Combinatorial depletion analysis to assemble the network architecture of the SAGA and ADA chromatin remodeling complexes

Molecular Systems Biology

Volumn 7, Issue , 2011, Pages

  Lee, Kenneth K ^a   Sardiu, Mihaela E ^a   Swanson, Selene K ^a   Gilmore, Joshua M ^a   Torok, Michael ^b   Grant, Patrick A ^b   Florens, Laurence ^a   Workman, Jerry L ^a   Washburn, Michael P ^a,c  

^a STOWERS INSTITUTE FOR MEDICAL RESEARCH   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

^c UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

Author keywords

ADA; architecture; protein interaction network; quantitative proteomics; SAGA

Indexed keywords

ADA PROTEIN; AHC2 PROTEIN; FUNGAL PROTEIN; HISTONE ACETYLTRANSFERASE; MULTIPROTEIN COMPLEX; PROTEIN SUBUNIT; SGF29 PROTEIN; UNCLASSIFIED DRUG; ADA2 PROTEIN, S CEREVISIAE; NGG1 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN; SAGA COMPLEX, S CEREVISIAE; SGF29 PROTEIN, S CEREVISIAE; TRANSACTIVATOR PROTEIN; TRANSCRIPTION FACTOR;

ARTICLE; BIOCHEMISTRY; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; COMPLEX FORMATION; MUTANT; NONHUMAN; NUCLEOSOME; ORGANIZATION; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FAMILY; PROTEIN INTERACTION; PROTEOMICS; QUANTITATIVE ANALYSIS; WILD TYPE; BIOLOGICAL MODEL; BIOLOGY; ENZYMOLOGY; GENE DELETION; GENETIC DATABASE; GENETICS; METABOLISM; METHODOLOGY; PLASMID; SACCHAROMYCES CEREVISIAE;

CHROMATIN ASSEMBLY AND DISASSEMBLY; COMPUTATIONAL BIOLOGY; DATABASES, GENETIC; GENE DELETION; HISTONE ACETYLTRANSFERASES; MODELS, GENETIC; PHENOTYPE; PLASMIDS; PROTEOMICS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS;

EID: 79960080101     PISSN: None     EISSN: 17444292     Source Type: Journal    
DOI: 10.1038/msb.2011.40     Document Type: Article

References (55)

