Functional Organization of the Yeast SAGA Complex: Distinct Components Involved in Structural Integrity, Nucleosome Acetylation, and TATA-Binding Protein Interaction

REFERENCES

• Ausubel F. M., R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, K. Struhl 1994. Current protocols in molecular biology. Wiley & Sons, Inc., New York, N.Y.
   Google Scholar
• Bannister, A. J., and J. Kouzarides 1996. The CBP co-activator is a histone acetyltransferase. Nature 384:641–643.
   PubMed Web of Science ®Google Scholar
• Barlev, N. A., R. Candau, L. Wang, P. Darpino, N. Silverman, and J. Berger 1995. Characterization of physical interactions of the putative transcriptional adaptor, ADA2, with acidic activation domains and TATA-binding protein. J. Biol. Chem. 270:19337–19344.
   PubMedGoogle Scholar
• Barlev, N. A., V. Poltoratsky, T. Owen-Hughes, C. Ying, L. Liu, J. L. Workman, and J. Berger 1998. Repression of GCN5 histone acetyltransferase activity via bromodomain-mediated binding and phosphorylation by the Ku/DNA-dependent protein kinase complex. Mol. Cell. Biol. 18:1349–1358.
   PubMedGoogle Scholar
• Berger, S. L., B. Piña, N. Silverman, G. A. Marcus, J. Agapite, J. L. Regier, S. J. Triezenberg, and J. Guarente 1992. Genetic isolation of ADA2: a potential transcriptional adaptor required for function of certain acidic activation domains. Cell 70:251–265.
   PubMed Web of Science ®Google Scholar
• Boeke, J. D., F. LaCroute, and J. Fink 1984. A positive selection for mutants lacking orotidine-5′-phosphate decarboxylase activity in yeast: 5-fluoro-orotic acid resistance. Mol. Gen. Genet. 197:345–346.
   PubMedGoogle Scholar
• Bradbury, E. M. 1992. Reversible histone modifications and the chromosome cell cycle. Bioessays 14:9–16.
   PubMed Web of Science ®Google Scholar
• Braunstein, M., A. B. Rose, S. G. Holmes, C. D. Allis, and J. Broach 1993. Transcriptional silencing in yeast is associated with reduced nucleosome acetylation. Genes Dev. 7:592–604.
   PubMed Web of Science ®Google Scholar
• Brownell, J. E., J. Zhou, T. Ranalli, R. Kobayashi, D. G. Edmondson, S. Y. Roth, and J. Allis 1996. Tetrahymena histone acetyltransferase A: a transcriptional co-activator linking gene expression to histone acetylation. Cell 84:843–851.
   PubMed Web of Science ®Google Scholar
• Cairns, B. R., Y. Lorch, Y. Li, M. Zhang, L. Lacomis, H. Erdjument-Bromage, P. Tempst, J. Du, B. Laurent, and J. Kornberg 1996. RSC, an essential, abundant chromatin-remodeling complex. Cell 87:1249–1260.
   PubMed Web of Science ®Google Scholar
• Candau, R., and J. Berger 1996. Structural and functional analysis of yeast putative adaptors: evidence for an adaptor complex in vivo. J. Biol. Chem. 271:5237–5345.
   PubMedGoogle Scholar
• Candau, R., P. A. Moore, L. Wang, N. Barlev, C. Y. Ying, C. A. Rosen, and J. Berger 1996. Identification of functionally conserved human homologues of the yeast adaptors ADA2 and GCN5. Mol. Cell. Biol. 16:593–602.
   PubMedGoogle Scholar
• Candau, R., J. Zhou, C. D. Allis, and J. Berger 1997. Histone acetyltransferase activity and interaction with ADA2 are critical for GCN5 function in vivo. EMBO J. 16:555–565.
   PubMedGoogle Scholar
• Chiang, Y. C., P. Komarnitsky, D. Chase, and J. Denis 1996. ADR1 activation domains contact the histone acetyltransferase GCN5 and the core transcriptional factor TFIIB. J. Biol. Chem. 271:32359–32365.
