Genetic identification of factors that modulate ribosomal DNA transcription in Saccharomyces cerevisiae

Genetics

Volumn 182, Issue 1, 2009, Pages 105-119

  Hontz, Robert D ^a   Niederer, Rachel O ^a   Johnson, Joseph M ^a   Smith, Jeffrey S ^a  

^a UNIVERSITY OF VIRGINIA HEALTH SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA DIRECTED RNA POLYMERASE; RIBOSOME DNA; RNA POLYMERASE II; URACIL; HISTONE DEACETYLASE; MESSENGER RNA;

ARTICLE; CENTROMERE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DNA TRANSCRIPTION; GENE EXPRESSION REGULATION; GENE MUTATION; GENETIC IDENTIFICATION; GENETIC SCREENING; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PULSED FIELD GEL ELECTROPHORESIS; REAL TIME POLYMERASE CHAIN REACTION; REPORTER GENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; TRANSPOSON; WESTERN BLOTTING; CHROMATIN; GENETIC TRANSCRIPTION; GENETICS; METABOLISM;

SACCHAROMYCES CEREVISIAE;

BLOTTING, WESTERN; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; DNA TRANSPOSABLE ELEMENTS; DNA, RIBOSOMAL; HISTONE DEACETYLASES; MUTAGENESIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA POLYMERASE I; RNA, MESSENGER; SACCHAROMYCES CEREVISIAE; TRANSCRIPTION, GENETIC;

EID: 67849106506     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.108.100313     Document Type: Article

References (84)