1. Auty R, Steen H, Myers LC, Persinger J, Bartholomew B, Gygi SP, Buratowski S (2004) Purification of active TFIID from Saccharomyces cerevisiae. Extensive promoter contacts and coactivator function. J Biol Chem 279: 49973-49981 (Pubitemid 39577806)
2. Balasubramanian R, Pray-Grant MG, Selleck W, Grant PA, Tan S (2002) Role of the Ada2 and Ada3 transcriptional coactivators in histone acetylation. J Biol Chem 277: 7989-7995 (Pubitemid 34968250)
3. Benecke A, Gaudon C, Garnier JM, vom Baur E, Chambon P, Losson R (2002) ADA3-containing complexes associate with estrogen receptor alpha. Nucleic Acids Res 30: 2508-2514 (Pubitemid 34619004)
4. Berger SL, Pina B, Silverman N, Marcus GA, Agapite J, Reigier JL, Triezenberg SJ, Guarente L (1992) Genetic isolation of ADA2: a potential transcriptional adaptor required for function of certain acidic activation domains. Cell 70: 251-265
5. Berndsen CE, Selleck W, McBryant SJ, Hansen JC, Tan S, Denu JM (2007) Nucleosome recognition by the piccolo NuA4 histone acetyltransferase complex. Biochemistry 46: 2091-2099 (Pubitemid 46355320)
6. Collins SR, Miller KM, Maas NL, Roguev A, Fillingham J, Chu CS, Schuldiner M, Gebbia M, Recht J, Shales M, Ding H, Xu H, Han J, Ingvarsdottir K, Cheng B, Andrews B, Boone C, Berger SL, Hieter P, Zhang Z et al (2007) Functional dissection of protein complexes involved in yeast chromosome biology using a genetic interaction map. Nature 446: 806-810 (Pubitemid 46582025)
7. Costanzo M, Baryshnikova A, Bellay J, Kim Y, Spear ED, Sevier CS, Ding H, Koh JL, Toufighi K, Mostafavi S, Prinz J, St Onge RP, VanderSluis B, Makhnevych T, Vizeacoumar FJ, Alizadeh S, Bahr S, Brost RL, Chen Y, Cokol M et al (2010) The genetic landscape of a cell. Science 327: 425-431
8. Daniel JA, Torok MS, Sun ZW, Schieltz D, Allis CD, Yates III JR, Grant PA (2004) Deubiquitination of histone H2B by a yeast acetyltransferase complex regulates transcription. J Biol Chem 279: 1867-1871 (Pubitemid 38084455)
9. Eberharter A, John S, Grant PA, Utley RT, Workman JL (1998) Identification and analysis of yeast nucleosomal histone acetyltransferase complexes. Methods (San Diego, Calif) 15: 315-321
10. Eberharter A, Sterner DE, Schieltz D, Hassan A, Yates III JR, Berger SL, Workman JL (1999) The ADA complex is a distinct histone acetyltransferase complex in saccharomyces cerevisiae. Mol Cell Biol 19: 6621-6631 (Pubitemid 29441846)
11. Eng JK, McCormack AL, Yates III JR (1994) An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database. J Am Soc Mass Spectrom 5: 976-989
12. Florens L, Washburn MP (2006) Proteomic analysis by multidimensional protein identification technology. Methods Mol Biol 328: 159-175
13. Grant PA, Duggan L, Cote J, Roberts SM, Brownell JE, Candau R, Ohba R, Owen-Hughes T, Allis CD, Winston F, Berger SL, Workman JL (1997) Yeast Gcn5 functions in two multisubunit complexes to acetylate nucleosomal histones: characterization of an Ada complex and the SAGA (Spt/Ada) complex. Genes Dev 11: 1640-1650 (Pubitemid 27300590)
14. Grant PA, Eberharter A, John S, Cook RG, Turner BM, Workman JL (1999) Expanded lysine acetylation specificity of Gcn5 in native complexes. J Biol Chem 274: 5895-5900 (Pubitemid 29109247)
15. Grant PA, Schieltz D, Pray-Grant MG, Steger DJ, Reese JC, Yates III JR, Workman JL (1998) A subset of TAF(II)s are integral components of the SAGA complex required for nucleosome acetylation and transcriptional stimulation. Cell 94: 45-53 (Pubitemid 28347468)
16. Henry KW, Wyce A, Lo WS, Duggan LJ, Emre NC, Kao CF, Pillus L, Shilatifard A, Osley MA, Berger SL (2003) Transcriptional activation via sequential histone H2B ubiquitylation and deubiquitylation, mediated by SAGA-associated Ubp8. Genes Dev 17: 2648-2663 (Pubitemid 37363070)
17. Horiuchi J, Silverman N, Pina B, Marcus GA, Guarente L (1997) ADA1, a novel component of the ADA/GCN5 complex, has broader effects than GCN5, ADA2, or ADA3. Mol Cell Biol 17: 3220-3228 (Pubitemid 27215037)
18. Ingvarsdottir K, Krogan NJ, Emre NC,Wyce A, Thompson NJ, Emili A, Hughes TR, Greenblatt JF, Berger SL (2005) H2B ubiquitin protease Ubp8 and Sgf11 constitute a discrete functional module within the Saccharomyces cerevisiae SAGA complex. Mol Cell Biol 25: 1162-1172 (Pubitemid 40165821)