   PubMedGoogle Scholar
• Côté, J., J. Quinn, J. L. Workman, and J. Peterson 1994. Stimulation of GAL4 derivative binding to nucleosomal DNA by the yeast SWI/SNF complex. Science 265:53–60.
   PubMed Web of Science ®Google Scholar
• Côté, J., R. T. Utley, and J. Workman 1995. Analysis of transcription factor binding to nucleosomes. Methods Mol. Genet. 6:108–128.
   Google Scholar
• Eisenmann, D. M., K. M. Arndt, S. L. Ricupero, J. W. Rooney, and J. Winston 1992. SPT3 interacts with TFIID to allow normal transcription in Saccharomyces cerevisiae. Genes Dev. 6:1319–1331.
   PubMed Web of Science ®Google Scholar
• Eisenmann, D. M., C. Chapon, S. M. Roberts, C. Dollard, and J. Winston 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.
   PubMedGoogle Scholar
• Eisenmann, D. M., C. Dollard, and J. Winston 1989. SPT15, the gene encoding the yeast TATA binding factor TFIID, is required for normal transcription initiation in vivo. Cell 58:1183–1191.
   PubMed Web of Science ®Google Scholar
• Gansheroff, L. J., C. Dollard, P. Tan, and J. Winston 1995. The Saccharomyces cerevisiae SPT7 gene encodes a very acidic protein important for transcription in vivo. Genetics 139:523–536.
   PubMedGoogle Scholar
• Georgakopoulos, T., N. Gounalaki, and J. Thireos 1995. Genetic evidence for the interaction of the yeast transcriptional co-activator proteins GCN5 and ADA2. Mol. Gen. Genet. 246:723–728.
   PubMedGoogle Scholar
• Georgakopoulos, T., and J. Thireos 1992. Two distinct yeast transcriptional activators require the function of the GCN5 protein to promote normal levels of transcription. EMBO J. 11:4145–4152.
   PubMed Web of Science ®Google Scholar
• Grant, P. A. Unpublished data.
   Google Scholar
• Grant, P. A., L. Duggan, J. Côté, S. M. Roberts, J. E. Brownell, R. Candau, R. Ohba, T. Owen-Hughes, C. D. Allis, F. Winston, S. L. Berger, and J. Workman 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.
   PubMed Web of Science ®Google Scholar
• Grant, P. A., D. Schieltz, M. G. Pray-Grant, D. J. Steger, J. C. Reese, J. R. Yates III, and J. Workman 1998. A subset of TAFIIs are integral components of the SAGA complex required for nucleosome acetylation and transcription stimulation. Cell 94:45–53.
   PubMedGoogle Scholar
• Grant, P. A., D. E. Sterner, L. J. Duggan, J. L. Workman, and J. Berger 1998. The SAGA unfolds: convergence of transcription regulators in chromatin-modifying complexes. Trends Cell. Biol. 8:193–197.
   PubMed Web of Science ®Google Scholar
• Gregory, P. D., A. Schmid, M. Zavari, L. Liu, S. L. Berger, and J. Hörz 1998. Absence of Gcn5 HAT activity defines a novel state in the opening of chromatin at the PHO5 promoter in yeast. Mol. Cell 1:495–505.
   PubMedGoogle Scholar
• Guarente, L. 1995. Transcriptional coactivators in yeast and beyond. Trends Biochem. Sci. 20:517–521.
   PubMedGoogle Scholar
• Hager, G., C. Smith, J. Svaren, and J. Hörz 1995. Initiation of expression: remodelling genes Chromatin structure and gene expression In S. C. R. Elgin (ed.), 9:89–103 IRL Press, Oxford, England.
   Google Scholar
• Hahn, S., S. Buratowski, P. A. Sharp, and J. Guarente 1989. Isolation of the gene encoding the yeast TATA binding protein TFIID: a gene identical to the SPT15 suppressor of Ty element insertions. Cell 58:1173–1181.
   PubMedGoogle Scholar
• Hampsey, M. 1997. A review of phenotypes in Saccharomyces cerevisiae. Yeast 13:1099–1133.
