New insights into the SAGA complex from studies of the Tra1 subunit in budding and fission yeast

Transcription

Volumn 3, Issue 1, 2012, Pages 13-18

  Helmlinger, Dominique ^a  

^a Centre National de la Recherche Scientifique   (France)

Author keywords

Signaling; Transcription; Yeast

Indexed keywords

TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SAGA; TRANSCRIPTION FACTOR TRA1; TRANSCRIPTION FACTOR TRRAP; UNCLASSIFIED DRUG;

ARTICLE; CELL BUDDING; CHROMATIN IMMUNOPRECIPITATION; DELETION MUTANT; ELECTRON MICROSCOPY; ENVIRONMENTAL CHANGE; FUNGAL DEVELOPMENT; GENE EXPRESSION PROFILING; GENE INDUCTION; MASS SPECTROMETRY; MUTATIONAL ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; SACCHAROMYCES CEREVISIAE; SCHIZOSACCHAROMYCES POMBE; TRANSCRIPTION REGULATION; YEAST CELL;

SCHIZOSACCHAROMYCETACEAE;

EID: 84857005119     PISSN: 21541264     EISSN: 21541272     Source Type: Journal    
DOI: 10.4161/trns.3.1.19271     Document Type: Article

References (59)

1. Hahn S, Young ET. Transcriptional regulation in Saccharomyces cerevisiae: transcription factor regulation and function, mechanisms of initiation, and roles of activators and coactivators. Genetics 2011; 189:705-36; PMID:22084422; http://dx.doi.org/10.1534/genetics.111.127019.
2. Weake VM, Workman JL. Inducible gene expression: diverse regulatory mechanisms. Nat Rev Genet 2010; 11:426-37; PMID:20421872; http://dx.doi.org/10.1038/nrg2781.
3. Koutelou E, Hirsch CL, Dent SY. Multiple faces of the SAGA complex. Curr Opin Cell Biol 2010; 22:374-82; PMID:20363118; http://dx.doi.org/10.1016/j.ceb.2010.03.005.
4. Rodríguez-Navarro S. Insights into SAGA function during gene expression. EMBO Rep 2009; 10:843-50; PMID:19609321; http://dx.doi.org/10.1038/embor.2009.168.
5. Baker SP, Grant PA. The SAGA continues: expanding the cellular role of a transcriptional co-activator complex. Oncogene 2007; 26:5329-40; PMID:17694076; http://dx.doi.org/10.1038/sj.onc.1210603.
6. Nagy Z, Tora L. Distinct GCN5/PCAF-containing complexes function as co-activators and are involved in transcription factor and global histone acetylation. Oncogene 2007; 26:5341-57; PMID:17694077; http://dx.doi.org/10.1038/sj.onc.1210604.
7. Bhaumik SR, Green MR. Differential requirement of SAGA components for recruitment of TATA-box-binding protein to promoters in vivo. Mol Cell Biol 2002; 22:7365-71; PMID:12370284; http://dx.doi.org/10.1128/MCB.22.21.7365-71.2002.
8. Dudley AM, Rougeulle C, Winston F. The Spt components of SAGA facilitate TBP binding to a promoter at a post-activator-binding step in vivo. Genes Dev 1999; 13:2940-5; PMID:10580001; http://dx.doi.org/10.1101/gad.13.22.2940.
9. Yu Y, Eriksson P, Bhoite LT, Stillman DJ. Regulation of TATA-binding protein binding by the SAGA complex and the Nhp6 high-mobility group protein. Mol Cell Biol 2003; 23:1910-21; PMID:12612066; http://dx.doi.org/10.1128/MCB.23.6.1910-21.2003.
10. Helmlinger D, Marguerat S, Villén J, Gygi SP, Bähler J, Winston F. The S. pombe SAGA complex controls the switch from proliferation to sexual differentiation through the opposing roles of its subunits Gcn5 and Spt8. Genes Dev 2008; 22:3184-95; PMID:19056896; http://dx.doi.org/10.1101/gad.1719908.
