Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review
  • Published:

The SAGA continues: expanding the cellular role of a transcriptional co-activator complex

Oncogene volume 26, pages 5329–5340 (2007)Cite this article

Abstract

Throughout the last decade, great advances have been made in our understanding of how DNA-templated cellular processes occur in the native chromatin environment. Proteins that regulate transcription, replication, DNA repair, mitosis and other processes must be targeted to specific regions of the genome and granted access to DNA, which is normally tightly packaged in the higher-order chromatin structure of eukaryotic nuclei. Massive multiprotein complexes have been discovered, which facilitate access to DNA and recruitment of downstream effectors through three distinct mechanisms: chemical modification of histone amino-acid residues, ATP-dependent chromatin remodeling and histone exchange. The yeast Spt-Ada-Gcn5-Acetyl transferase (SAGA) transcriptional co-activator complex regulates numerous cellular processes through coordination of multiple histone post-translational modifications. SAGA is known to generate and interact with a number of histone modifications, including acetylation, methylation, ubiquitylation and phosphorylation. Although best characterized for its role in regulating transcriptional activation, SAGA is also required for optimal transcription elongation, mRNA export and perhaps nucleotide excision repair. Here, we discuss findings from recent years that have elucidated the function of this 1.8-MDa complex in multiple cellular processes, and how misregulation of the homologous complexes in humans may ultimately play a role in development of disease.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1

Similar content being viewed by others

References

  • Altaf M, Saksouk N, Côté J . (2007). Histone modifications in response to DNA damage. Mutat Res 618: 81–90.

    CAS  PubMed  Google Scholar 

  • Baker SP, Grant PA . (2005). The proteasome: not just degrading anymore. Cell 4: 361–363.

    Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • Belotserkovskaya R, Sterner DE, Deng M, Sayre MH, Lieberman PM, Berger SL . (2000). Inhibition of TATA-binding protein function by SAGA subunits Spt3 and Spt8 at Gcn4-activated promoters. Mol Cell Biol 20: 634–647.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Berger SL, Pina B, Silverman N, Marcus GA, Agapite J, Regier JL et al. (1992). Genetic isolation of ADA2: a potential transcriptional adaptor required for function of certain acidic activation domains. Cell 70: 251–265.

    CAS  PubMed  Google Scholar 

  • Bhaumik SR, Raha T, Aiello DP, Green MR . (2004). In vivo target of a transcriptional activator revealed by fluorescence resonance energy transfer. Genes Dev 18: 333–343.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Brand M, Moggs JG, Oulad-Abdelghani M, Lejeune F, Dilworth FJ, Stevenin J et al. (2001). UV-damaged DNA-binding protein in the TFTC complex links DNA damage recognition to nucleosome acetylation. EMBO J 20: 3187–3196.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Briggs SD, Xiao T, Sun ZW, Caldwell JA, Shabanowitz J, Hunt DF et al. (2002). Gene silencing: trans-histone regulatory pathway in chromatin. Nature 418: 498.

    CAS  PubMed  Google Scholar 

  • Brown CE, Howe L, Sousa K, Alley SC, Carrozza MJ, Tan S et al. (2001). Recruitment of HAT complexes by direct activator interactions with the ATM-related Tra1 subunit. Science 292: 2333–2337.

    CAS  PubMed  Google Scholar 

  • Brownell JE, Allis CD . (1995). An activity gel assay detects a single, catalytically active histone acetyltransferase subunit in Tetrahymena macronuclei. Proc Natl Acad Sci USA 92: 6364–6368.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Brownell JE, Zhou J, Ranalli T, Kobayashi R, Edmondson DG, Roth SY et al. (1996). Tetrahymena histone acetyltransferase A: a homolog to yeast Gcn5p linking histone acetylation to gene activation. Cell 84: 843–851.

    CAS  PubMed  Google Scholar 

  • Bu P, Evrard YA, Lozano G, Dent SY . (2007). Loss of gcn5 acetyltransferase activity leads to neural tube closure defects and exencephaly in mouse embryos. Mol Cell Biol 27: 3405–3416.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Burley SK, Roeder RG . (1996). Biochemistry and structural biology of transcription factor IID (TFIID). Annu Rev Biochem 65: 769–799.

    CAS  PubMed  Google Scholar 

  • Butow RA, Avadhani NG . (2004). Mitochondrial signaling: the retrograde response. Mol Cell 14: 1–15.