1. AUSUBEL, F. M., R. BRENT, R. E. KINGSTON, D. D. MOORE, J. G. SEIDMAN et al. (Editors), 2000 Current Protocols in Molecular Biology. John Wiley & Sons, New York.
2. BODEM, J., G. DOBREVA, U. HOFFMANN-ROHRER, S. IBEN, H. ZENTGRAF et al., 2000 TIF-IA, the factor mediating growth-dependent control of ribosomal RNA synthesis, is the mammalian homolog of yeast Rrn3p. EMBO Rep. 1: 171-175.
3. BOEKE, J. D., F. LACROUTE and G. R. FINK, 1984 A positive selection for mutants lacking orotidine-59-phosphate decarboxylase activity in yeast: 5-fluoro-orotic acid resistance. Mol. Gen. Genet. 197: 345-346.
4. BRIGGS, S. D., M. BRYK, B. D. STRAHL, W. L. CHEUNG, J. K. DAVIE et al., 2001 Histone H3 lysine 4 methylation is mediated by Set1 and required for cell growth and rDNA silencing in Saccharomyces cerevisiae. Genes Dev. 15: 3286-3295.
5. BROACH, J. R., 1991 Ras-regulated signaling processes in Saccharomyces cerevisiae. Curr. Opin. Genet. Dev. 1: 370-377.
6. BRYK, M., M. BANERJEE, M. MURPHY, K. E. KNUDSEN, D. J. GARFINKEL et al., 1997 Transcriptional silencing of Ty1 elements in the RDN1 locus of yeast. Genes Dev. 11: 255-269.
7. BUCK, S. W., J. J. SANDMEIER and J. S. SMITH, 2002 RNA polymerase I propagates unidirectional spreading of rDNA silent chromatin. Cell 111: 1003-1014.
8. BURKE, D., D. DAWSON and T. STEARNS, 2000 Methods in Yeast Genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
9. BURNS, N., B. GRIMWADE, P. B. ROSS-MACDONALD, E. Y. CHOI, K. FINBERG et al., 1994 Large-scale analysis of gene expression, protein localization, and gene disruption in Saccharomyces cerevisiae. Genes Dev. 8: 1087-1105. (Pubitemid 24145671)
10. CARROZZA, M. J., B. LI, L. FLORENS, T. SUGANUMA, S. K. SWANSON et al., 2005 Histone H3 methylation by Set2 directs deacetylation of coding regions by Rpd3S to suppress spurious intragenic transcription. Cell 123: 581-592.
11. CHU, Y., R. SIMIC, M. H. WARNER, K. M. ARNDT and G. PRELICH, 2007 Regulation of histone modification and cryptic transcription by the Bur1 and Paf1 complexes. EMBO J. 26: 4646-4656. (Pubitemid 350126792)
12. CIOCI, F., L. VU, K. ELIASON, M. OAKES, I. N. SIDDIQI et al., 2003 Silencing in yeast rDNA chromatin: reciprocal relationship in gene expression between RNA polymerase I and II. Mol. Cell 12: 135-145.
13. COELHO, P. S., A. C. BRYAN, A. KUMAR, G. S. SHADEL and M. SNYDER, 2002 A novel mitochondrial protein, Tar1p, is encoded on the antisense strand of the nuclear 25S rDNA. Genes Dev. 16: 2755-2760.
14. 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. (Pubitemid 23180807)
15. DASGUPTA, A., S. A. JUEDES, R. O. SPROUSE and D. T. AUBLE, 2005 Mot1-mediated control of transcription complex assembly and activity. EMBO J. 24: 1717-1729.
16. DICKSON, R. C., C. SUMANASEKERA and R. L. LESTER, 2006 Functions and metabolism of sphingolipids in Saccharomyces cerevisiae. Prog. Lipid Res. 45: 447-465.
17. EGGERMONT, J., and N. J. PROUDFOOT, 1993 Poly(A) signals and transcriptional pause sites combine to prevent interference between RNA polymerase II promoters. EMBO J. 12: 2539-2548. (Pubitemid 23194205)
18. FATH, S., P. MILKEREIT, G. PEYROCHE, M. RIVA, C. CARLES et al., 2001 Differential roles of phosphorylation in the formation of transcriptional active RNA polymerase I. Proc. Natl. Acad. Sci. USA 98: 14334-14339.
19. FRENCH, S. L., Y. N. OSHEIM, F. CIOCI, M. NOMURA and A. L. BEYER, 2003 In exponentially growing Saccharomyces cerevisiae cells, rRNA synthesis is determined by the summed RNA polymerase I loading rate rather than by the number of active genes. Mol. Cell. Biol. 23: 1558-1568.
20. FRITZE, C. E., K. VERSCHUEREN, R. STRICH and R. E. ESPOSITO, 1997 Direct evidence for SIR2 modulation of chromatin structure in yeast rDNA. EMBO J. 16: 6495-6509.
21. GALLAGHER, J. E., D. A. DUNBAR, S. GRANNEMAN, B. M. MITCHELL, Y. OSHEIM et al., 2004 RNA polymerase I transcription and pre-rRNA processing are linked by specific SSU processome components. Genes Dev. 18: 2506-2517.
