Rapamycin induces the G0 program of transcriptional repression in yeast by interfering with the TOR signaling pathway

Molecular and Cellular Biology

Volumn 18, Issue 8, 1998, Pages 4463-4470

  Zaragoza, Dean ^a   Ghavidel, Ataollah ^a   Heitman, Joseph ^b   Schultz, Michael C ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASEIN KINASE II; PHOSPHOPROTEIN PHOSPHATASE 2A; PROTEIN KINASE; RAPAMYCIN; ANTIFUNGAL AGENT; CELL CYCLE PROTEIN; DNA DIRECTED RNA POLYMERASE III; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOTRANSFERASE; POLYENE; SACCHAROMYCES CEREVISIAE PROTEIN; TOR2 PROTEIN, S CEREVISIAE;

ANIMAL CELL; ARTICLE; CELL CYCLE G0 PHASE; CELL GROWTH; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; DOWN REGULATION; GENE CONTROL; GROWTH INHIBITION; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; STRUCTURAL GENE; TRANSCRIPTION REGULATION; YEAST; CELL CYCLE G1 PHASE; DRUG ANTAGONISM; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; PROTEIN SYNTHESIS; SACCHAROMYCES CEREVISIAE; TEMPERATURE;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANTIBIOTICS, ANTIFUNGAL; CELL CYCLE PROTEINS; G0 PHASE; G1 PHASE; GENE EXPRESSION REGULATION, FUNGAL; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); POLYENES; PROTEIN BIOSYNTHESIS; RNA POLYMERASE III; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SIGNAL TRANSDUCTION; SIROLIMUS; TEMPERATURE; TRANSCRIPTION, GENETIC;

EID: 0031596416     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.18.8.4463     Document Type: Article

References (50)