    CAS  PubMed  Google Scholar 

  • Cabal GG, Genovesio A, Rodriguez-Navarro S, Zimmer C, Gadal O, Lesne A et al. (2006). SAGA interacting factors confine sub-diffusion of transcribed genes to the nuclear envelope. Nature 441: 770–773.

    CAS  PubMed  Google Scholar 

  • Cheung P, Tanner KG, Cheung WL, Sassone-Corsi P, Denu JM, Allis CD . (2000). Synergistic coupling of histone H3 phosphorylation and acetylation in response to epidermal growth factor stimulation. Mol Cell 5: 905–915.

    CAS  PubMed  Google Scholar 

  • Cleaver JE . (2000). Common pathways for ultraviolet skin carcinogenesis in the repair and replication defective groups of xeroderma pigmentosum. J Dermatol Sci 23: 1–11.

    CAS  PubMed  Google Scholar 

  • Clements A, Poux AN, Lo WS, Pillus L, Berger SL, Marmorstein R . (2003). Structural basis for histone and phosphohistone binding by the GCN5 histone acetyltransferase. Mol Cell 12: 461–473.

    CAS  PubMed  Google Scholar 

  • Daniel JA, Pray-Grant MG, Grant PA . (2005). Effector proteins for methylated histones: an expanding family. Cell Cycle 4: 919–926.

    CAS  PubMed  Google Scholar 

  • Daniel JA, Torok MS, Sun ZW, Schieltz D, Allis CD, Yates III JR et al. (2004). Deubiquitination of histone H2B by a yeast acetyltransferase complex regulates transcription. J Biol Chem 279: 1867–1871.

    CAS  PubMed  Google Scholar 

  • David G, Durr A, Stevanin G, Cancel G, Abbas N, Benomar A et al. (1998). Molecular and clinical correlations in autosomal dominant cerebellar ataxia with progressive macular dystrophy (SCA7). Hum Mol Genet 7: 165–170.

    CAS  PubMed  Google Scholar 

  • Dover J, Schneider J, Tawiah-Boateng MA, Wood A, Dean K, Johnston M et al. (2002). Methylation of histone H3 by COMPASS requires ubiquitination of histone H2B by Rad6. J Biol Chem 277: 28368–28371.

    CAS  PubMed  Google Scholar 

  • Dudley AM, Rougeulle C, Winston F . (1999). The Spt components of SAGA facilitate TBP binding to a promoter at a post-activator-binding step in vivo. Genes Dev 13: 2940–2945.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Eisenmann DM, Chapon C, Roberts SM, Dollard C, Winston F . (1994). The Saccharomyces cerevisiae SPT8 gene encodes a very acidic protein that is functionally related to SPT3 and TATA-binding protein. Genetics 137: 647–657.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Eisenmann DM, Dollard C, Winston F . (1989). SPT15, the gene encoding the yeast TATA binding factor TFIID, is required for normal transcription initiation in vivo. Cell 58: 1183–1191.

    CAS  PubMed  Google Scholar 

  • Ezhkova E, Tansey WP . (2004). Proteasomal ATPases link ubiquitylation of histone H2B to methylation of histone H3. Mol Cell 13: 435–442.

    CAS  PubMed  Google Scholar 

  • Ferdous A, Gonzalez F, Sun L, Kodadek T, Johnston SA . (2001). The 19S regulatory particle of the proteasome is required for efficient transcription elongation by RNA polymerase II. Mol Cell 7: 981–991.

    CAS  PubMed  Google Scholar 

  • Ferreiro JA, Powell NG, Karabetsou N, Mellor J, Waters R . (2006). Roles for Gcn5p and Ada2p in transcription and nucleotide excision repair at the Saccharomyces cerevisiae MET16 gene. Nucleic Acids Res 34: 976–985.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fischer T, Sträßer K, Racz A, Rodriguez-Navarro S, Oppizzi M, Ihrig P et al. (2002). The mRNA export machinery requires the novel Sac3p–Thp1p complex to dock at the nucleoplasmic entrance of the nuclear pores. EMBO J 21: 5843–5852.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Flanagan JF, Mi LZ, Chruszcz M, Cymborowski M, Clines KL, Kim Y et al. (2005). Double chromodomains cooperate to recognize the methylated histone H3 tail. Nature 438: 1181–1185.

