The Cyc8-Tup1 complex inhibits transcription primarily by masking the activation domain of the recruiting protein

Genes and Development

Volumn 25, Issue 23, 2011, Pages 2525-2539

  Wong, Koon Ho ^a   Struhl, Kevin ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Cyc8 Tup1; Gene regulation; Stress responses transcriptional activation; Transcriptional corepressor; Transcriptional repression

Indexed keywords

COREPRESSOR PROTEIN; NUCLEOSOME ANTIBODY;

ARTICLE; BACTERIAL GENE; CYC8 TUP1 GENE; DNA BINDING; GENE EXPRESSION; GENE INTERACTION; GENE TARGETING; HISTONE ACETYLATION; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

CHROMOSOMAL PROTEINS, NON-HISTONE; GENE EXPRESSION REGULATION, FUNGAL; MEDIATOR COMPLEX; MODELS, BIOLOGICAL; NUCLEAR PROTEINS; REPRESSOR PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 82955217673     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.179275.111     Document Type: Article

References (75)

1. Bryant GO, Prabhu V, Floer M, Wang X, Spagna D, Schreiber D, Ptashne M. 2008. Activator control of nucleosome occupancy in activation and repression of transcription. PLoS Biol 6: 2928-2939.
2. Buhler M, Verdel A, Moazed D. 2006. Tethering RITS to a nascent transcript initiates RNAi-and heterochromatindependent gene silencing. Cell 125: 873-886.
3. Cooper JP, Roth SY, Simpson RT. 1994. The global transcriptional regulators, SSN6 and TUP1, play distinct roles in the establishment of a repressive chromatin structure. Genes Dev 8: 1400-1410.
4. Davie JK, Edmondson DG, Coco CB, Dent SY. 2003. Tup1-Ssn6 interacts with multiple class I histone deacetylases in vivo. J Biol Chem 278: 50158-50162.
5. Desimone AM, Laney JD. 2010. Corepressor-directed preacetylation of histone H3 in promoter chromatin primes rapid transcriptional switching of cell-type-specific genes in yeast. Mol Cell Biol 30: 3342-3356.
6. Dohmen RJ, Varshavsky A. 2005. Heat-inducible degron and the making of conditional mutants. Methods Enzymol 399: 799-822.
7. Ducker CE, Simpson RT. 2000. The organized chromatin domain of the repressed yeast a cell-specific gene STE6 contains twomolecules of the corepressor Tup1p per nucleosome. EMBO J 19: 400-409.
8. Edmondson DG, Smith MM, Roth SY. 1996. Repression domain of the yeast global repressor Tup1 interacts directly with histones H3 and H4. Genes Dev 10: 1247-1259.
9. Fan X, Lamarre-Vincent N, Wang Q, Struhl K. 2008. Extensive chromatin fragmentation improves enrichment of protein binding sites in chromatin immunoprecipitation experiments. Nucleic Acids Res 36: e125. doi: 10.1093/nar/gkn535.
10. Fan X, Geisberg JV, Wong KH, Jin Y. 2011. Conditional depletion of nuclear proteins by the anchor away system. Curr Protoc Mol Biol 93: 1310B1-1310B8. doi:10.1002/0471142727.mb1310bs93.
11. Fleming AB, Pennings S. 2001. Antagonistic remodelling by Swi-Snf and Tup1-Ssn6 of an extensive chromatin region forms the background for FLO1 gene regulation. EMBO J 20: 5219-5231.
12. Fleming AB, Pennings S. 2007. Tup1-Ssn6 and Swi-Snf remodelling activities influence long-range chromatin organization upstream of the yeast SUC2 gene. Nucleic Acids Res 35: 5520-5531.
13. Fragiadakis GS, Tzamarias D, Alexandraki D. 2004. Nhp6 facilitates Aft1 binding and Ssn6 recruitment, both essential for FRE2 transcriptional activation. EMBO J 23: 333-342.
14. Garcia-Gimeno MA, Struhl K. 2000. Aca1 and Aca2, ATF/CREB activators in Saccharomyces cerevisiae, are important for carbon-source utilization but not the response to stress. Mol Cell Biol 20: 4340-4349.