1. Alarcon, C. M., M. E. Cardenas, and J. Heitman. 1996. Mammalian RAFT1 kinase domain provides rapamycin-sensitive TOR function in yeast. Genes Dev. 10:279-288.
2. Allende, J. E., and C. C. Allende. 1995. Protein kinase CK2: an enzyme with multiple substrates and a puzzling regulation. FASEB J. 9:313-323.
3. Baker, R. E., and B. D. Hall. 1984. Structural features of yeast tRNA genes which affect transcription factor binding. EMBO J. 3:2793-2800.
4. Barbet, N. C., U. Schneider, S. B. Helliwell, I. Stansfield, M. F. Tuite, and M. N. Hall. 1996. TOR controls translation initiation and early G1 progression in yeast. Mol. Biol. Cell 7:25-42.
5. Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle or protein-dye binding. Anal. Biochem. 72:248-254.
6. Burke, D. J., and D. Church. 1991. Protein synthesis requirements for nuclear division, cytokinesis, and cell separation in Saccharomyces cerevisiae. Mol. Cell. Biol. 11:3691-3698.
7. Cardenas, M. E., and J. Heitman. 1995. FKBP12-rapamycin target TOR2 is a vacuolar protein with an associated phosphatidylinositol 4-kinase activity. EMBO J. 14:5892-5907.
8. Choder, M. 1991. A general topoisomerase I-dependent transcriptional repression in the stationary phase in yeast. Genes Dev. 5:2315-2326.
9. Clarke, E. M., C. L. Peterson, A. V. Brainard, and D. L. Riggs. 1996. Regulation of the RNA polymerase I and III transcription systems in response to growth conditions. J. Biol. Chem. 271:22189-22195.
10. 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.
11. Dieci, G., L. Duimio, G. Peracchia, and S. Ottonello. 1995. Selective inactivation of two components of the multiprotein transcription factor TFIIIB in cycloheximide growth-arrested yeast cells. J. Biol. Chem. 270:13476-13482.
12. Leu gene promoters. Proc. Natl. Acad. Sci. USA 84:8763-8767.
13. Geiduschek, E. P., and G. A. Kassavetis. 1992. RNA polymerase III transcription complexes, p. 247-280. In S. L. McKnight and K. Yamamoto (ed.), Transcriptional regulation. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
14. Ghadivel, A., D. J. Hockman, and M. C. Schultz. A review of progress towards elucidating the role of protein kinase CK2 in polymerase III transcription: regulation of the TATA binding protein. Mol. Cell. Biochem., in press.
15. Ghavidel, A., and M. C. Schultz. 1997. Casein kinase II regulation of yeast TFIIIB is mediated by the TATA binding protein. Genes Dev. 11:2780-2789.
16. Ghavidel, A., and M. C. Schultz. Unpublished data.
17. Hammond, C. I., and M. J. Holland. 1983. Purification of yeast RNA polymerases using heparin agarose affinity chromatography. Transcriptional properties of the purified enzymes on defined templates. J. Biol. Chem. 258:3230-3241.
18. Hanna, D. E., A. Rethinaswamy, and C. V. C. Glover III. 1995. Casein kinase II is required for cell cycle progression during G1 and G2/M in Saccharomyces cerevisiae. J. Biol. Chem. 270:25905-25914.
19. Heitman, J., N. R. Movva, and M. N. Hall. 1991. Targets for cell cycle arrest by the immunosuppressant rapamycin in yeast. Science 253:905-909.
20. Helliwell, S. B., I. Howald, N. Barbet, and M. N. Hall. 1998. TOR2 is part of two related signaling pathways coordinating cell growth in Saccharomyces cerevisiae. Genetics 148:99-112.
21. Hereford, L. M., and L. H. Hartwell. 1974. Sequential gene function in the initiation of Saccharomyces cerevisiae DNA synthesis. J. Mol. Biol. 84:445-461.
22. Hockman, D. J., and M. C. Schultz. 1996. Casein kinase II is required for efficient transcription by RNA polymerase III. Mol. Cell. Biol. 16:892-898.
23. James, C. B. L., and T. H. Carter. 1992. Activation of protein kinase C inhibits adenovirus VA gene transcription in vitro. J. Gen. Virol. 73:3133-3139.
24. Jin, Y. J., and S. J. Burakoff. 1993. The 25-kDa FK506-binding protein is localized in the nucleus and associates with casein kinase II and nucleolin. Proc. Natl. Acad. Sci. USA 90:7769-7773.
25. Jones, E. W. 1991. Tackling the protease problem in Saccharomyces cerevisiae. Methods Enzymol. 194:428-453.
26. Ju, Q., and J. R. Warner. 1994. Ribosome synthesis during the growth cycle of Saccharomyces cerevisiae. Yeast 10:151-157.