    CAS  PubMed  Google Scholar 

  • Gansheroff LJ, Dollard C, Tan P, Winston F . (1995). The Saccharomyces cerevisiae SPT7 gene encodes a very acidic protein important for transcription in vivo. Genetics 139: 523–536.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gavin AC, Bosche M, Krause R, Grandi P, Marzioch M, Bauer A et al. (2002). Functional organization of the yeast proteome by systematic analysis of protein complexes. Nature 425: 141–147.

    Google Scholar 

  • Gillette TG, Gonzalez F, Delahodde A, Johnston SA, Kodadek T . (2004). Physical and functional association of RNA polymerase II and the proteasome. Proc Natl Acad Sci USA 101: 5904–5909.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Govind CK, Zhang F, Qiu H, Hofmeyer K, Hinnebusch AG . (2007). Gcn5 promotes acetylation, eviction, and methylation of nucleosomes in transcribed coding regions. Mol Cell 25: 31–42.

    CAS  PubMed  Google Scholar 

  • Grant PA, Duggan L, Côté J, Roberts SM, Brownell JE, Candau R et al. (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.

    CAS  PubMed  Google Scholar 

  • Grant PA, Schieltz D, Pray-Grant MG, Steger DJ, Reese JC, Yates III JR et al. (1998a). A subset of TAFIIs are integral components of the SAGA complex required for nucleosome acetylation and transcriptional stimulation. Cell 94: 45–53.

    CAS  PubMed  Google Scholar 

  • Grant PA, Schieltz D, Pray-Grant MG, Yates III JR, Workman JL . (1998b). The ATM-related cofactor Tra1 is a component of the purified SAGA complex. Mol Cell 2: 863–867.

    CAS  PubMed  Google Scholar 

  • Green MR . (2000). TBP-associated factors (TAFIIs): multiple, selective transcriptional mediators in common complexes. Trends Biochem Sci 25: 59–63.

    CAS  PubMed  Google Scholar 

  • Hassan AH, Prochasson P, Neely KE, Galasinki SC, Chandy M, Carrozza MJ et al. (2002). Function and selectivity of bromodomains in anchoring chromatin-modifying complexes to promoter nucleosomes. Cell 111: 369–379.

    CAS  PubMed  Google Scholar 

  • Helmlinger D, Hardy S, Sasorith S, Klein F, Robert F, Weber C et al. (2004). Ataxin-7 is a subunit of GCN5 histone acetyltransferase-containing complexes. Hum Mol Genet 13: 1257–1265.

    CAS  PubMed  Google Scholar 

  • Henry KW, Wyce A, Lo WS, Duggan LJ, Emre NC, Kao CF et al. (2003). Transcriptional activation via sequential histone H2B ubiquitylation and deubiquitylation, mediated by SAGA-associated Ubp8. Genes Dev 17: 2648–2663.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Huisinga KL, Pugh BF . (2004). A genome-wide housekeeping role for TFIID and a highly regulated stress-related role for SAGA in Saccharomyces cerevisiae. Mol Cell 13: 573–585.

    CAS  PubMed  Google Scholar 

  • Hwang WW, Venkatasubrahmanyam S, Ianculescu AG, Tong A, Boone C, Madhani HD . (2003). A conserved RING finger protein required for histone H2B monoubiquitination and cell size control. Mol Cell 11: 261–266.

    CAS  PubMed  Google Scholar 

  • Ikeda K, Steger DJ, Eberharter A, Workman JL . (1999). Activation domain-specific and general transcription stimulation by native histone acetyltransferase complexes. Mol Cell Biol 19: 855–863.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ingvarsdottir K, Krogan NJ, Emre NC, Wyce A, Thompson NJ, Emili A et al. (2005). H2B ubiquitin protease Ubp8 and Sgf11 constitute a discrete functional module within the Saccharomyces cerevisiae SAGA complex. Mol Cell Biol 25: 1162–1172.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jia Y, Rothermel B, Thornton J, Butow RA . (1997). A basic helix–loop–helix–leucine zipper transcription complex in yeast functions in a signaling pathway from mitochondria to the nucleus. Mol Cell Biol 17: 1110–1117.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kinyamu HK, Chen J, Archer TK . (2005). Linking the ubiquitin–proteasome pathway to chromatin remodeling/modification by nuclear receptors. J Mol Endocrinol 34: 281–297.