22. GERBER, J., A. REITER, R. STEINBAUER, S. JAKOB, C. D. KUHN et al., 2008 Site specific phosphorylation of yeast RNA polymerase I. Nucleic Acids Res. 36: 793-802.
23. GERRING, S. L., C. CONNELLY and P. HIETER, 1991 Positional mapping of genes by chromosome blotting and chromosome fragmentation. Methods Enzymol. 194: 57-77.
24. GOVIND, C. K., F. ZHANG, H. QIU, K. HOFMEYER and A. G. HINNEBUSCH, 2007 Gcn5 promotes acetylation, eviction, and methylation of nucleosomes in transcribed coding regions. Mol. Cell 25: 31-42.
25. HANNAN, R. D., and L. I. ROTHBLUM, 1995 Regulation of ribosomal DNA transcription during neonatal cardiomyocyte hypertrophy. Cardiovasc. Res. 30: 501-510.
26. HARASHIMA, T., and J. HEITMAN, 2002 The Galpha protein Gpa2 controls yeast differentiation by interacting with kelch repeat proteins that mimic Gbeta subunits. Mol. Cell 10: 163-173.
27. HARASHIMA, T., S. ANDERSON, J. R. YATES, III and J. HEITMAN, 2006 The kelch proteins Gpb1 and Gpb2 inhibit Ras activity via association with the yeast RasGAP neurofibromin homologs Ira1 and Ira2. Mol. Cell 22: 819-830.
28. HO, Y., A. GRUHLER, A. HEILBUT, G. D. BADER, L. MOORE et al., 2002 Systematic identification of protein complexes in Saccharomyces cerevisiae by mass spectrometry. Nature 415: 180-183. (Pubitemid 34059520)
29. HONTZ, R. D., S. L. FRENCH, M. L. OAKES, P. TONGAONKAR, M. NOMURA et al., 2008 Transcription of multiple yeast ribosomal DNA genes requires targeting of UAF to the promoter by Uaf30. Mol. Cell. Biol. 28: 6709-6719.
30. HOUSELEY, J., K. KOTOVIC, A. EL HAGE and D. TOLLERVEY, 2007 Trf4 targets ncRNAs from telomeric and rDNA spacer regions and functions in rDNA copy number control. EMBO J. 26: 4996-5006.
31. HWANG, W. W., S. VENKATASUBRAHMANYAM, A. G. IANCULESCU, A. TONG, C. BOONE et al., 2003 A conserved RING finger protein required for histone H2B monoubiquitination and cell size control. Mol. Cell 11: 261-266.
32. ITO, T., T. CHIBA, R. OZAWA, M. YOSHIDA, M. HATTORI et al., 2001 A comprehensive two-hybrid analysis to explore the yeast protein interactome. Proc. Natl. Acad. Sci. USA 98: 4569-4574.
33. JONES, H. S., J. KAWAUCHI, P. BRAGLIA, C. M. ALEN, N. A. KENT et al., 2007 RNA polymerase I in yeast transcribes dynamic nucleosomal rDNA. Nat. Struct. Mol. Biol. 14: 123-130.
34. JU, Q., and J. R. WARNER, 1994 Ribosome synthesis during the growth cycle of Saccharomyces cerevisiae. Yeast 10: 151-157. (Pubitemid 24099030)
35. KADOSH, D., and K. STRUHL, 1997 Repression by Ume6 involves recruitment of a complex containing Sin3 corepressor and Rpd3 histone deacetylase to target promoters. Cell 89: 365-371.
36. KEOGH, M. C., S. K. KURDISTANI, S. A. MORRIS, S. H. AHN, V. PODOLNY et al., 2005 Cotranscriptional set2 methylation of histone H3 lysine 36 recruits a repressive Rpd3 complex. Cell 123: 593-605.
37. KEYS, D. A., B.-S. LEE, J. A. DODD, T. T. NGUYEN, L. VU et al., 1996 Multiprotein transcription factor UAF interacts with the upstream element of the yeast RNA polymerase I promoter and forms a stable preinitiation complex. Genes Dev. 10: 887-903.
38. KLEIN, C., and K. STRUHL, 1994 Protein kinase A mediates growth-regulated expression of yeast ribosomal protein genes by modulating RAP1 transcriptional activity. Mol. Cell. Biol. 14: 1920-1928.
39. KOBAYASHI, T., and A. R. GANLEY, 2005 Recombination regulation by transcription-induced cohesin dissociation in rDNA repeats. Science 309: 1581-1584.
40. KROGAN, N. J., J. DOVER, A. WOOD, J. SCHNEIDER, J. HEIDT et al., 2003 The Paf1 complex is required for histone H3 methylation by COMPASS and Dot1p: linking transcriptional elongation to histone methylation. Mol. Cell 11: 721-729. (Pubitemid 36385125)
41. LALO, D., J. S. STEFFAN, J. A. DODD and M. NOMURA, 1996 RRN11 encodes the third subunit of the complex containing Rrn6p and Rrn7p that is essential for the initiation of rDNA transcription by yeast RNA polymerase I. J. Biol. Chem. 271: 21062-21067.
42. LI, B., M. GOGOL, M. CAREY, D. LEE, C. SEIDEL et al., 2007 Combined action of PHD and chromo domains directs the Rpd3S HDAC to transcribed chromatin. Science 316: 1050-1054.