19. Ito T, Chiba T, Ozawa R, Yoshida M, Hattori M, Sakaki Y (2001) A comprehensive two-hybrid analysis to explore the yeast protein interactome. Proc Natl Acad Sci USA 98: 4569-4574 (Pubitemid 32295017)
20. Kohler A, Pascual-Garcia P, Llopis A, Zapater M, Posas F, Hurt E, Rodriguez-Navarro S (2006) The mRNA export factor Sus1 is involved in Spt/Ada/Gcn5 acetyltransferase-mediated H2B deubiquitinylation through its interaction with Ubp8 and Sgf11. Mol Biol Cell 17: 4228-4236 (Pubitemid 44522044)
21. Kohler A, Schneider M, Cabal GG, Nehrbass U, Hurt E (2008) Yeast Ataxin-7 links histone deubiquitination with gene gating and mRNA export. Nat Cell Biol 10: 707-715 (Pubitemid 351772936)
22. Kohler A, Zimmerman E, Schneider M, Hurt E, Zheng N (2010) Structural basis for assembly and activation of the heterotetrameric SAGA histone H2B deubiquitinase module. Cell 141: 606-617
23. Koutelou E, Hirsch CL, Dent SY (2010) Multiple faces of the SAGA complex. Curr Opin Cell Biol 22: 374-382
24. Krogan NJ, Cagney G, Yu H, Zhong G, Guo X, Ignatchenko A, Li J, Pu S, Datta N, Tikuisis AP, Punna T, Peregrin-Alvarez JM, Shales M, Zhang X, Davey M, Robinson MD, Paccanaro A, Bray JE, Sheung A, Beattie B et al (2006) Global landscape of protein complexes in the yeast Saccharomyces cerevisiae. Nature 440: 637-643
25. Kurabe N, Katagiri K, Komiya Y, Ito R, Sugiyama A, Kawasaki Y, Tashiro F (2007) Deregulated expression of a novel component of TFTC/STAGA histone acetyltransferase complexes, rat SGF29, in hepatocellular carcinoma: possible implication for the oncogenic potential of c-Myc. Oncogene 26: 5626-5634 (Pubitemid 47267841)
26. Layer JH, Miller SG,Weil PA (2010) Direct transactivator-transcription factor IID (TFIID) contacts drive yeast ribosomal protein gene transcription. J Biol Chem 285: 15489-15499
27. Lee KK, Florens L, Swanson SK, Washburn MP, Workman JL (2005) The deubiquitylation activity of Ubp8 is dependent upon Sgf11 and its association with the SAGA complex. Mol Cell Biol 25: 1173-1182 (Pubitemid 40165822)
28. Lee KK, Swanson SK, Florens L, Washburn MP, Workman JL (2009) Yeast Sgf73/Ataxin-7 serves to anchor the deubiquitination module into both SAGA and Slik(SALSA) HAT complexes. Epigenetics Chromatin 2: 2
29. Lee KK,Workman JL (2007) Histone acetyltransferase complexes: one size doesnt fit all. Nat Rev 8: 284-295 (Pubitemid 46474661)
30. Lin YY, Qi Y, Lu JY, Pan X, Yuan DS, Zhao Y, Bader JS, Boeke JD (2008) A comprehensive synthetic genetic interaction network governing yeast histone acetylation and deacetylation. Genes Dev 22: 2062-2074
31. Marcus GA, Silverman N, Berger SL, Horiuchi J, Guarente L (1994) Functional similarity and physical association between GCN5 and ADA2: putative transcriptional adaptors. EMBO J 13: 4807-4815 (Pubitemid 24319362)
32. McDonald WH, Ohi R, Miyamoto DT, Mitchison TJ, Yates III JR (2002) Comparison of three directly coupled HPLC MS/MS strategies for identification of proeins from complex mixtures: single-dimension LC-MS/MS, 2-phase MudPIT, and 3-phase MudPIT. Int J Mass Spectrom 219: 245-251
33. McMahon SJ, Pray-Grant MG, Schieltz D, Yates III JR, Grant PA (2005) Polyglutamine-expanded spinocerebellar ataxia-7 protein disrupts normal SAGA and SLIK histone acetyltransferase activity. Proc Natl Acad Sci USA 102: 8478-8482 (Pubitemid 40862761)
34. Mitchell L, Lambert JP, Gerdes M, Al-Madhoun AS, Skerjanc IS, Figeys D, Baetz K (2008) Functional dissection of the NuA4 histone acetyltransferase reveals its role as a genetic hub and that Eaf1 is essential for complex integrity. Mol Cell Biol 28: 2244-2256 (Pubitemid 351429971)
35. Pray-Grant MG, Daniel JA, Schieltz D, Yates III JR, Grant PA (2005) Chd1 chromodomain links histone H3 methylation with SAGA- and SLIK-dependent acetylation. Nature 433: 434-438 (Pubitemid 40203325)
36. Pray-Grant MG, Schieltz D, McMahon SJ,Wood JM, Kennedy EL, Cook RG, Workman JL, Yates III JR, Grant PA (2002) The novel SLIK histone acetyltransferase complex functions in the yeast retrograde response pathway. Mol Cell Biol 22: 8774-8786 (Pubitemid 35397190)
37. Roberts SM, Winston F (1997) Essential functional interactions of SAGA, a Saccharomyces cerevisiae complex of Spt, Ada, and Gcn5 proteins, with the Snf/Swi and Srb/mediator complexes. Genetics 147: 451-465 (Pubitemid 27418558)