    CAS  PubMed  Google Scholar 

  • Kohler A, Pascual-Garcia P, Llopis A, Zapater M, Posas F, Hurt E et al. (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.

    PubMed  PubMed Central  Google Scholar 

  • Kulesza CA, Van Buskirk HA, Cole MD, Reese JC, Smith MM, Engel DA . (2002). Adenovirus E1A requires the yeast SAGA histone acetyltransferase complex and associates with SAGA components Gcn5 and Tra1. Oncogene 21: 1411–1422.

    CAS  PubMed  Google Scholar 

  • Larschan E, Winston F . (2001). The S. cerevisiae SAGA complex functions in vivo as a coactivator for transcriptional activation by Gal4. Genes Dev 15: 1946–1956.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lee D, Ezhkova E, Li B, Pattenden SG, Tansey WP, Workman JL . (2005a). The proteasome regulatory particle alters the SAGA coactivator to enhance its interactions with transcriptional activators. Cell 123: 423–436.

    CAS  PubMed  Google Scholar 

  • Lee KK, Florens L, Swanson SK, Washburn MP, Workman JL . (2005b). The deubiquitylation activity of Ubp8 is dependent upon Sgf11 and its association with the SAGA complex. Mol Cell Biol 25: 1173–1182.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liu X, Tesfai J, Evrard YA, Dent SY, Martinez E . (2003). c-Myc transformation domain recruits the human STAGA complex and requires TRRAP and GCN5 acetylase activity for transcription activation. J Biol Chem 278: 20405–20412.

    CAS  PubMed  Google Scholar 

  • Lo WS, Duggan L, Emre NC, Belotserkovskya R, Lane WS, Shiekhattar R et al. (2001). Snf1 – a histone kinase that works in concert with the histone acetyltransferase Gcn5 to regulate transcription. Science 293: 1142–1146.

    CAS  PubMed  Google Scholar 

  • Lo WS, Gamache ER, Henry KW, Yang D, Pillus L, Berger SL . (2005). Histone H3 phosphorylation can promote TBP recruitment through distinct promoter-specific mechanisms. EMBO J 24: 997–1008.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lo WS, Trievel RC, Rojas JR, Duggan L, Hsu JY, Allis CD et al. (2000). Phosphorylation of serine 10 in histone H3 is functionally linked in vitro and in vivo to Gcn5-mediated acetylation at lysine 14. Mol Cell 5: 917–926.

    CAS  PubMed  Google Scholar 

  • Macdonald N, Welburn JP, Noble ME, Nguyen A, Yaffe MB, Clynes D et al. (2005). Molecular basis for the recognition of phosphorylated and phosphoacetylated histone H3 by 14-3-3. Mol Cell 20: 199–211.

    CAS  PubMed  Google Scholar 

  • Marcus GA, Horiuchi J, Silverman N, Guarente L . (1996). ADA5/SPT20 links the ADA and SPT genes, which are involved in yeast transcription. Mol Cell Biol 16: 3197–3205.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Martinez E, Palhan VB, Tjernberg A, Lymar ES, Gamper AM, Kundu TK et al. (2001). Human STAGA complex is a chromatin-acetylating transcription coactivator that interacts with pre-mRNA splicing and DNA damage-binding factors in vivo. Mol Cell Biol 21: 6782–6795.

    CAS  PubMed  PubMed Central  Google Scholar 

  • McMahon SB, Van Buskirk HA, Dugan KA, Copeland TD, Cole MD . (1998). The novel ATM-related protein TRRAP is an essential cofactor for the c-Myc and E2F oncoproteins. Cell 94: 363–374.

    CAS  PubMed  Google Scholar 

  • McMahon SB, Wood MA, Cole MD . (2000). The essential cofactor TRRAP recruits the histone acetyltransferase hGCN5 to c-Myc. Mol Cell Biol 20: 556–562.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mitra D, Parnell EJ, Landon JW, Yu Y, Stillman DJ . (2006). SWI/SNF binding to the HO promoter requires histone acetylation and stimulates TATA-binding protein recruitment. Mol Cell Biol 26: 4095–4110.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Muratani M, Tansey WP . (2003). How the ubiquitin–proteasome system controls transcription. Nat Rev Mol Cell Biol 4: 192–201.

    CAS  PubMed  Google Scholar 

  • Murr R, Vaissière T, Sawan C, Shukla V, Herceg Z . (2007). Orchestration of chromatin-based processes: mind the TRRAP. Oncogene 26: 5358–5372.