15. Gavin IM, Kladde MP, Simpson RT. 2000. Tup1p represses Mcm1p transcriptional activation and chromatin remodeling of an a-cell-specific gene. EMBO J 19: 5875-5883.
16. Geisberg JV, Struhl K. 2000. TATA-binding protein mutants that increase transcription from enhancerless and repressed promoters in vivo. Mol Cell Biol 20: 1478-1488.
17. Gligoris T, Thireos G, Tzamarias D. 2007. The Tup1 corepressor directs Htz1 deposition at a specific promoter nucleosome marking the GAL1 gene for rapid activation. Mol Cell Biol 27: 4198-4205.
18. Green SR, Johnson AD. 2004. Promoter-dependent roles for the Srb10 cyclin-dependent kinase and the Hda1 deacetylase in Tup1-mediated repression in Saccharomyces cerevisiae. Mol Biol Cell 15: 4191-4202.
19. Green SR, Johnson AD. 2005. Genome-wide analysis of the functions of a conserved surface on the corepressor Tup1. Mol Biol Cell 16: 2605-2613.
20. Grewal SI, Elgin SC. 2007. Transcription and RNA interference in the formation of heterochromatin. Nature 447: 399-406.
21. Grewal SI, Jia S. 2007. Heterochromatin revisited. Natl Rev 8: 35-46.
22. Gromoller A, Lehming N. 2000. Srb7p is a physical and physiological target of Tup1p. EMBO J 19: 6845-6852.
23. Han SJ, Lee JS, Kang JS, Kim YJ. 2001. Med9/Cse2 and Gal11 modules are required for transcriptional repression of distinct group of genes. J Biol Chem 276: 37020-37026.
24. Haruki H, Nishikawa J, Laemmli UK. 2008. The anchor-away technique: Rapid, conditional establishment of yeast mutant phenotypes. Mol Cell 31: 925-932.
25. Hickman MJ, Winston F. 2007. Heme levels switch the function of Hap1 of Saccharomyces cerevisiae between transcriptional activator and transcriptional repressor. Mol Cell Biol 27: 7414-7424.
26. Hill DE, Hope IA, Macke JP, Struhl K. 1986. Saturation mutagenesis of the yeast HIS3 regulatory site: Requirements for transcriptional induction and for binding by GCN4 activator protein. Science 234: 451-457.
27. Hirschhorn JN, Brown SA, Clark CD, Winston F. 1992. Evidence that SNF2/SWI2 and SNF5 activate transcription in yeast by altering chromatin structure. Genes Dev 6: 2288-2298.
28. Ho S, Biggar SR, Spencer DM, Schreiber SL, Crabtree GR. 1996. Dimeric ligands define a role for transcriptional activation domains in reinitiation. Nature 382: 822-826.
29. Huang L, Zhang W, Roth SY. 1997. Amino termini of histones H3 and H4 are required for a1-a2 repression in yeast. Mol Cell Biol 17: 6555-6562.
30. Jiang F, Frey BR, Evans ML, Friel JC, Hopper JE. 2009. Gene activation by dissociation of an inhibitor from a transcriptional activation domain. Mol Cell Biol 29: 5604-5610.
31. Katan-Khaykovich Y, Struhl K. 2002. Dynamics of global histone acetylation and deacetylation in vivo: Rapid restoration of normal histone acetylation status upon removal of activators and repressors. Genes Dev 16: 743-752.
32. Keleher CA, Redd MJ, Schultz J, Carlson M, Johnson AD. 1992. Ssn6-Tup1 is a general repressor of transcription in yeast. Cell 68: 709-719.
33. Kim SJ, Swanson MJ, Qiu H, Govind CK, Hinnebusch AG. 2005. Activator Gcn4p and Cyc8p/Tup1p are interdependent for promoter occupancy at ARG1 in vivo. Mol Cell Biol 25: 11171-11183.
34. Kobayashi Y, Inai T, Mizunuma M, Okada I, Shitamukai A, Hirata D, Miyakawa T. 2008. Identification of Tup1 and Cyc8 mutations defective in the responses to osmotic stress. Biochem Biophys Res Commun 368: 50-55.
35. Komachi K, Redd MJ, Johnson AD. 1994. The WD repeats of Tup1 interact with the homeo domain protein a2. Genes Dev 8: 2857-2867.