   PubMed Web of Science ®Google Scholar
• Harlow, E., I. Lane 1988. Antibodies: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
   Google Scholar
• Haynes, S. R., C. Dollard, F. Winston, S. Beck, J. Trowsdale, and J. Dawid 1992. The bromodomain: a conserved sequence found in human, Drosophila and yeast proteins. Nucleic Acids Res. 20:2603.
   PubMed Web of Science ®Google Scholar
• Hebbes, T. R., A. L. Clayton, A. W. Thorne, and J. Crane-Robinson 1994. Core histone hyperacetylation co-maps with generalized DNase I sensitivity in the chicken beta-globin chromosomal domain. EMBO J. 13:1823–1830.
   PubMed Web of Science ®Google Scholar
• Hirschhorn, J. N., S. A. Brown, C. D. Clark, and J. Winston 1992. Evidence that SNF2/SWI2 and SNF5 activate transcription in yeast by altering chromatin structure. Genes Dev. 6:2288–2298.
   PubMed Web of Science ®Google Scholar
• Horiuchi, J., N. Silverman, G. A. Marcus, and J. Guarente 1995. ADA3, a putative transcriptional adaptor, consists of two separable domains and interacts with ADA2 and GCN5 in a trimeric complex. Mol. Cell. Biol. 15:1203–1209.
   PubMed Web of Science ®Google Scholar
• Horiuchi, J., N. Silverman, B. Piña, G. A. Marcus, and J. Guarente 1997. ADA1, a novel component of the ADA/GCN5 complex, has broader effects than GCN5, ADA2, or ADA3. Mol. Cell. Biol. 17:3220–3228.
   PubMedGoogle Scholar
• Imbalzano, A. N., H. Kwon, M. R. Green, and J. Kingston 1994. Facilitated binding of TATA-binding protein to nucleosomal DNA. Nature 370:481–485.
   PubMed Web of Science ®Google Scholar
• Ito, T., M. Bulger, M. J. Pazin, R. Kobayashi, and J. Kadonaga 1997. ACF, an ISWI-containing and ATP-utilizing chromatin assembly and remodeling factor. Cell 90:145–155.
   PubMed Web of Science ®Google Scholar
• Iyer, V., and J. Struhl 1996. Absolute mRNA levels and transcriptional initiation rates in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 93:5208–5212.
   PubMed Web of Science ®Google Scholar
• Jeanmougin, F., J.-M. Wurtz, B. Le Douarin, P. Chambon, and J. Losson 1997. The bromodomain revisited. Trends Biochem. Sci. 22:151–153.
   PubMed Web of Science ®Google Scholar
• Jeppesen, P., and J. Turner 1993. The inactive X chromosome in female mammals is distinguished by a lack of histone H4 acetylation, a cytogenetic marker for gene expression. Cell 74:281–289.
   PubMed Web of Science ®Google Scholar
• Kingston, R. E., C. A. Bunker, and J. Imbalzano 1996. Repression and activation by multiprotein complexes that alter chromatin structure. Genes Dev. 10:905–920.
   PubMed Web of Science ®Google Scholar
• Kuo, M.-H., J. Zhou, P. Jambeck, M. E. A. Churchill, and J. Allis 1998. Histone acetyltransferase activity of yeast Gcn5p is required for the activation of target genes in vivo. Genes Dev. 12:627–639.
   PubMed Web of Science ®Google Scholar
• Kwon, H., A. N. Imbalzano, P. A. Khavari, R. E. Kingston, and J. Green 1994. Nucleosome disruption and enhancement of activator binding by a human SWI/SNF complex. Nature 370:477–481.
   PubMed Web of Science ®Google Scholar
• Laurent, B. C., M. A. Treitel, and J. Carlson 1990. The SNF5 protein of Saccharomyces cerevisiae is a glutamine- and proline-rich transcriptional activator that affects expression of a broad spectrum of genes. Mol. Cell. Biol. 10:5616–5625.
   PubMed Web of Science ®Google Scholar
• Marcus, G. A., J. Horiuchi, N. Silverman, and J. Guarente 1996. ADA5/SPT20 links the ADA and SPT genes, which are involved in yeast transcription. Mol. Cell. Biol. 16:3197–3205.
