Reduction in ribosomal protein synthesis is sufficient to explain major effects on ribosome production after short-term TOR inactivation in Saccharomyces cerevisiae

Molecular and Cellular Biology

Volumn 31, Issue 4, 2011, Pages 803-817

  Reiter, Alarich ^a   Steinbauer, Robert ^a   Philippi, Anja ^a,b   Gerber, Jochen ^a   Tschochner, Herbert ^a   Milkereit, Philipp ^a   Griesenbeck, Joachim ^a  

^a UNIVERSITY OF REGENSBURG   (Germany)

^b KIST Europe Forschungsgesellschaft mbH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLOHEXIMIDE; DNA DIRECTED RNA POLYMERASE; PROTEIN PRECURSOR; RAPAMYCIN; RIBOSOME PROTEIN; RIBOSOME RNA; TARGET OF RAPAMYCIN KINASE;

ARTICLE; ENZYME INACTIVATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN SYNTHESIS; RIBOSOME; RIBOSOME SUBUNIT; RNA GENE; RNA PROCESSING; RNA TRANSCRIPTION; SACCHAROMYCES CEREVISIAE; TRANSLATION REGULATION;

BASE SEQUENCE; CYCLOHEXIMIDE; DNA, FUNGAL; GENES, FUNGAL; GENES, RRNA; PROTEIN-SERINE-THREONINE KINASES; RIBOSOMAL PROTEINS; RIBOSOMES; RNA POLYMERASE I; RNA PRECURSORS; RNA, FUNGAL; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SIGNAL TRANSDUCTION; SIROLIMUS;

EUKARYOTA; SACCHAROMYCES CEREVISIAE;

EID: 79251576154     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.01227-10     Document Type: Article

References (88)