36. Kuchin S, Carlson M. 1998. Functional relationships of Srb10- Srb11 kinase, carboxy-terminal domain kinase CTDK-1, and transcriptional corepressor Ssn6-Tup1. Mol Cell Biol 18: 1163-1171.
37. Kumar PR, Yu Y, Sternglanz R, Johnston SA, Joshua-Tor L. 2008. NADP regulates the GAL induction system. Science 319: 1090-1092.
38. Kuras L, Struhl K. 1999. Binding of TBP to promoters in vivo is stimulated by activators and requires Pol II holoenzyme. Nature 399: 609-612.
39. Lee M, Chatterjee S, Struhl K. 2000. Genetic analysis of the role of Pol II holoenzyme components in repression by the Cyc8- Tup1 corepressor. Genetics 155: 1535-1542.
40. Li B, Reese JC. 2001. Ssn6-Tup1 regulates RNR3 by positioning nucleosomes and affecting the chromatin structure of the upstream repression sequence. J Biol Chem 276: 33788-33797.
41. Longtine MS, McKenzie A, Demarini DJ, Shah NG, Wach A, Brachat A, Philippsen P, Pringle JR. 1998. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14: 953-961.
42. Malave TM, Dent SY. 2006. Transcriptional repression by Tup1- Ssn6. Biochem Cell Biol 84: 437-443.
43. Matallana E, Franco L, Perez-Ortin JE. 1992. Chromatin structure of the yeast SUC2 promoter in regulatory mutants. Mol Gen Genet 231: 395-400.
44. Mennella TA, Klinkenberg LG, Zitomer RS. 2003. Recruitment of Tup1-Ssn6 by yeast hypoxic genes and chromatin-independent exclusion of TATA binding protein. Eukaryot Cell 2: 1288-1303.
45. Moqtaderi Z, Bai Y, Poon D, Weil PA, Struhl K. 1996. TBPassociated factors are not generally required for transcriptional activation in yeast. Nature 382: 188-191.
46. Morohashi N, Nakajima K, Kurihara D, Mukai Y, Mitchell AP, Shimizu M. 2007. A nucleosome positioned by a2/Mcm1prevents Hap1 activator binding in vivo. Biochem Biophys Res Commun 364: 583-588.
47. Mosammaparast N, Shi Y. 2010. Reversal of histone methylation: Biochemical and molecular mechanisms of histone demethylases. Annu Rev Biochem 79: 155-179.
48. Oliphant AR, Brandl CJ, Struhl K. 1989. Defining sequence specificity of DNA-binding proteins by selecting binding sites from random-sequence oligonucleotides: Analysis of the yeast GCN4 protein. Mol Cell Biol 9: 2944-2949.
49. Papamichos-Chronakis M, Conlan RS, Gounalaki N, Copf T, Tzamarias D. 2000. Hrs1/Med3: A Cyc8-Tup1 corepressor target in the RNA polymerase II holoenzyme. J Biol Chem 275: 8397-8403.
50. Papamichos-Chronakis M, Petrakis T, Ktistaki E, Topalidou I, Tzamarias D. 2002. Cti6, a PHD domain protein, bridges the Cyc8-Tup1 corepressor and the SAGA coactivator to overcome repression at GAL1. Mol Cell 9: 1297-1305.
51. Papamichos-Chronakis M, Gligoris T, Tzamarias D. 2004. The Snf1 kinase controls glucose repression in yeast by modulating interactions between the Mig1 repressor and the Cyc8-Tup1 co-repressor. EMBO Rep 5: 368-372.
52. Proft M, Struhl K. 2002. Hog1 kinase converts the Sko1-Cyc8- Tup1 repressor complex into an activator that recruits SAGA and SWI/SNF in response to osmotic stress. Mol Cell 9: 1307-1317.
53. Redd MJ, Stark MR, Johnson AD. 1996. Accessibility of a2- repressed promoters to the activator Gal4. Mol Cell Biol 16: 2865-2869.
54. Rep M, Proft M, Remize F, Tamas M, Serrano R, Thevelein JM, Hohmann S. 2001. The Saccharomyces cerevisiae Sko1p transcription factor mediates HOG pathway-dependent osmotic regulation of a set of genes encoding enzymes implicated in protection from oxidative damage. Mol Microbiol 40: 1067-1083.