27. Kassavetis, G. A., D. L. Riggs, R. Negri, L. H. Nguyen, and E. P. Geiduschek. 1989. Transcription factor IIIB generates extended DNA interactions in RNA polymerase III transcription complexes on tRNA genes. Mol. Cell. Biol. 9:2551-2566.
28. Kay, J. E. 1996. Structure-function relationships in the FK506-binding protein (FKBP) family of peptidylprolyl cis-trans isomerases. Biochem. J. 314:361-385.
29. Litchfield, D. W., and B. Lüscher. 1993. Casein kinase II in signal transduction and cell cycle regulation. Mol. Cell. Biochem. 127/128:187-199.
30. Lorenz, M. C., and J. Heitman. 1995. TOR mutations confer rapamycin resistance by preventing interaction with FKBP12 rapamycin. J. Biol. Chem. 270:27531-27537.
31. Pinna, L. A. 1990. Casein kinase 2: an 'eminence grise' in cellular regulation? Biochim. Biophys. Acta 1054:267-284.
32. Roeder, R. G. 1974. Multiple forms of deoxyribonucleic acid-dependent ribonucleic acid polymerase in Xenopus laevis. Isolation and partial characterization. J. Biol. Chem. 249:241-248.
33. Schultz, M. C., S. Y. Choe, and R. H. Reeder. 1991. Specific initiation by RNA polymerase I in a whole-cell extract from yeast. Proc. Natl. Acad. Sci. USA 88:1004-1008.
34. Schultz, M. C., D. J. Hockman, T. A. A. Harkness, W. I. Garinther, and B. A. Altheim. 1997. Chromatin assembly in a yeast whole-cell extract. Proc. Natl. Acad. Sci. USA 94:9034-9039.
35. Schultz, M. C., R. H. Reeder, and S. Hahn. 1992. Variants of the TATA-binding protein can distinguish subsets of RNA polymerase I, II, and III promoters. Cell 69:697-702.
36. 70 and TFIIIC. J. Biol. Chem. 270:28463-28470.
37. Stan, R., M. M. McLaughlin, R. Cafferkey, R. K. Johnson, M. Rosenberg, and G. P. Livi. 1994. Interaction between FKBP12-rapamycin and TOR involves a conserved serine residue. J. Biol. Chem. 269:32027-32030.
38. Thomas, B. J., and R. Rothstein. 1989. Elevated recombination rates in transcriptionally active DNA. Cell 56:619-630.
39. Tower, J., and B. Sollner-Webb. 1987. Transcription of mouse rDNA is regulated by an activated subform of RNA polymerase I. Cell 50:873-883.
40. Tower, J., and B. Sollner-Webb. 1988. Polymerase III transcription factor B activity is reduced in extracts of growth-restricted cells. Mol. Cell. Biol. 8:1001-1005.
41. van Zyl, W., W. Huang, A. A. Sneddon, M. Stark, S. Camier, M. Werner, C. Marck, A. Sentenac, and J. R. Broach. 1992. Inactivation of the protein phosphatase 2A regulatory subunit A results in morphological and transcriptional defects in Saccharomyces cerevisiae. Mol. Cell. Biol. 12:4946-4959.
42. Wang, H.-D., C.-H. Yuh, C. V. Dang, and D. L. Johnson. 1995. The hepatitis B virus X protein increases the cellular level of TATA-binding protein, which mediates transactivation of RNA polymerase III genes. Mol. Cell. Biol. 15:6720-6728.
43. Werner-Washburne, M., D. Brown, and E. Braun. 1991. Bcy1, the regulatory subunit of cAMP-dependent protein kinase A in yeast, is differentially modified in response to the physiological status of the cell. J. Biol. Chem. 266:19704-19709.
44. Werner-Washburne, M., E. Braun, G. C. Johnston, and R. A. Singer. 1993. Stationary phase in the yeast Saccharomyces cerevisiae. Microbiol. Rev. 57:383-401.
45. Werner-Washburne, M., E. L. Braun, M. E. Crawford, and V. M. Peck. 1996. Stationary phase in Saccharomyces cerevisiae. Mol. Microbiol. 19:1159-1166.
46. White, R. J., T. M. Gottlieb, C. S. Downes, and S. P. Jackson. 1995. Cell cycle regulation of RNA polymerase III transcription. Mol. Cell. Biol. 15:6653-6662.
47. Willis, I. M. 1993. RNA polymerase III. Genes, factors and transcriptional specificity. Eur. J. Biochem. 212:1-11.
48. Wilson, L. K., N. Dhillon, J. Thorner, and G. S. Martin. 1997. Casein kinase II catalyzes tyrosine phosphorylation of the yeast nucleolar immunophilin Fpr3. J. Biol. Chem. 272:12961-12967.
49. Zaragoza, D., and M. C. Schultz. Unpublished data.
50. Zheng, X.-F., D. Fiorentino, J. Chen, G. R. Crabtree, and S. L. Schreiber. 1995. TOR kinase domains are required for two distinct functions, only one of which is inhibited by rapamycin. Cell 82:121-130.