Functional organization of the yeast SAGA complex: Distinct components involved in structural integrity, nucleosome acetylation, and TATA-binding protein interaction

Molecular and Cellular Biology

Volumn 19, Issue 1, 1999, Pages 86-98

  Sterner, David E ^a   Grant, Patrick A ^b   Roberts, Shannon M ^c   Duggan, Laura J ^a   Belotserkovskaya, Rimma ^a   Pacella, Lisa A ^c   Winston, Fred ^c   Workman, Jerry L ^b   Berger, Shelley L ^a  

^a WISTAR INSTITUTE   (United States)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTATHIONE TRANSFERASE; HISTONE; TATA BINDING PROTEIN; TRANSCRIPTION FACTOR;

ACETYLATION; ARTICLE; FUNGUS MUTANT; NONHUMAN; NUCLEOSOME; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; SACCHAROMYCES CEREVISIAE; TATA BOX; TRANSCRIPTION INITIATION;

SACCHAROMYCES CEREVISIAE;

EID: 0032911635     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.19.1.86     Document Type: Article

References (82)

1. Ausubel, F. M., R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl (ed.). 1994. Current protocols in molecular biology. Wiley & Sons, Inc., New York, N.Y.
2. Bannister, A. J., and T. Kouzarides. 1996. The CBP co-activator is a histone acetyltransferase. Nature 384:641-643.
3. Barlev, N. A., R. Candau, L. Wang, P. Darpino, N. Silverman, and S. L. 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.
4. Barlev, N. A., V. Poltoratsky, T. Owen-Hughes, C. Ying, L. Liu, J. L. Workman, and S. L. 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.
5. Berger, S. L., B. Piña, N. Silverman, G. A. Marcus, J. Agapite, J. L. Regier, S. J. Triezenberg, and L. Guarenle. 1992. Genetic isolation of ADA2: a potential transcriptional adaptor required for function of certain acidic activation domains. Cell 70:251-265.
6. Boeke, J. D., F. LaCroute, and G. R. 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.
7. Bradbury, E. M. 1992. Reversible histone modifications and the chromosome cell cycle. Bioessays 14:9-16.
8. Braunstein, M., A. B. Rose, S. G. Holmes, C. D. Allis, and J. R. Broach. 1993. Transcriptional silencing in yeast is associated with reduced nucleosome acetylation. Genes Dev. 7:592-604.
9. Brownell, J. E., J. Zhou, T. Ranalli, R. Kobayashi, D. G. Edmondson, S. Y. Roth, and C. D. Allis. 1996. Tetrahymena histone acetyltransferase A: a transcriptional co-activator linking gene expression to histone acetylation. Cell 84:843-851.
10. Cairns, B. R., Y. Lorch, Y. Li, M. Zhang, L. Lacomis, H. Erdjument-Bromage, P. Tempst, J. Du, B. Laurent, and R. D. Kornberg. 1996. RSC, an essential, abundant chromatin-remodeling complex. Cell 87:1249-1260.
11. Candau, R., and S. L. Berger. 1996. Structural and functional analysis of yeast putative adaptors: evidence for an adaptor complex in vivo. J. Biol. Chem. 271:5237-5345.
12. Candau, R., P. A. Moore, L. Wang, N. Barlev, C. Y. Ying, C. A. Rosen, and S. L. Berger. 1996. Identification of functionally conserved human homologues of the yeast adaptors ADA2 and GCN5. Mol. Cell. Biol. 16:593-602.
13. Candau, R., J. Zhou, C. D. Allis, and S. L. Berger. 1997. Histone acetyltransferase activity and interaction with ADA2 are critical for GCN5 function in vivo. EMBO J. 16:555-565.
14. Chiang, Y. C., P. Komarnitsky, D. Chase, and C. L. Denis. 1996. ADR1 activation domains contact the histone acetyllransferase GCN5 and the core transcriptional factor TFIIB. J. Biol. Chem. 271:32359-32365.