11. McMahon SB, Van Buskirk HA, Dugan KA, Copeland TD, Cole MD. The novel ATM-related protein TRRAP is an essential cofactor for the c-Myc and E2F oncoproteins. Cell 1998; 94:363-74; PMID:9708738; http://dx.doi.org/10.1016/S0092-8674(00)81479-8.
12. Knutson BA, Hahn S. Domains of Tra1 important for activator recruitment and transcription coactivator functions of SAGA and NuA4 complexes. Mol Cell Biol 2011; 31:818-31; PMID:21149579; http://dx.doi.org/10.1128/MCB.00687-10.
13. Boudeau J, Miranda-Saavedra D, Barton GJ, Alessi DR. Emerging roles of pseudokinases. Trends Cell Biol 2006; 16:443-52; PMID:16879967; http://dx.doi.org/10.1016/j.tcb.2006.07.003.
14. Saleh A, Schieltz D, Ting N, McMahon SB, Litchfield DW, Yates JR, 3rd, et al. Tra1p is a component of the yeast Ada. Spt transcriptional regulatory complexes. J Biol Chem 1998; 273:26559-65; PMID:9756893; http://dx.doi.org/10.1074/jbc.273.41.26559.
15. Grant PA, Schieltz D, Pray-Grant MG, Yates JR, 3rd, Workman JL. The ATM-related cofactor Tra1 is a component of the purified SAGA complex. Mol Cell 1998; 2:863-7; PMID:9885573; http://dx.doi.org/10.1016/S1097-2765(00)80300-7.
16. Vassilev A, Yamauchi J, Kotani T, Prives C, Avantaggiati ML, Qin J, et al. The 400 kDa subunit of the PCAF histone acetylase complex belongs to the ATM superfamily. Mol Cell 1998; 2:869-75; PMID:9885574; http://dx.doi.org/10.1016/S1097-2765(00)80301-9.
17. Allard S, Utley RT, Savard J, Clarke A, Grant P, Brandl CJ, et al. NuA4, an essential transcription adaptor/histone H4 acetyltransferase complex containing Esa1p and the ATM-related cofactor Tra1p. EMBO J 1999; 18:5108-19; PMID:10487762; http://dx.doi.org/10.1093/emboj/18.18.5108.
18. Chittuluru JR, Chaban Y, Monnet-Saksouk J, Carrozza MJ, Sapountzi V, Selleck W, et al. Structure and nucleosome interaction of the yeast NuA4 and Piccolo-NuA4 histone acetyltransferase complexes. Nat Struct Mol Biol 2011; 18:1196-203; PMID:21984211; http://dx.doi.org/10.1038/nsmb.2128.
19. Herceg Z, Hulla W, Gell D, Cuenin C, Lleonart M, Jackson S, et al. Disruption of Trrap causes early embryonic lethality and defects in cell cycle progression. Nat Genet 2001; 29:206-11; PMID:11544477; http://dx.doi.org/10.1038/ng725.
20. Mutiu AI, Hoke SM, Genereaux J, Hannam C, MacKenzie K, Jobin-Robitaille O, et al. Structure/function analysis of the phosphatidylinositol-3-kinase domain of yeast tra1. Genetics 2007; 177:151-66; PMID:17660562; http://dx.doi.org/10.1534/genetics.107.074476.
21. Hoke SM, Guzzo J, Andrews B, Brandl CJ. Systematic genetic array analysis links the Saccharomyces cerevisiae SAGA/SLIK and NuA4 component Tra1 to multiple cellular processes. BMC Genet 2008; 9:46; PMID:18616809; http://dx.doi.org/10.1186/1471-2156-9-46.
22. Hoke SM, Irina Mutiu A, Genereaux J, Kvas S, Buck M, Yu M, et al. Mutational analysis of the C-terminal FATC domain of Saccharomyces cerevisiae Tra1. Curr Genet 2010; 56:447-65; PMID:20635087; http://dx.doi.org/10.1007/s00294-010-0313-3.