    CAS  PubMed  Google Scholar 

  • Nagy Z, Tora L . (2007). Distinct GCN5/PCAF-containing complexes function as coactivators and are involved in transcription factor and global histone acetylation. Oncogene 26: 5341–5357.

    CAS  PubMed  Google Scholar 

  • Okuda M, Horikoshi M, Nishimura Y . (2007). Structural polymorphism of chromodomains in Chd1. J Mol Biol 365: 1047–1062.

    CAS  PubMed  Google Scholar 

  • Palhan VB, Chen S, Peng GH, Tjernberg A, Gamper AM, Fan Y et al. (2005). Polyglutamine-expanded ataxin-7 inhibits STAGA histone acetyltransferase activity to produce retinal degeneration. Proc Natl Acad Sci USA 102: 8472–8477.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pavri R, Zhu B, Li G, Trojer P, Mandal S, Shilatifard A et al. (2006). Histone H2B monoubiquitination functions cooperatively with FACT to regulate elongation by RNA polymerase II. Cell 125: 703–717.

    CAS  PubMed  Google Scholar 

  • Powell DW, Weaver CM, Jennings JL, McAfee KJ, He Y, Weil PA et al. (2004). Cluster analysis of mass spectrometry data reveals a novel component of SAGA. Mol Cell Biol 24: 7249–7259.

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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.

    CAS  PubMed  Google Scholar 

  • Pray-Grant MG, Schieltz D, McMahon SJ, Wood JM, Kennedy EL, Cook RG et al. (2002). The novel SLIK histone acetyltransferase complex functions in the yeast retrograde response pathway. Mol Cell Biol 22: 8774–8786.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Reeves WM, Hahn S . (2005). Targets of the Gal4 transcription activator in functional transcription complexes. Mol Cell Biol 25: 9092–9102.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ricci AR, Genereaux J, Brandl CJ . (2002). Components of the SAGA histone acetyltransferase complex are required for repressed transcription of ARG1 in rich medium. Mol Cell Biol 22: 4033–4042.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rodriguez-Navarro S, Fischer T, Luo MJ, Antunez O, Brettschneider S, Lechner J et al. (2004). Sus1, a functional component of the SAGA histone acetylase complex and the nuclear pore-associated mRNA export machinery. Cell 116: 75–86.

    CAS  PubMed  Google Scholar 

  • Russell SJ, Reed SH, Huang W, Friedberg EC, Johnston SA . (1999). The 19S regulatory complex of the proteasome functions independently of proteolysis in nucleotide excision repair. Mol Cell 3: 687–695.

    CAS  PubMed  Google Scholar 

  • Saleh A, Schieltz D, Ting N, McMahon SB, Litchfield DW, Yates III JR et al. (1998). Tra1p is a component of the yeast Ada–Spt transcriptional regulatory complexes. J Biol Chem 273: 26559–26565.

    CAS  PubMed  Google Scholar 

  • Santos-Rosa H, Schneider R, Bannister AJ, Sherriff J, Bernstein BE, Emre NC et al. (2002). Active genes are tri-methylated at K4 of histone H3. Nature 419: 407–411.

    CAS  PubMed  Google Scholar 

  • Schauber C, Chen L, Tongaonkar P, Vega I, Lambertson D, Potts W et al. (1998). Rad23 links DNA repair to the ubiquitin/proteasome pathway. Nature 391: 715–718.

    CAS  PubMed  Google Scholar 

  • Sekito T, Thornton J, Butow RA . (2000). Mitochondria-to-nuclear signaling is regulated by the subcellular localization of the transcription factors Rtg1p and Rtg3p. Mol Biol Cell 11: 2103–2115.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shukla A, Bajwa P, Bhaumik SR . (2006b). SAGA-associated Sgf73p facilitates formation of the preinitiation complex assembly at the promoters either in a HAT-dependent or independent manner in vivo. Nucleic Acids Res 34: 6225–6232.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shukla A, Stanojevic N, Duan Z, Sen P, Bhaumik SR . (2006a). Ubp8p, a histone deubiquitinase whose association with SAGA is mediated by Sgf11p, differentially regulates lysine 4 methylation of histone H3 in vivo. Mol Cell Biol 26: 3339–3352.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sims III RJ, Chen CF, Santos-Rosa H, Kouzarides T, Patel SS, Reinberg D . (2005). Human but not yeast Chd1 binds directly and selectively to histone H3 methylated at lysine 4 via its tandem chromodomains. J Biol Chem 280: 41789–41792.

