-1675.
45. 1 for progression into S phase. Cold Spring Harbor Symp. Quant. Biol. 56:75-81.
46. Tavalin, S. J., M. Colledge, J. W. Hell, L. K. Langeberg, R. L. Huganir, and J. D. Scott. 2002. Regulation of GluR1 by the A-kinase anchoring protein 79 (AKAP79) signaling complex shares properties with long-term depression. J. Neurosci. 22:3044-3051.
47. Tee, A. R., B. D. Manning, P. P. Roux, L. C. Cantley, and J. Blenis. 2003. Tuberous sclerosis complex gene products, tuberin and hamartin, control mTOR signaling by acting as a GTPase-activating protein complex toward Rheb. Curr. Biol. 13:1259-1268.
48. Valenzuela, L., C. Aranda, and A. Gonzalez. 2001. TOR modulates GCN4-dependent expression of genes turned on by nitrogen limitation. J. Bacteriol. 183:2331-2334.
49. + regulate arginine uptake and metabolism in Schizosaccharomyces pombe. J. Biol. Chem. 279:12706-12713.
50. Wang, H., and Y. Jiang. 2003. The Tap42-protein phosphatase type 2A catalytic subunit complex is required for cell cycle-dependent distribution of actin in yeast. Mol. Cell. Biol. 23:3116-3125.
51. Wedaman, K. P., A. Reinke, S. Anderson, J. Yates III, J. M. McCaffery, and T. Powers. 2003. Tor kinases are in distinct membrane-associated protein complexes in Saccharomyces cerevisiae. Mol. Biol. Cell 14:1204-1220.
52. Wek, R. C., J. F. Cannon, T. E. Dever, and A. G. Hinnebusch. 1992. Truncated protein phosphatase GLC7 restores translational activation of GCN4 expression in yeast mutants defective for the eIF-2 alpha kinase GCN2. Mol. Cell. Biol. 12:5700-5710.
53. Wolfe, K. H., and D. C. Shields. 1997. Molecular evidence for an ancient duplication of the entire yeast genome. Nature 387:708-713.
54. Yocum, R. R., S. Hanley, R. West, Jr., and M. Ptashne. 1984. Use of lacZ fusions to delimit regulatory elements of the inducible divergent GAL1-GAL10 promoter in Saccharomyces cerevisiae. Mol. Cell. Biol. 4:1985-1998.