38. Saleh A, Lang V, Cook R, Brandl CJ (1997) Identification of native complexes containing the yeast coactivator/repressor proteins NGG1/ADA3 and ADA2. J Biol Chem 272: 5571-5578 (Pubitemid 27102381)
39. Samara NL, Datta AB, Berndsen CE, Zhang X, Yao T, Cohen RE, Wolberger C (2010) Structural insights into the assembly and function of the SAGA deubiquitinating module. Science 328: 1025-1029
40. Sardiu ME, Cai Y, Jin J, Swanson SK, Conaway RC, Conaway JW, Florens L, Washburn MP (2008) Probabilistic assembly of human protein interaction networks from label-free quantitative proteomics. Proc Natl Acad Sci USA 105: 1454-1459 (Pubitemid 351346535)
41. Sardiu ME, Florens L, Washburn MP (2009a) Evaluation of clustering algorithms for protein complex and protein interaction network assembly. J Proteome Res 8: 2944-2952
42. Sardiu ME, Gilmore JM, Carrozza MJ, Li B, Workman JL, Florens L, Washburn MP (2009b) Determining protein complex connectivity using a probabilistic deletion network derived from quantitative proteomics. PloS One 4: e7310
43. Selleck W, Fortin I, Sermwittayawong D, Cote J, Tan S (2005) The Saccharomyces cerevisiae Piccolo NuA4 histone acetyltransferase complex requires the enhancer of polycomb A domain and chromodomain to acetylate nucleosomes. Mol Cell Biol 25: 5535-5542 (Pubitemid 40853588)
44. Sterner DE, Belotserkovskaya R, Berger SL (2002) SALSA, a variant of yeast SAGA, contains truncated Spt7, which correlates with activated transcription. Proc Natl Acad Sci USA 99: 11622-11627 (Pubitemid 34994449)
45. Sterner DE, Grant PA, Roberts SM, Duggan LJ, Belotserkovskaya R, Pacella LA, Winston F, Workman JL, Berger SL (1999) Functional organization of the yeast SAGA complex: distinct components involved in structural integrity, nucleosome acetylation, and TATAbinding protein interaction. Mol Cell Biol 19: 86-98 (Pubitemid 29018412)
46. Swanson SK, Florens L,Washburn MP (2009) Generation and analysis of multidimensional protein identification technology datasets. Methods Mol Biol 492: 1-20
47. Tabb DL, McDonald WH, Yates III JR (2002) DTASelect and contrast: tools for assembling and comparing protein identifications from shotgun proteomics. J Proteome Res 1: 21-26
48. Uetz P, Giot L, Cagney G, Mansfield TA, Judson RS, Knight JR, Lockshon D, Narayan V, Srinivasan M, Pochart P, Qureshi-Emili A, Li Y, Godwin B, Conover D, Kalbfleisch T, Vijayadamodar G, Yang M, Johnston M, Fields S, Rothberg JM (2000) A comprehensive analysis of protein-protein interactions in Saccharomyces cerevisiae. Nature 403: 623-627 (Pubitemid 30103994)
49. Wang L, Liu L, Berger SL (1998) Critical residues for histone acetylation by Gcn5, functioning in Ada and SAGA complexes, are also required for transcriptional function in vivo. Genes Dev 12: 640-653 (Pubitemid 28134297)
50. Wang L, Mizzen C, Ying C, Candau R, Barlev N, Brownell J, Allis CD, Berger SL (1997) Histone acetyltransferase activity is conserved between yeast and human GCN5 and is required for complementation of growth and transcriptional activation. Mol Cell Biol 17: 519-527 (Pubitemid 26425641)
51. Wu PY, Ruhlmann C, Winston F, Schultz P (2004) Molecular architecture of the S. cerevisiae SAGA complex. Mol Cell 15: 199-208 (Pubitemid 38950967)
52. Yatherajam G, Zhang L, Kraemer SM, Stargell LA (2003) Protein-protein interaction map for yeast TFIID. Nucleic Acids Res 31: 1252-1260 (Pubitemid 36284967)
53. Yu H, Braun P, Yildirim MA, Lemmens I, Venkatesan K, Sahalie J, Hirozane-Kishikawa T, Gebreab F, Li N, Simonis N, Hao T, Rual JF, Dricot A, Vazquez A, Murray RR, Simon C, Tardivo L, Tam S, Svrzikapa N, Fan C et al (2008) High-quality binary protein interaction map of the yeast interactome network. Science 322: 104-110
54. Zhang Y, Wen Z, Washburn MP, Florens L (2010) Refinements to label free proteome quantitation: how to deal with peptides shared by multiple proteins. Anal Chem 82: 2272-2281
55. Zybailov B, Mosley AL, Sardiu ME, Coleman MK, Florens L,Washburn MP (2006) Statistical analysis of membrane proteome expression changes in Saccharomyces cerevisiae. J Proteome Res 5: 2339-2347 (Pubitemid 44330827)