43. LI, C., J. E. MUELLER and M. BRYK, 2006 Sir2 represses endogenous polymerase II transcription units in the ribosomal DNA nontranscribed spacer. Mol. Biol. Cell 17: 3848-3859.
44. LONGTINE, M. S., A. MCKENZIE, III, D. J. DEMARINI, N. G. SHAH, A. WACH et al., 1998 Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14: 953-961.
45. LORENZ, M. C., and J. HEITMAN, 1998 Regulators of pseudohyphal differentiation in Saccharomyces cerevisiae identified through multicopy suppressor analysis in ammonium permease mutant strains. Genetics 150: 1443-1457.
46. MARTIN, D. E., T. POWERS and M. N. HALL, 2006 Regulation of ribosome biogenesis: Where is TOR? Cell Metab. 4: 259-260.
47. MARTON, H. A., and S. DESIDERIO, 2008 The Paf1 complex promotes displacement of histones upon rapid induction of transcription by RNA polymerase II. BMC Mol. Biol. 9: 4.
48. MILKEREIT, P., and H. TSCHOCHNER, 1998 A specialized form of RNA polymerase I, essential for initiation and growth-dependent regulation of rRNA synthesis, is disrupted during transcription. EMBO J. 17: 3692-3703.
49. MOSS, T., F. LANGLOIS, T. GAGNON-KUGLER and V. STEFANOVSKY, 2007 A housekeeper with power of attorney: the rRNA genes in ribosome biogenesis. Cell Mol. Life Sci. 64: 29-49.
50. MUELLER, J. E., M. CANZE and M. BRYK, 2006 The requirements for COMPASS and Paf1 in transcriptional silencing and methylation of histone H3 in Saccharomyces cerevisiae. Genetics 173: 557-567.
51. Nomura, M., 2001 Ribosomal RNA genes, RNA polymerases, nucleolar structures, and synthesis of rRNA in the yeast Saccharomyces cerevisiae. Cold Spring Harbor Symp. Quant. Biol. 66: 555-565.
52. OAKES, M. L., I. SIDDIQI, S. L. FRENCH, L. VU, M. SATO et al., 2006 Role of histone deacetylase Rpd3 in regulating rRNA gene transcription and nucleolar structure in yeast. Mol. Cell. Biol. 26: 3889-3901.
53. PEETERS, T., W. LOUWET, R. GELADE, D. NAUWELAERS, J. M. THEVELEIN et al., 2006 Kelch-repeat proteins interacting with the Galpha protein Gpa2 bypass adenylate cyclase for direct regulation of protein kinase A in yeast. Proc. Natl. Acad. Sci. USA 103: 13034-13039.
54. PIJNAPPEL, W. W., D. SCHAFT, A. ROGUEV, A. SHEVCHENKO, H. TEKOTTE et al., 2001 The S. cerevisiae SET3 complex includes two histone deacetylases, Hos2 and Hst1, and is a meiotic-specific repressor of the sporulation gene program. Genes Dev. 15: 2991-3004.
55. PORTER, S. E., K. L. PENHEITER and J. A. JAEHNING, 2005 Separation of the Saccharomyces cerevisiae Paf1 complex from RNA polymerase II results in changes in its subnuclear localization. Eukaryot. Cell 4: 209-220.
56. REEDER, R. H., P. GUEVARA and J. G. ROAN, 1999 Saccharomyces cerevisiae RNA polymerase I terminates transcription at the Reb1 terminator in vivo. Mol. Cell. Biol. 19: 7369-7376.
57. ROBYR, D., Y. SUKA, I. XENARIOS, S. K. KURDISTANI, A. WANG et al., 2002 Microarray deacetylation maps determine genome-wide functions for yeast histone deacetylases. Cell 109: 437-446.
58. RUSSELL, M., J. BRADSHAW-ROUSE, D. MARKWARDT and W. HEIDEMAN, 1993 Changes in gene expression in the Ras/adenylate cyclase system of Saccharomyces cerevisiae: correlation with cAMP levels and growth arrest. Mol. Biol. Cell 4: 757-765.
59. SANDMEIER, J. J., S. FRENCH, Y. OSHEIM, W. L. CHEUNG, C. M. GALLO et al., 2002 RPD3 is required for the inactivation of yeast ribosomal DNA genes in stationary phase. EMBO J. 21: 4959-4968.
60. SANIJ, E., G. POORTINGA, K. SHARKEY, S. HUNG, T. P. HOLLOWAY et al., 2008 UBF levels determine the number of active ribosomal RNA genes in mammals. J. Cell Biol. 183: 1259-1274.
61. SCHMELZLE, T., T. BECK, D. E. MARTIN and M. N. HALL, 2004 Activation of the RAS/cyclic AMP pathway suppresses a TOR deficiency in yeast. Mol. Cell. Biol. 24: 338-351.
62. SCHULTZ, M. C., S. J. BRILL, Q. JU, R. STERNGLANZ and R. H. REEDER, 1992 Topoisomerases and yeast rRNA transcription: negative supercoiling stimulates initiation and topoisomerase activity is required for elongation. Genes Dev. 6: 1332-1341.