23. Helmlinger D, Marguerat S, Villén J, Swaney DL, Gygi SP, Bähler J, et al. Tra1 has specific regulatory roles, rather than global functions, within the SAGA co-activator complex. EMBO J 2011; 30:2843-52; PMID:21642955; http://dx.doi.org/10.1038/emboj.2011.181.
24. Murr R, Loizou JI, Yang YG, Cuenin C, Li H, Wang ZQ, et al. Histone acetylation by Trrap-Tip60 modulates loading of repair proteins and repair of DNA double-strand breaks. Nat Cell Biol 2006; 8:91-9; PMID:16341205; http://dx.doi.org/10.1038/ncb1343.
25. Robert F, Hardy S, Nagy Z, Baldeyron C, Murr R, Déry U, et al. The transcriptional histone acetyltransferase cofactor TRRAP associates with the MRN repair complex and plays a role in DNA double-strand break repair. Mol Cell Biol 2006; 26:402-12; PMID:16382133; http://dx.doi.org/10.1128/MCB.26.2.402-12.2006.
26. Li H, Cuenin C, Murr R, Wang ZQ, Herceg Z. HAT cofactor Trrap regulates the mitotic checkpoint by modulation of Mad1 and Mad2 expression. EMBO J 2004; 23:4824-34; PMID:15549134; http://dx.doi.org/10.1038/sj.emboj.7600479.
27. Calonge TM, Eshaghi M, Liu J, Ronai Z, O'Connell MJ. Transformation/transcription domain-associated protein (TRRAP)-mediated regulation of Wee1. Genetics 2010; 185:81-93; PMID:20194963; http://dx.doi.org/10.1534/genetics.110.114769.
28. Loizou JI, Oser G, Shukla V, Sawan C, Murr R, Wang ZQ, et al. Histone acetyltransferase cofactor Trrap is essential for maintaining the hematopoietic stem/progenitor cell pool. J Immunol 2009; 183:6422-31; PMID:19880447; http://dx.doi.org/10.4049/jimmunol.0901969.
29. Wurdak H, Zhu S, Romero A, Lorger M, Watson J, Chiang CY, et al. An RNAi screen identifies TRRAP as a regulator of brain tumor-initiating cell differentiation. Cell Stem Cell 2010; 6:37-47; PMID:20085741; http://dx.doi.org/10.1016/j.stem.2009.11.002.
30. Ceol CJ, Horvitz HR. A new class of C. elegans synMuv genes implicates a Tip60/NuA4-like HAT complex as a negative regulator of Ras signaling. Dev Cell 2004; 6:563-76; PMID:15068795; http://dx.doi.org/10.1016/S1534-5807(04)00065-6.
31. Finkbeiner MG, Sawan C, Ouzounova M, Murr R, Herceg Z. HAT cofactor TRRAP mediates beta-catenin ubiquitination on the chromatin and the regulation of the canonical Wnt pathway. Cell Cycle 2008; 7:3908-14; PMID:19066453; http://dx.doi.org/10.4161/cc.7.24.7354.
32. Gause M, Eissenberg JC, Macrae AF, Dorsett M, Misulovin Z, Dorsett D. Nipped-A, the Tra1/TRRAP subunit of the Drosophila SAGA and Tip60 complexes, has multiple roles in Notch signaling during wing development. Mol Cell Biol 2006; 26:2347-59; PMID:16508010; http://dx.doi.org/10.1128/MCB.26.6.2347-59.2006.
33. Murr R, Vaissière T, Sawan C, Shukla V, Herceg Z. Orchestration of chromatin-based processes: mind the TRRAP. Oncogene 2007; 26:5358-72; PMID:17694078; http://dx.doi.org/10.1038/sj.onc.1210605.
34. Wei X, Walia V, Lin JC, Teer JK, Prickett TD, Gartner J, et al. NISC Comparative Sequencing Program. Exome sequencing identifies GRIN2A as frequently mutated in melanoma. Nat Genet 2011; 43:442-6; PMID:21499247; http://dx.doi.org/10.1038/ng.810.