1. Albig, A. R., and C. J. Decker. 2001. The target of rapamycin signaling pathway regulates mRNA turnover in the yeast Saccharomyces cerevisiae. Mol. Biol. Cell 12:3428-3438.
2. Barbet, N. C., et al. 1996. TOR controls translation initiation and early G1 progression in yeast. Mol. Biol. Cell 7:25-42.
3. Beretta, L., A. C. Gingras, Y. V. Svitkin, M. N. Hall, and N. Sonenberg. 1996. Rapamycin blocks the phosphorylation of 4E-BP1 and inhibits cap-dependent initiation of translation. EMBO J. 15:658-664.
4. Berger, A. B., et al. 2007. Hmo1 is required for TOR-dependent regulation of ribosomal protein gene transcription. Mol. Cell. Biol. 27:8015-8026.
5. Berset, C., H. Trachsel, and M. Altmann. 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. U. S. A. 95:4264-4269. (Pubitemid 128620773)
6. Brachmann, C. B., et al. 1998. Designer deletion strains derived from Saccharomyces cerevisiae S288C: a useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast 14:115-132.
7. Cadwell, C., H. J. Yoon, Y. Zebarjadian, and J. Carbon. 1997. The yeast nucleolar protein Cbf5p is involved in rRNA biosynthesis and interacts genetically with the RNA polymerase I transcription factor RRN3. Mol. Cell. Biol. 17:6175-6183.
8. 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.
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. 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.
11. Claypool, J. A., et al. 2004. Tor pathway regulates Rrn3p-dependent recruitment of yeast RNA polymerase I to the promoter but does not participate in alteration of the number of active genes. Mol. Biol. Cell 15:946-956.
12. Conconi, A., R. M. Widmer, T. Koller, and J. M. Sogo. 1989. Two different chromatin structures coexist in ribosomal RNA genes throughout the cell cycle. Cell 57:753-761.
13. Dammann, R., R. Lucchini, T. Koller, and J. M. Sogo. 1993. Chromatin structures and transcription of rDNA in yeast Saccharomyces cerevisiae. Nucleic Acids Res. 21:2331-2338.
14. de Kloet, S. R. 1966. Ribonucleic acid synthesis in yeast. The effect of cycloheximide on the synthesis of ribonucleic acid in Saccharomyces carlsbergensis. Biochem. J. 99:566-581.
15. Deutschbauer, A. M., et al. 2005. Mechanisms of haploinsufficiency revealed by genome-wide profiling in yeast. Genetics 169:1915-1925. (Pubitemid 40695608)
16. Dodd, J., J. M. Kolb, and M. Nomura. 1991. Lack of complete cooperativity of ribosome assembly in vitro and its possible relevance to in vivo ribosome assembly and the regulation of ribosomal gene expression. Biochimie 73:757-767.
17. Donovan, D. M., et al. 1990. Functional analysis of a duplicated linked pair of ribosomal protein genes in Saccharomyces cerevisiae. Mol. Cell. Biol. 10:6097-6100.
18. Fatica, A., and D. Tollervey. 2002. Making ribosomes. Curr. Opin. Cell Biol. 14:313-318.
19. Ferreira-Cerca, S., G. Poll, P. E. Gleizes, H. Tschochner, and P. Milkereit. 2005. Roles of eukaryotic ribosomal proteins in maturation and transport of pre-18S rRNA and ribosome function. Mol. Cell 20:263-275.
20. Ferreira-Cerca, S., et al. 2007. Analysis of the in vivo assembly pathway of eukaryotic 40S ribosomal proteins. Mol. Cell 28:446-457.
21. Gasch, A. P., et al. 2000. Genomic expression programs in the response of yeast cells to environmental changes. Mol. Biol. Cell 11:4241-4257.
22. Goetze, H., et al. 2010. Alternative chromatin structures of the 35S ribosomal RNA genes in Saccharomyces cerevisiae provide a molecular basis for the selective recruitment of RNA polymerases I and II. Mol. Cell. Biol. 30:2028-2045.
23. Gokal, P. K., A. H. Cavanaugh, and E. A. Thompson, Jr. 1986. The effects of cycloheximide upon transcription of rRNA, 5S RNA, and tRNA genes. J. Biol. Chem. 261:2536-2541.
24. Gorenstein, C., and J. R. Warner. 1976. Coordinate regulation of the synthesis of eukaryotic ribosomal proteins. Proc. Natl. Acad. Sci. U. S. A. 73:1547-1551.
25. Gorenstein, C., and J. R. Warner. 1977. Synthesis and turnover of ribosomal proteins in the absence of 60S subunit assembly in Saccharomyces cerevisiae. Mol. Gen. Genet. 157:327-332.
26. Hall, D. B., J. T. Wade, and K. Struhl. 2006. An HMG protein, Hmo1, associates with promoters of many ribosomal protein genes and throughout the rRNA gene locus in Saccharomyces cerevisiae. Mol. Cell. Biol. 26:3672-3679.
27. 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. U. S. A. 96:14866-14870.
28. Hartwell, L. H., C. S. McLaughlin, and J. R. Warner. 1970. Identification of ten genes that control ribosome formation in yeast. Mol. Gen. Genet. 109:42-56.
29. Henras, A. K., et al. 2008. The post-transcriptional steps of eukaryotic ribosome biogenesis. Cell Mol. Life Sci. 65:2334-2359.
30. Hiller, M. M., A. Finger, M. Schweiger, and D. H. Wolf. 1996. ER degradation of a misfolded luminal protein by the cytosolic ubiquitin-proteasome pathway. Science 273:1725-1728.
31. Holz, M. K., B. A. Ballif, S. P. Gygi, and J. Blenis. 2005. mTOR and S6K1 mediate assembly of the translation preinitiation complex through dynamic protein interchange and ordered phosphorylation events. Cell 123:569-580.