   PubMedGoogle Scholar
• Marcus, G. A., N. Silverman, S. L. Berger, J. Horiuchi, and J. Guarente 1994. Functional similarity and physical association between GCN5 and ADA2: putative transcriptional adaptors. EMBO J. 13:4807–4815.
   PubMed Web of Science ®Google Scholar
• Mizzen, C. A., X.-J. Yang, T. Kokubo, J. E. Brownell, A. J. Bannister, T. Owen-Hughes, J. Workman, L. Wang, S. L. Berger, T. Kouzarides, Y. Nakatani, and J. Allis 1996. The TAFII250 subunit of TFIID has histone acetyltransferase activity. Cell 87:1261–1270.
   PubMed Web of Science ®Google Scholar
• O’Neill, L. P., and J. Turner 1995. Histone H4 acetylation distinguishes coding regions of the human genome from heterochromatin in a differentiation-dependent but transcription-independent manner. EMBO J. 14:3946–3957.
   PubMed Web of Science ®Google Scholar
• Ogryzko, V. V., R. L. Schlitz, V. Russanova, B. H. Howard, and J. Nakatani 1996. The transcriptional coactivators p300 and CBP are histone acetyltransferases. Cell 87:953–959.
   PubMed Web of Science ®Google Scholar
• Owen-Hughes, T., R. T. Utley, J. Côté, C. L. Peterson, and J. Workman 1996. Persistent site-specific remodeling of a nucleosome array by transient action of the SWI/SNF complex. Science 273:513–516.
   PubMedGoogle Scholar
• Owen-Hughes, T., and J. Workman 1994. Experimental analysis of chromatin function in transcription control. Crit. Rev. Eukaryotic Gene Expr. 4:403–441.
   PubMedGoogle Scholar
• Ozer, J., L. E. Lezina, J. Ewing, S. Audi, and J. Lieberman 1998. Association of transcription factor IIA with TATA binding protein is required for transcriptional activation of a subset of promoters and cell cycle progression in Saccharomyces cerevisiae. Mol. Cell. Biol. 18:2559–2570.
   PubMedGoogle Scholar
• Paranjape, S. M., R. T. Kamakaka, and J. Kadonaga 1994. Role of chromatin structure in the regulation of transcription by RNA polymerase II. Annu. Rev. Biochem. 63:265–297.
   PubMed Web of Science ®Google Scholar
• Peterson, C. L., and J. Herskowitz 1992. Characterization of the yeast SWI1, SWI2, and SWI3 genes, which encode a global activator of transcription. Cell 68:573–583.
   PubMed Web of Science ®Google Scholar
• Piña, B., S. Berger, G. A. Marcus, N. Silverman, J. Agapite, and J. Guarente 1993. ADA3: a gene, identified by resistance to GAL4-VP16, with properties similar to and different from those of ADA2. Mol. Cell. Biol. 13:5981–5989.
   PubMedGoogle Scholar
• Pollard, K. J., and J. Peterson 1997. Role for ADA/GCN5 products in antagonizing chromatin-mediated transcriptional repression. Mol. Cell. Biol. 17:6212–6222.
   PubMedGoogle Scholar
• Roberts, S. M., and J. Winston 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.
   PubMedGoogle Scholar
• Roberts, S. M., and J. Winston 1996. SPT20/ADA5 encodes a novel protein functionally related to the TATA-binding protein and important for transcription in Saccharomyces cerevisiae. Mol. Cell. Biol. 16:3206–3213.
   PubMedGoogle Scholar
• Rose, M. D., F. Winston, P. Hieter 1990. Methods in yeast genetics: a laboratory course manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
   Google Scholar
• Rothstein, R. J. 1983. One-step gene disruption in yeast. Methods Enzymol. 101:202–211.
   PubMed Web of Science ®Google Scholar
• Ruiz-García, A. B., R. Sendra, M. Pamblanco, and J. Tordera 1997. Gcn5p is involved in the acetylation of histone H3 in nucleosomes. FEBS Lett. 403:186–190.
   PubMedGoogle Scholar
• Saleh, A., V. Lang, R. Cook, and J. Brandl 1997. Identification of native complexes containing the yeast coactivator/repressor proteins NGG1/ADA3 and ADA2. J. Biol. Chem. 272:5571–5578.