35. Brown CE, Howe L, Sousa K, Alley SC, Carrozza MJ, Tan S, et al. Recruitment of HAT complexes by direct activator interactions with the ATM-related Tra1 subunit. Science 2001; 292:2333-7; PMID:11423663; http://dx.doi.org/10.1126/science.1060214.
36. Bhaumik SR, Raha T, Aiello DP, Green MR. In vivo target of a transcriptional activator revealed by fluorescence resonance energy transfer. Genes Dev 2004; 18:333-43; PMID:14871930; http://dx.doi.org/10.1101/gad.1148404.
37. Fishburn J, Mohibullah N, Hahn S. Function of a eukaryotic transcription activator during the transcription cycle. Mol Cell 2005; 18:369-78; PMID:15866178; http://dx.doi.org/10.1016/j.molcel.2005.03.029.
38. Reeves WM, Hahn S. Targets of the Gal4 transcription activator in functional transcription complexes. Mol Cell Biol 2005; 25:9092-102; PMID:16199885; http://dx.doi.org/10.1128/MCB.25.20.9092-102.2005.
39. Herbig E, Warfield L, Fish L, Fishburn J, Knutson BA, Moorefield B, et al. Mechanism of Mediator recruitment by tandem Gcn4 activation domains and three Gal11 activator-binding domains. Mol Cell Biol 2010; 30:2376-90; PMID:20308326; http://dx.doi.org/10.1128/MCB.01046-09.
40. Memedula S, Belmont AS. Sequential recruitment of HAT and SWI/SNF components to condensed chromatin by VP16. Curr Biol 2003; 13:241-6; PMID:12573221; http://dx.doi.org/10.1016/S0960-9822(03)00048-4.
41. Wu PY, Ruhlmann C, Winston F, Schultz P. Molecular architecture of the S. cerevisiae SAGA complex. Mol Cell 2004; 15:199-208; PMID:15260971; http://dx.doi.org/10.1016/j.molcel.2004.06.005.
42. Köhler A, Zimmerman E, Schneider M, Hurt E, Zheng N. Structural basis for assembly and activation of the heterotetrameric SAGA histone H2B deubiquitinase module. Cell 2010; 141:606-17; PMID:20434206; http://dx.doi.org/10.1016/j.cell.2010.04.026.
43. Samara NL, Datta AB, Berndsen CE, Zhang X, Yao T, Cohen RE, et al. Structural insights into the assembly and function of the SAGA deubiquitinating module. Science 2010; 328:1025-9; PMID:20395473; http://dx.doi.org/10.1126/science.1190049.
44. Bhaumik SR, Green MR. SAGA is an essential in vivo target of the yeast acidic activator Gal4p. Genes Dev 2001; 15:1935-45; PMID:11485988; http://dx.doi.org/10.1101/gad.911401.
45. Jiang X, Sun Y, Chen S, Roy K, Price BD. The FATC domains of PIKK proteins are functionally equivalent and participate in the Tip60-dependent activation of DNA-PKcs and ATM. J Biol Chem 2006; 281:15741-6; PMID:16603769; http://dx.doi.org/10.1074/jbc.M513172200.
46. Hayashi T, Hatanaka M, Nagao K, Nakaseko Y, Kanoh J, Kokubu A, et al. Rapamycin sensitivity of the Schizosaccharomyces pombe tor2 mutant and organization of two highly phosphorylated TOR complexes by specific and common subunits. Genes Cells 2007; 12:1357-70; PMID:18076573; http://dx.doi.org/10.1111/j.1365-2443.2007.01141.x.
47. Shevchenko A, Roguev A, Schaft D, Buchanan L, Habermann B, Sakalar C, et al. Chromatin Central: towards the comparative proteome by accurate mapping of the yeast proteomic environment. Genome Biol 2008; 9:167; PMID:19040720; http://dx.doi.org/10.1186/gb-2008-9-11-r167.