15. Côté, J., J. Quinn, J. L. Workman, and C. L. Peterson. 1994. Stimulation of GAL4 derivative binding to nucleosomal DNA by the yeast SWI/SNF complex. Science 265:53-60.
16. Côté, J., R. T. Utley, and J. L. Workman. 1995. Analysis of transcription factor binding to nucleosomes. Methods Mol. Genet. 6:108-128.
17. Eisenmann, D. M., K. M. Arndt, S. L. Ricupero, J. W. Rooney, and F. Winston. 1992. SPT3 interacts with TFIID to allow normal transcription in Saccharomyces cerevisiae. Genes Dev. 6:1319-1331.
18. Eisenmann, D. M., C. Chapon, S. M. Roberts, C. Dollard, and F. 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.
19. Eisenmann, D. M., C. Dollard, and F. Winston. 1989. SPT15, the gene encoding the yeast TATA binding factor TFIID, is required for normal transcription initiation in vivo. Cell 58:1183-1191.
20. Gansheroff, L. J., C. Dollard, P. Tan, and F. Winston. 1995. The Saccharomyces cerevisiae SPT7 gene encodes a very acidic protein important for transcription in vivo. Genetics 139:523-536.
21. Georgakopoulos, T., N. Gounalaki, and G. Thireos. 1995. Genetic evidence for the interaction of the yeast transcriptional co-activator proteins GCN5 and ADA2. Mol. Gen. Genet. 246:723-728.
22. Georgakopoulos, T., and G. Thireos. 1992. Two distinct yeast transcriptional activators require the function of the GCN5 protein to promote normal levels of transcription. EMBO J. 11:4145-1152.
23. Grant, P. A. Unpublished data.
24. 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. L. 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.
25. Grant, P. A., D. Schieltz, M. G. Pray-Grant, D. J. Steger, J. C. Reese, J. R. Yates III, and J. L. Workman. 1998. A subset of TAFnS are integral components of the SAGA complex required for nucleosome acetylation and transcription stimulation. Cell 94:45-53.
26. Grant, P. A., D. E. Sterner, L. J. Duggan, J. L. Workman, and S. L. Berger. 1998. The SAGA unfolds: convergence of transcription regulators in chromatin-modifying complexes. Trends Cell. Biol. 8:193-197.
27. Gregory, P. D., A. Schmid, M. Zavari, L. Liu, S. L. Berger, and W. 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.
28. Guarente, L. 1995. Transcriptional coactivators in yeast and beyond. Trends Biochem. Sci. 29:517-521.
29. Hager, G., C. Smith, J. Svaren, and W. Hörz. 1995. Initiation of expression: remodelling genes, p. 89-103. In S. C. R. Elgin (ed.), Chromatin structure and gene expression, vol. 9. IRL Press, Oxford, England.
30. Hahn, S., S. Buratowski, P. A. Sharp, and L. 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.
31. Hampsey, M. 1997. A review of phenotypes in Saccharomyces cerevisiae. Yeast 13:1099-1133.
32. Harlow, E., and I. Lane. 1988. Antibodies: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
33. Haynes, S. R., C. Dollard, F. Winston, S. Beck, J. Trowsdale, and I. B. David. 1992. The bromodomain: a conserved sequence found in human. Drosophila and yeast proteins. Nucleic Acids Res. 20:2603.
34. Hebbes, T. R., A. L. Clayton, A. W. Thorne, and C. 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.
35. Hirschhorn, J. N., S. A. Brown, C. D. Clark, and F. Winston. 1992. Evidence that SNF2/SWI2 and SNF5 activate transcription in yeast by altering chromatin structure. Genes Dev. 6:2288-2298.
36. Horiuchi, J., N. Silverman, G. A. Marcus, and L. 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.
37. Horiuchi, J., N. Silverman, B. Piña, G. A. Marcus, and L. 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.