32. Honma, Y., et al. 2006. TOR regulates late steps of ribosome maturation in the nucleoplasm via Nog1 in response to nutrients. EMBO J. 25:3832-3842.
33. Hughes, J. D., P. W. Estep, S. Tavazoie, and G. M. Church. 2000. Computational identification of cis-regulatory elements associated with groups of functionally related genes in Saccharomyces cerevisiae. J. Mol. Biol. 296:1205-1214.
34. Jorgensen, P., J. L. Nishikawa, B. J. Breitkreutz, and M. Tyers. 2002. Systematic identification of pathways that couple cell growth and division in yeast. Science 297:395-400.
35. Jorgensen, P., et al. 2004. A dynamic transcriptional network communicates growth potential to ribosome synthesis and critical cell size. Genes Dev. 18:2491-2505.
36. Karagyozov, L. K., B. B. Stoyanova, and A. A. Hadjiolov. 1980. Effect of cycloheximide on the in vivo and in vitro synthesis of ribosomal RNA in rat liver. Biochim. Biophys. Acta 607:295-303.
37. Kasahara, K., et al. 2007. Assembly of regulatory factors on rRNA and ribosomal protein genes in Saccharomyces cerevisiae. Mol. Cell. Biol. 27:6686-6705.
38. Kim, J. E., and J. Chen. 2000. Cytoplasmic-nuclear shuttling of FKBP12-rapamycin-associated protein is involved in rapamycin-sensitive signaling and translation initiation. Proc. Natl. Acad. Sci. U. S. A. 97:14340-14345.
39. Knop, M., et al. 1999. Epitope tagging of yeast genes using a PCR-based strategy: more tags and improved practical routines. Yeast 15:963-972. (Pubitemid 129703097)
40. Kruiswijk, T., R. J. Planta, and J. M. Krop. 1978. The course of the assembly of ribosomal subunits in yeast. Biochim. Biophys. Acta 517:378-389.
41. Laferte, A., et al. 2006. The transcriptional activity of RNA polymerase I is a key determinant for the level of all ribosome components. Genes Dev. 20:2030-2040.
42. Li, H., C. K. Tsang, M. Watkins, P. G. Bertram, and X. F. Zheng. 2006. Nutrient regulates Tor1 nuclear localization and association with rDNA promoter. Nature 442:1058-1061.
43. Lin, T. A., X. Kong, A. R. Saltiel, P. J. Blackshear, and J. C. Lawrence, Jr. 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.
44. Lipton, J. M., and S. R. Ellis. 2009. Diamond-Blackfan anemia: diagnosis, treatment, and molecular pathogenesis. Hematol. Oncol. Clin. North Am. 23:261-282.
45. Lipton, J. M., and S. R. Ellis. 2010. Diamond Blackfan anemia 2008-2009: broadening the scope of ribosome biogenesis disorders. Curr. Opin. Pediatr. 22:12-19.
46. Lucioli, A., et al. 1988. Gene dosage alteration of L2 ribosomal protein genes in Saccharomyces cerevisiae: effects on ribosome synthesis. Mol. Cell. Biol. 8:4792-4798.
47. Maden, B. E., M. H. Vaughan, J. R. Warner, and J. E. Darnell. 1969. Effects of valine deprivation on ribosome formation in HeLa cells. J. Mol. Biol. 45:265-275.
48. Marion, R. M., et al. 2004. Sfp1 is a stress- and nutrient-sensitive regulator of ribosomal protein gene expression. Proc. Natl. Acad. Sci. U. S. A. 101:14315-14322.
49. Martin, D. E., A. Soulard, and M. N. Hall. 2004. TOR regulates ribosomal protein gene expression via PKA and the Forkhead transcription factor FHL1. Cell 119:969-979.
50. Mayer, C., and I. Grummt. 2006. Ribosome biogenesis and cell growth: mTOR coordinates transcription by all three classes of nuclear RNA polymerases. Oncogene 25:6384-6391.
51. Mayer, C., J. Zhao, X. Yuan, and I. Grummt. 2004. mTOR-dependent activation of the transcription factor TIF-IA links rRNA synthesis to nutrient availability. Genes Dev. 18:423-434.
52. Merz, K., et al. 2008. Actively transcribed rRNA genes in S. cerevisiae are organized in a specialized chromatin associated with the high-mobility group protein Hmo1 and are largely devoid of histone molecules. Genes Dev. 22:1190-1204.
53. O'Donohue, M. F., V. Choesmel, M. Faubladier, G. Fichant, and P. E. Gleizes. 2010. Functional dichotomy of ribosomal proteins during the synthesis of mammalian 40S ribosomal subunits. J. Cell Biol. 190:853-866.
54. Oeffinger, M., M. Dlakic, and D. Tollervey. 2004. A pre-ribosome- associated HEAT-repeat protein is required for export of both ribosomal subunits. Genes Dev. 18:196-209.
55. Petitjean, A., N. Bonneaud, and F. Lacroute. 1995. The duplicated Saccharomyces cerevisiae gene SSM1 encodes a eucaryotic homolog of the eubacterial and archaebacterial L1 ribosomal proteins. Mol. Cell. Biol. 15:5071-5081.
56. Philippi, A., et al. 2010. TOR-dependent reduction in the expression level of Rrn3p lowers the activity of the yeast RNA Pol I machinery, but does not account for the strong inhibition of rRNA production. Nucleic Acids Res. 38:5315-5326.
57. Poll, G., et al. 2009. rRNA maturation in yeast cells depleted of large ribosomal subunit proteins. PLoS One 4:e8249.
58. 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.
59. Robledo, S., et al. 2008. The role of human ribosomal proteins in the maturation of rRNA and ribosome production. RNA 14:1918-1929.