63. SHOU, W., J. H. SEOL, A. SHEVCHENKO, C. BASKERVILLE, D. MOAZED et al., 1999 Exit from mitosis is triggered by Tem1-dependent release of the protein phosphatase Cdc14 from nucleolar RENT complex. Cell 97: 233-244.
64. SIDDIQI, I. N., J. A. DODD, L. VU, K. ELIASON, M. L. OAKES et al., 2001 Transcription of chromosomal rRNA genes by both RNA polymerase I and II in yeast uaf30 mutants lacking the 30 kDa subunit of transcription factor UAF. EMBO J. 20: 4512-4521.
65. SMITH, J. S., and J. D. BOEKE, 1997 An unusual form of transcriptional silencing in yeast ribosomal DNA. Genes Dev. 11: 241-254.
66. SMITH, J. S., C. B. BRACHMANN, L. PILLUS and J. D. BOEKE, 1998 Distribution of a limited Sir2 protein pool regulates the strength of yeast rDNA silencing and is modulated by Sir4p. Genetics 149: 1205-1219.
67. SMITH, J. S., E. CAPUTO and J. D. BOEKE, 1999 A genetic screen for ribosomal DNA silencing defects identifies multiple DNA replication and chromatin-modulating factors. Mol. Cell. Biol. 19: 3184-3197.
68. SQUAZZO, S. L., P. J. COSTA, D. L. LINDSTROM, K. E. KUMER, R. SIMIC et al., 2002 The Paf1 complex physically and functionally associates with transcription elongation factors in vivo. EMBO J. 21: 1764-1774.
69. STEFANOVSKY, V., F. LANGLOIS, T. GAGNON-KUGLER, L. I. ROTHBLUM and T. MOSS, 2006 Growth factor signaling regulates elongation of RNA polymerase I transcription in mammals via UBF phosphorylation and r-chromatin remodeling. Mol. Cell 21: 629-639.
70. TANNY, J. C., G. J. DOWD, J. HUANG, H. HILZ and D. MOAZED, 1999 An enzymatic activity in the yeast Sir2 protein that is essential for gene silencing. Cell 99: 735-745.
71. THEVELEIN, J. M., and J. H. DE WINDE, 1999 Novel sensing mechanisms and targets for the cAMP-protein kinase A pathway in the yeast Saccharomyces cerevisiae. Mol. Microbiol. 33: 904-918.
72. TONG, A. H., G. LESAGE, G. D. BADER, H. DING, H. XU et al., 2004 Global mapping of the yeast genetic interaction network. Science 303: 808-813. (Pubitemid 38174652)
73. TSANG, C. K., and X. F. ZHENG, 2007 TOR-in(g) the nucleus. Cell Cycle 6: 25-29.
74. VASILJEVA, L., M. KIM, N. TERZI, L. M. SOARES and S. BURATOWSKI, 2008 Transcription termination and RNA degradation contribute to silencing of RNA polymerase II transcription within heterochromatin. Mol. Cell 29: 313-323.
75. VU, L., I. SIDDIQI, B.-S. LEE, C. A. JOSAITIS and M. NOMURA, 1999 RNA polymerase switch in transcription of yeast rDNA: role of transcription factor UAF (upstream activation factor) in silencing rDNA transcription by RNA polymerase I. Proc. Natl. Acad. Sci. USA 96: 4390-4395.
76. WANG, A., S. K. KURDISTANI and M. GRUNSTEIN, 2002 Requirement of Hos2 histone deacetylase for gene activity in yeast. Science 298: 1412-1414.
77. WARNER, J. R., 1999 The economics of ribosome biosynthesis in yeast. Trends Biochem. Sci. 24: 437-440.
78. WERY, M., E. SHEMATOROVA, B. VAN DRIESSCHE, J. VANDENHAUTE, P. THURIAUX et al., 2004 Members of the SAGA and Mediator complexes are partners of the transcription elongation factor TFIIS. EMBO J. 23: 4232-4242.
79. WHITE, R. J., 2005 RNA polymerases I and III, growth Wind, M., and D. Reines, 2000 Transcription elongation factor SII. BioEssays 22: 327-336.
80. WOOD, A., N. J. KROGAN, J. DOVER, J. SCHNEIDER, J. HEIDT et al., 2003 Bre1, an E3 ubiquitin ligase required for recruitment and substrate selection of Rad6 at a promoter. Mol. Cell 11: 267-274.
81. WORKMAN, J. L., 2006 Nucleosome displacement in transcription. Genes Dev. 20: 2009-2017.
82. XIAO, T., H. HALL, K. O. KIZER, Y. SHIBATA, M. C. HALL et al., 2003 Phosphorylation of RNA polymerase II CTD regulates H3 methylation in yeast. Genes Dev. 17: 654-663. (Pubitemid 36307549)
83. ZHANG, Y., M. L. SIKES, A. L. BEYER and D. A. SCHNEIDER, 2009 The Paf1 complex is required for efficient transcription elongation by RNA polymerase I. Proc. Natl. Acad. Sci. USA 106: 2153-2158.
84. ZURITA-MARTINEZ, S. A., and M. E. CARDENAS, 2005 Tor and cyclic AMP-protein kinase A: two parallel pathways regulating expression of genes required for cell growth. Eukaryot. Cell 4: 63-71.