38. Imbalzano, A. N., H. Kwon, M. R. Green, and R. E. Kingston. 1994. Facilitated binding of TATA-binding protein to nucleosomal DNA. Nature 370: 481-485.
39. Ito, T., M. Bulger, M. J. Pazin, R. Kobayashi, and J. T. Kadonaga. 1997. ACT, an ISWI-containing and ATP-utilizing chromatin assembly and remodeling factor. Cell 90:145-155.
40. Iyer, V., and K. Struhl. 1996. Absolute mRNA levels and transcriptional initiation rates in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 93: 5208-5212.
41. Jeanmougin, F., J.-M. Wurtz, B. Le Douarin, P. Chambon, and R. Losson. 1997. The bromodomain revisited. Trends Biochem. Sci. 22:151-153.
42. Jeppesen, P., and B. M. 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.
43. Kingston, R. E., C. A. Bunker, and A. N. Imbalzano. 1996. Repression and activation by multiprotein complexes that alter chromatin structure. Genes Dev. 10:905-920.
44. Kuo, M.-H., J. Zhou, P. Jambeck, M. E. A. Churchill, and C. D. Allis. 1998. Histone acetyltransferase activity of yeast Gcn5p is required for the activation of target genes in vivo. Genes Dev. 12:627-639.
45. Kwon, H., A. N. Imbalzano, P. A. Khavari, R. E. Kingston, and M. R. Green. 1994. Nucleosome disruption and enhancement of activator binding by a human SWI/SNF complex. Nature 370:477-481.
46. Laurent, B. C., M. A. Treitel, and M. 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.
47. Marcus, G. A., J. Horiuchi, N. Silverman, and L. Guarente. 1996. ADA5/ SPT20 links the ADA and SPT genes, which are involved in yeast transcription. Mol. Cell. Biol. 16:3197-3205.
48. Marcus, G. A., N. Silverman, S. L. Berger, J. Huriuchi, and L. Guarente. 1994. Functional similarity and physical association between GCN5 and ADA2: putative transcriptional adaptors. EMBO J 13:4807-4815.
49. H250 subunit of TFIID has histone acetyltransferase activity. Cell 87:1261-1270.
50. O'Neill, L. P., and B. M. 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.
51. Ogryzko, V. V., R. L. Schlitz, V. Russanova, B. H. Howard, and Y. Nakatani. 1996. The transcriptional coactivators p300 and CBP arc histone acetyltransferases. Cell 87:953-959.
52. Owen-Hughes, T., R. T. Utley, J. Côté, C. L. Peterson, and J. L. Workman. 1996. Persistent site-specific remodeling of a nucleosome array by transient action of the SWI/SNF complex. Science 273:513-516.
53. Owen-Hughes, T., and J. L. Workman. 1994. Experimental analysis of chromalin function in transcription control. Crit. Rev. Eukaryotic Gene Expr. 4:403-441.
54. Ozer, J., L. E. Lezina, J. Ewing, S. Audi, and P. M. 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.
55. Paranjape, S. M., R. T. Kamakaka, and J. T. Kadonaga. 1994. Role of chromatin structure in the regulation of transcription by RNA polymerasc II. Annu. Rev. Biochem. 63:265-297.
56. Peterson, C. L., and I. Herskowitz. 1992. Characterization of the yeast SWII, SW12, and SW13 genes, which encode a global activator of transcription. Cell 68:573-583.
57. Pin̄a, B., S. Berger, G. A. Marcus, N. Silverman, J. Agapite, and L. 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.
58. Pollard, K. J., and C. L. Peterson. 1997. Role for ADA/GCN5 products in antagonizing chromatin-mediated transcriptional repression. Mol. Cell. Biol. 17:6212-6222.
59. Roberts, S. M., and F. 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 147:451-165.
60. Roberts, S. M., and F. 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.