60. Rosbash, M., P. K. Harris, J. L. Woolford, Jr., and J. L. Teem. 1981. The effect of temperature-sensitive RNA mutants on the transcription products from cloned ribosomal protein genes of yeast. Cell 24:679-686.
61. Rudra, D., Y. Zhao, and J. R. Warner. 2005. Central role of Ifh1p-Fhl1p interaction in the synthesis of yeast ribosomal proteins. EMBO J. 24:533-542.
62. Schawalder, S. B., et al. 2004. Growth-regulated recruitment of the essential yeast ribosomal protein gene activator Ifh1. Nature 432:1058-1061.
63. Schmid, M., T. Durussel, and U. K. Laemmli. 2004. ChIC and ChEC; genomic mapping of chromatin proteins. Mol. Cell 16:147-157.
64. Seufert, W., and S. Jentsch. 1992. In vivo function of the proteasome in the ubiquitin pathway. EMBO J. 11:3077-3080.
65. Shevchenko, A., H. Tomas, J. Havlis, J. V. Olsen, and M. Mann. 2006. In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat. Protoc. 1:2856-2860.
66. Shevchenko, A., M. Wilm, O. Vorm, and M. Mann. 1996. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 68:850-858.
67. Shulman, R. W., C. E. Sripati, and J. R. Warner. 1977. Noncoordinated transcription in the absence of protein synthesis in yeast. J. Biol. Chem. 252:1344-1349.
68. Song, J. M., E. Cheung, and J. C. Rabinowitz. 1996. Organization and characterization of the two yeast ribosomal protein YL19 genes. Curr. Genet. 30:273-278.
69. Stoyanova, B. B., and M. D. Dabeva. 1980. Ribosomal RNA precursor transcription in rat liver is not dependent on continuous synthesis of proteins. Biochim. Biophys. Acta 608:358-367.
70. Stoyanova, B. B., and A. A. Hadjiolov. 1979. Alterations in the processing of rat-liver ribosomal RNA caused by cycloheximide inhibition of protein synthesis. Eur. J. Biochem. 96:349-356.
71. Thomas, B. J., and R. Rothstein. 1989. Elevated recombination rates in transcriptionally active DNA. Cell 56:619-630.
72. Tschochner, H., and E. Hurt. 2003. Pre-ribosomes on the road from the nucleolus to the cytoplasm. Trends Cell Biol. 13:255-263.
73. Udem, S. A., and J. R. Warner. 1972. Ribosomal RNA synthesis in Saccharomyces cerevisiae. J. Mol. Biol. 65:227-242.
74. van Beekvelt, C. A., et al. 2001. All three functional domains of the large ribosomal subunit protein L25 are required for both early and late pre-rRNA processing steps in Saccharomyces cerevisiae. Nucleic Acids Res. 29:5001-5008.
75. van Beekvelt, C. A., et al. 2000. Domain III of Saccharomyces cerevisiae 25 S ribosomal RNA: its role in binding of ribosomal protein L25 and 60 S subunit formation. J. Mol. Biol. 296:7-17.
76. Vanrobays, E., et al. 2008. TOR regulates the subcellular distribution of DIM2, a KH domain protein required for cotranscriptional ribosome assembly and pre-40S ribosome export. RNA 14:2061-2073.
77. von Manteuffel, S. R., A. C. Gingras, X. F. Ming, N. Sonenberg, and G. Thomas. 1996. 4E-BP1 phosphorylation is mediated by the FRAP-p70s6k pathway and is independent of mitogen-activated protein kinase. Proc. Natl. Acad. Sci. U. S. A. 93:4076-4080.
78. Wade, C., K. A. Shea, R. V. Jensen, and M. A. McAlear. 2001. EBP2 is a member of the yeast RRB regulon, a transcriptionally coregulated set of genes that are required for ribosome and rRNA biosynthesis. Mol. Cell. Biol. 21:8638-8650.
79. Wade, J. T., D. B. Hall, and K. Struhl. 2004. The transcription factor Ifh1 is a key regulator of yeast ribosomal protein genes. Nature 432:1054-1058.
80. Warner, J. R. 1999. The economics of ribosome biosynthesis in yeast. Trends Biochem. Sci. 24:437-440.
81. Warner, J. R. 1977. In the absence of ribosomal RNA synthesis, the ribosomal proteins of HeLa cells are synthesized normally and degraded rapidly. J. Mol. Biol. 115:315-333.
82. Warner, J. R., and C. Gorenstein. 1978. Yeast has a true stringent response. Nature 275:338-339.
83. Warner, J. R., and S. A. Udem. 1972. Temperature sensitive mutations affecting ribosome synthesis in Saccharomyces cerevisiae. J. Mol. Biol. 65:243-257.
84. Wei, Y., C. K. Tsang, and X. F. Zheng. 2009. Mechanisms of regulation of RNA polymerase III-dependent transcription by TORC1. EMBO J. 28:2220-2230.
85. Wittekind, M., et al. 1990. Conditional expression of RPA190, the gene encoding the largest subunit of yeast RNA polymerase I: effects of decreased rRNA synthesis on ribosomal protein synthesis. Mol. Cell. Biol. 10:2049-2059.
86. Wullschleger, S., R. Loewith, and M. N. Hall. 2006. TOR signaling in growth and metabolism. Cell 124:471-484.
87. Yon, J., A. Giallongo, and M. Fried. 1991. The organization and expression of the Saccharomyces cerevisiae L4 ribosomal protein genes and their identification as the homologues of the mammalian ribosomal protein gene L7a. Mol. Gen. Genet. 227:72-80.
88. Zhang, Y., A. D. Smith IV, M. B. Renfrow, and D. A. Schneider. 2010. The RNA polymerase-associated factor 1 complex (Paf1C) directly increases the elongation rate of RNA polymerase I and is required for efficient regulation of rRNA synthesis. J. Biol. Chem. 285:14152-14159.