48. Gómez EB, Nugent RL, Laria S, Forsburg SL. Schizosaccharomyces pombe histone acetyltransferase Mst1 (KAT5) is an essential protein required for damage response and chromosome segregation. Genetics 2008; 179:757-71; PMID:18505873; http://dx.doi.org/10.1534/genetics.107.085779.
49. Zhang W, Bone JR, Edmondson DG, Turner BM, Roth SY. Essential and redundant functions of histone acetylation revealed by mutation of target lysines and loss of the Gcn5p acetyltransferase. EMBO J 1998; 17:3155-67; PMID:9606197; http://dx.doi.org/10.1093/emboj/17.11.3155.
50. Clarke AS, Lowell JE, Jacobson SJ, Pillus L. Esa1p is an essential histone acetyltransferase required for cell cycle progression. Mol Cell Biol 1999; 19:2515-26; PMID:10082517.
51. Klein J, Nolden M, Sanders SL, Kirchner J, Weil PA, Melcher K. Use of a genetically introduced cross-linker to identify interaction sites of acidic activators within native transcription factor IID and SAGA. J Biol Chem 2003; 278:6779-86; PMID:12501245; http://dx.doi.org/10.1074/jbc.M212514200.
52. Qiu H, Hu C, Zhang F, Hwang GJ, Swanson MJ, Boonchird C, et al. Interdependent recruitment of SAGA and Srb mediator by transcriptional activator Gcn4p. Mol Cell Biol 2005; 25:3461-74; PMID:15831453; http://dx.doi.org/10.1128/MCB.25.9.3461-74.2005.
53. Hurov KE, Cotta-Ramusino C, Elledge SJ. A genetic screen identifies the Triple T complex required for DNA damage signaling and ATM and ATR stability. Genes Dev 2010; 24:1939-50; PMID:20810650; http://dx.doi.org/10.1101/gad.1934210.
54. Kaizuka T, Hara T, Oshiro N, Kikkawa U, Yonezawa K, Takehana K, et al. Tti1 and Tel2 are critical factors in mammalian target of rapamycin complex assembly. J Biol Chem 2010; 285:20109-16; PMID:20427287; http://dx.doi.org/10.1074/jbc.M110.121699.
55. Takai H, Wang RC, Takai KK, Yang H, de Lange T. Tel2 regulates the stability of PI3K-related protein kinases. Cell 2007; 131:1248-59; PMID:18160036; http://dx.doi.org/10.1016/j.cell.2007.10.052.
56. Takai H, Xie Y, de Lange T, Pavletich NP. Tel2 structure and function in the Hsp90-dependent maturation of mTOR and ATR complexes. Genes Dev 2010; 24:2019-30; PMID:20801936; http://dx.doi.org/10.1101/gad.1956410.
57. Anderson CM, Korkin D, Smith DL, Makovets S, Seidel JJ, Sali A, et al. Tel2 mediates activation and localization of ATM/Tel1 kinase to a double-strand break. Genes Dev 2008; 22:854-9; PMID:18334620; http://dx.doi.org/10.1101/gad.1646208.
58. Horejsí Z, Takai H, Adelman CA, Collis SJ, Flynn H, Maslen S, et al. CK2 phospho-dependent binding of R2TP complex to TEL2 is essential for mTOR and SMG1 stability. Mol Cell 2010; 39:839-50; PMID:20864032; http://dx.doi.org/10.1016/j.molcel.2010.08.037.
59. Lee KK, Sardiu ME, Swanson SK, Gilmore JM, Torok M, Grant PA, et al. Combinatorial depletion analysis to assemble the network architecture of the SAGA and ADA chromatin remodeling complexes. Mol Syst Biol 2011; 7:503; PMID:21734642; http://dx.doi.org/10.1038/msb.2011.40.