61. Rose, M. D., F. Winston, and P. Hieter, 1990. Methods in yeast genetics: a laboratory course manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
62. Rothstein, R. J. 1983. One-step gene disruption in yeast. Methods Enzymol. 101:202-211.
63. Ruiz-García, A. B., R. Sendra, M. Pamblanco, and V. Tordera. 1997. Gcn5p is involved in the acetylation of histone H3 in nucleosomes. FEBS Lett. 403:186-190.
64. Saleh, A., V. Lang, R. Cook, and C. J. Brandi. 1997. Identification of native complexes containing the yeast coactivator/repressor proteins NGG1/ADA3 and ADA2. J. Biol. Chem. 272:5571-5578.
65. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
66. Scherer, S., and R. W. Davis. 1979. Replacement of chromosome segments with altered DNA sequences constructed in vitro. Proc. Natl. Acad. Sci. USA 76:4951-4955.
67. Sikorski, R. S., and P. Hieter. 1989. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122:19-27.
68. Silverman, N., J. Agapite, and L. Guarente. 1994. Yeast ADA2 protein hinds to the VP16 protein activation domain and activates transcription. Proc. Natl. Acad. Sci. USA 91:11665-11668.
69. Steger, D. J., and J. L. Workman. 1996. Remodeling chromatin structures for transcription: What happens to the histones? Bioessays 18:875-884.
70. Struhl, K. 1986. Constitutive and inducible Saccharomyces cerevisiae promoters: evidence for two distinct molecular mechanisms. Mol. Cell. Biol. 6:3847-3853.
71. Svaren, J., and W. Hörz. 1996. Regulation of gene expression by nucleosomes. Curr. Opin. Genet. Dev. 6:164-170.
72. Tamkun, J. W., R. Deuring, M. P. Scott, M. Kissinger, A. M. Pattatucci, T. C. Kaufman, and J. A. Kennison, 1992. brahma: a regulator of Drosophila homeotic genes structurally related to the yeast transcriptional activator SNF2/SW12. Cell 68:561-572.
73. Tsukiyama, T., and C. Wu. 1995. Purification and properties of an ATP dependent nucleosome remodeling factor. Cell 83:1011-1020.
74. Turner, B. M., A. J. Birley, and J. Lavender. 1992 Historic H4 isoforms acetylated at specific lysine residues define individual chromosomes and chromatin domains in Drosophila polytene nuclei. Cell 69:375-384.
75. Utley, R. T., K. Ikeda, P. A. Grant, J. Côté, D. J. Steger, A. Eberharter, S. John, and J. L. Workman. 1998. Transcriptional activators direct histone acetyltransferase complexes to nucleosomes. Nature 394:498-502.
76. Varga-Weisz, P. D., M. Wilm, E. Bonte, K. Dumas, M. Mann, and P. B. Becker. 1997. Chromatin-remodelling factor CHRAC contains the ATPases ISWI and topoisomerase II. Nature 388:598-602.
77. Vettese-Dadey, M., P. A. Grant, T. R. Hebbes, C. Crane-Robinson, C. D. Allis, and J. L. 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.
78. Wang, L., L. Liu, and S. L. 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.
79. Winston, F. 1992. Analysis of SPTgenes: a genetic approach toward analysis of TFIID, histones, and other transcription factors of yeast. p. 1271-1293. In S. L. McKnight and K. R. Yamamoto (ed.), Transcriptional regulation. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
80. Winston, F., C. Dollard, and S. L. Ricupero-Hovasse. 1995. Construction of a set of convenient Saccharomyces cerevisiae strains that are isogenic to S288C. Yeast 11:53-55.
81. Wolffe, A. P. 1992. Chromatin: structure and function. Academic Press, London, England.
82. Yang, X.-J., V. V. Ogryzko, J. Nishikawa, B. H. Howard, and Y. Nakatani. 1996. A p300/CBP-associated factor that competes with the adenoviral E1A oncoprotein. Nature 382:319-324.