   PubMed Web of Science ®Google Scholar
• Sambrook, J., E. F. Fritsch, T. Maniatis 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
   Google Scholar
• Scherer, S., and J. Davis 1979. Replacement of chromosome segments with altered DNA sequences constructed in vitro. Proc. Natl. Acad. Sci. USA 76:4951–4955.
   PubMed Web of Science ®Google Scholar
• Sikorski, R. S., and J. Hieter 1989. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122:19–27.
   PubMed Web of Science ®Google Scholar
• Silverman, N., J. Agapite, and J. Guarente 1994. Yeast ADA2 protein binds to the VP16 protein activation domain and activates transcription. Proc. Natl. Acad. Sci. USA 91:11665–11668.
   PubMedGoogle Scholar
• Steger, D. J., and J. Workman 1996. Remodeling chromatin structures for transcription: What happens to the histones? Bioessays 18:875–884.
   PubMedGoogle Scholar
• Struhl, K. 1986. Constitutive and inducible Saccharomyces cerevisiae promoters: evidence for two distinct molecular mechanisms. Mol. Cell. Biol. 6:3847–3853.
   PubMedGoogle Scholar
• Svaren, J., and J. Hörz 1996. Regulation of gene expression by nucleosomes. Curr. Opin. Genet. Dev. 6:164–170.
   PubMedGoogle Scholar
• Tamkun, J. W., R. Deuring, M. P. Scott, M. Kissinger, A. M. Pattatucci, T. C. Kaufman, and J. Kennison 1992. brahma: a regulator of Drosophila homeotic genes structurally related to the yeast transcriptional activator SNF2/SWI2. Cell 68:561–572.
   PubMed Web of Science ®Google Scholar
• Tsukiyama, T., and J. Wu 1995. Purification and properties of an ATP dependent nucleosome remodeling factor. Cell 83:1011–1020.
   PubMed Web of Science ®Google Scholar
• Turner, B. M., A. J. Birley, and J. Lavender 1992. Histone H4 isoforms acetylated at specific lysine residues define individual chromosomes and chromatin domains in Drosophila polytene nuclei. Cell 69:375–384.
   PubMed Web of Science ®Google Scholar
• Utley, R. T., K. Ikeda, P. A. Grant, J. Côté, D. J. Steger, A. Eberharter, S. John, and J. Workman 1998. Transcriptional activators direct histone acetyltransferase complexes to nucleosomes. Nature 394:498–502.
   PubMed Web of Science ®Google Scholar
• Varga-Weisz, P. D., M. Wilm, E. Bonte, K. Dumas, M. Mann, and J. Becker 1997. Chromatin-remodelling factor CHRAC contains the ATPases ISWI and topoisomerase II. Nature 388:598–602.
   PubMedGoogle Scholar
• Vettese-Dadey, M., P. A. Grant, T. R. Hebbes, C. Crane-Robinson, C. D. Allis, and J. Workman 1996. Acetylation of histone H4 plays a primary role in enhancing transcription factor binding to nucleosomal DNA in vitro. EMBO J. 15:2508–2518.
   PubMed Web of Science ®Google Scholar
• Wang, L., L. Liu, and J. Berger 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.
   PubMed Web of Science ®Google Scholar
• Winston, F. 1992. Analysis of SPT genes: a genetic approach toward analysis of TFIID, histones, and other transcription factors of yeast, p. 1271–1293. In S. L. McKnight, K. R. Yamamoto (ed.), Transcriptional regulation. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
   Google Scholar
• Winston, F., C. Dollard, and J. Ricupero-Hovasse 1995. Construction of a set of convenient Saccharomyces cerevisiae strains that are isogenic to S288C. Yeast 11:53–55.
   PubMed Web of Science ®Google Scholar
• Wolffe, A. P. 1992. Chromatin: structure and function. Academic Press, London, England.
   Google Scholar
• Yang, X.-J., V. V. Ogryzko, J. Nishikawa, B. H. Howard, and J. Nakatani 1996. A p300/CBP-associated factor that competes with the adenoviral E1A oncoprotein. Nature 382:319–324.
   PubMed Web of Science ®Google Scholar