55. Rinn JL, Kertesz M, Wang JK, Squazzo SL, Xu X, Brugmann SA, Goodnough LH, Helms JA, Farnham PJ, Segal E, et al. 2007. Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell 129: 1311-1323.
56. Rizzo JM, Mieczkowski PA, and Buck MJ. 2011. Tup1 stabilizes promoter nucleosome positioning and occupancy at transcriptionally plastic genes. Nucl Acids Res 39: 8803-8819.
57. Robyr D, Suka Y, Xenarios I, Kurdistani SK, Wang A, Suka N, Grunstein M. 2002. Microarray deacetylation maps determine genome-wide functions for yeast histone deacetylases. Cell 109: 437-446.
58. Schwartz YB, Pirrotta V. 2007. Polycomb silencing mechanisms and the management of genomic programmes. Natl Rev 8: 9-22.
59. Simon JA, Kingston RE. 2009. Mechanisms of polycomb gene silencing: Knowns and unknowns. Nat Rev Mol Cell Biol 10: 697-708.
60. Smith RL, Johnson AD. 2000. Turning genes off by Ssn6-Tup1: A conserved system of transcriptional repression in eukaryotes. Trends Biochem Sci 25: 325-330.
61. Struhl K. 1998. Histone acetylation and transcriptional regulatory mechanisms. Genes Dev 12: 599-606.
62. Thoden JB, Ryan LA, Reece RJ, Holden HM. 2008. The interaction between an acidic transcriptional activator and its inhibitor. The molecular basis of the Gal4 recognition by Gal80. J Biol Chem 283: 30266-30272.
63. Tzamarias D, Struhl K. 1994. Functional dissection of the yeast Cyc8-Tup1 transcriptional corepressor complex. Nature 369: 758-761.
64. Tzamarias D, Struhl K. 1995. Distinct TPR motifs of Cyc8 are involved in recruiting the Cyc8-Tup1 co-repressor complex to differentially regulated promoters. Genes Dev 9: 821-831.
65. Varanasi US, Klis M, Mikesell PB, Trumbly RJ. 1996. The Cyc8 (Ssn6)-Tup1 corepressor complex is composed of one Cyc8 and four Tup1 subunits. Mol Cell Biol 16: 6707-6714.
66. Venters BJ, Wachi S, Mavrich TN, Andersen BE, Jena P, Sinnamon AJ, Jain P, Rolleri NS, Jiang C, Hemeryck-Walsh C, et al. 2011. A comprehensive genomic binding map of gene and chromatin regulatory proteins in Saccharomyces. Mol Cell 41: 480-492.
67. Watson AD, Edmondson DG, Bone JR, Mukai Y, Yu Y, Du W, Stillman DJ, Roth SY. 2000. Ssn6-Tup1 interacts with class I histone deacetylases required for repression. Genes Dev 14: 2737-2744.
68. Wu J, Suka N, Carlson M, Grunstein M. 2001. TUP1 utilizes histone H3/H2B-specific HDA1 deacetylase to repress gene activity in yeast. Mol Cell 7: 117-126.
69. Zhang H, Emmons SW. 2002. Caenorhabditis elegans unc-37/ groucho interacts genetically with components of the transcriptional mediator complex. Genetics 160: 799-803.
70. Zhang Z, Reese JC. 2004a. Redundant mechanisms are used by Ssn6-Tup1 in repressing chromosomal gene transcription in Saccharomyces cerevisiae. J Biol Chem 279: 39240-39250.
71. Zhang Z, Reese JC. 2004b. Ssn6-Tup1 requires the ISW2 complex to position nucleosomes in Saccharomyces cerevisiae. EMBO J 23: 2246-2257.
72. Zhang Z, Reese JC. 2005. Molecular genetic analysis of the yeast repressor Rfx1/Crt1 reveals a novel two-step regulatory mechanism. Mol Cell Biol 25: 7399-7411.
73. Zhang Z, Varanasi U, Trumbly RJ. 2002. Functional dissection of the global repressor Tup1 in yeast: Dominant role of the Cterminal repression domain. Genetics 161: 957-969.
74. Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, Nussbaum C, Myers RM, Brown M, Li W, et al. 2008. Model-based analysis of ChIP-seq (MACS). Genome Biol 9: R137. doi:10.1186/gb-2008-9-9-r137.
75. Zhao J, Sun BK, Erwin JA, Song JJ, Lee JT. 2008. Polycomb proteins targeted by a short repeat RNA to the mouse X chromosome. Science 2008: 750-756.