    CAS  PubMed  Google Scholar 

  • 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.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sterner DE, Grant PA, Roberts SM, Duggan LJ, Belotserkovskaya R, Pacella LA et al. (1999). Functional organization of the yeast SAGA complex: distinct components involved in structural integrity, nucleosome acetylation, and TATA-binding protein interaction. Mol Cell Biol 19: 86–98.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Strahl BD, Allis CD . (2000). The language of covalent histone modifications. Nature 403: 41–45.

    CAS  PubMed  Google Scholar 

  • Sträßer K, Hurt E . (2000). Yra1p, a conserved nuclear RNA-binding protein, interacts directly with Mex67p and is required for mRNA export. EMBO J 19: 410–420.

    PubMed  PubMed Central  Google Scholar 

  • Sun ZW, Allis CD . (2002). Ubiquitination of histone H2B regulates H3 methylation and gene silencing in yeast. Nature 418: 104–108.

    CAS  PubMed  Google Scholar 

  • Timmers HT, Tora L . (2005). SAGA unveiled. Trends Biochem Sci 30: 7–10.

    CAS  PubMed  Google Scholar 

  • Utley RT, Ikeda K, Grant PA, Côté J, Steger DJ, Eberharter A et al. (1998). Transcriptional activators direct histone acetyltransferase complexes to nucleosomes. Nature 394: 498–502.

    CAS  PubMed  Google Scholar 

  • van Hemert MJ, van Heusden GP, Steensma HY . (2001). Yeast 14-3-3 proteins. Yeast 18: 889–895.

    CAS  PubMed  Google Scholar 

  • Winston F, Carlson M . (1992). Yeast SNF/SWI transcriptional activators and the SPT/SIN chromatin connection. Trends Genet 8: 387–391.

    CAS  PubMed  Google Scholar 

  • Wood A, Krogan NJ, Dover J, Schneider J, Heidt J, Boateng MA et al. (2003). Bre1, an E3 ubiquitin ligase required for recruitment and substrate selection of Rad6 at a promoter. Mol Cell 11: 267–274.

    CAS  PubMed  Google Scholar 

  • Wu PY, Ruhlmann C, Winston F, Schultz P. . (2004). Molecular architecture of the S. cerevisiae SAGA complex. Mol Cell 15: 199–208.

    CAS  PubMed  Google Scholar 

  • Wu PY, Winston F . (2002). Analysis of Spt7 function in the Saccharomyces cerevisiae SAGA coactivator complex. Mol Cell Biol 22: 5367–5379.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xu W, Edmondson DG, Evrard YA, Wakamiya M, Behringer RR, Roth SY . (2000). Loss of Gcn5l2 leads to increased apoptosis and mesodermal defects during mouse development. Nat Genet 26: 229–232.

    CAS  PubMed  Google Scholar 

  • Yang XJ . (2004). Lysine acetylation and the bromodomain: a new partnership for signaling. Bioessays 26: 1076–1087.

    CAS  PubMed  Google Scholar 

  • Yu Y, Teng Y, Liu H, Reed SH, Waters R . (2005). UV irradiation stimulates histone acetylation and chromatin remodeling at a repressed yeast locus. Proc Natl Acad Sci USA 102: 8650–8655.

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We apologize to those authors whose work could not be cited due to space limitations. We thank Christine H Baker for helpful comments and technical reading of this manuscript. Research in the Grant lab is funded from National Institutes of Health R01 Grant no. NS049065. SPB is supported by National Institutes of Health predoctoral cancer training Grant no. 5 T32 CA009109-30.

Author information

Authors and Affiliations

  1. Department of Biochemistry and Molecular Genetics, University of Virginia School of Medicine, Charlottesville, VA, USA

    S P Baker & P A Grant

Authors
  1. S P Baker
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. P A Grant
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to P A Grant.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Baker, S., Grant, P. The SAGA continues: expanding the cellular role of a transcriptional co-activator complex. Oncogene 26, 5329–5340 (2007). https://doi.org/10.1038/sj.onc.1210603

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/sj.onc.1210603

Keywords

This article is cited by

Search

Advanced search

Quick links