The novel SLIK histone acetyltransferase complex functions in the yeast retrograde response pathway

Molecular and Cellular Biology

Volumn 22, Issue 24, 2002, Pages 8774-8786

  Pray Grant, Marilyn G ^a   Schieltz, David ^b   McMahon, Stacey J ^a   Wood, Jennifer M ^a   Kennedy, Erin L ^a   Cook, Richard G ^c   Workman, Jerry L ^d   Yates III, John R ^e   Grant, Patrick A ^a,f  

^a UNIVERSITY OF VIRGINIA   (United States)

^b SYNGENTA BIOTECHNOLOGY INC   (United States)

^c BAYLOR COLLEGE OF MEDICINE   (United States)

^d PENNSYLVANIA STATE UNIVERSITY   (United States)

^e SCRIPPS RESEARCH INSTITUTE   (United States)

^f UNIVERSITY OF VIRGINIA HEALTH SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACYLTRANSFERASE; HISTONE ACETYLTRANSFERASE; PROTEIN RTG2; PROTEIN SLIK; REGULATOR PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SAGA; UNCLASSIFIED DRUG;

ARTICLE; COMPLEX FORMATION; DNA RESPONSIVE ELEMENT; FUNGUS MUTANT; GENE CONTROL; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEUS; SACCHAROMYCES CEREVISIAE;

ACETYLTRANSFERASES; CHROMATIN; CULTURE MEDIA; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; GENES, FUNGAL; HISTONE ACETYLTRANSFERASES; HUMANS; MACROMOLECULAR SUBSTANCES; MUTATION; PHENOTYPE; PROMOTER REGIONS (GENETICS); PROTEIN BINDING; PROTEIN SUBUNITS; RECOMBINANT FUSION PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

ADA; FUNGI; SACCHAROMYCES CEREVISIAE;

EID: 18744374136     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.22.24.8774-8786.2002     Document Type: Article

References (65)

1. Allard, S., R. T. Utley, J. Savard, A. Clarke, P. Grant, C. Brandl, L. Pillus, J. L. Workman, and J. Côté. 1999. NuA4, an essential transcription adaptor/histone H4 acetyltransferase complex containing Esa1p and the ATM-related cofactor Tra1p. EMBO J. 18:5108-5119.
2. Apone, L. M., C. M. Virbasius, J. C. Reese, and M. R. Green. 1996. Yeast TAF(II)90 is required for cell-cycle progression through G2/M but not for general transcription activation. Genes Dev. 10:2368-2380.
3. Balasubramanian, R., M. G. Pray-Grant, W. Selleck, P. A. Grant, and S. Tan. 2002. Role of the Ada2 and Ada3 transcriptional coactivators in histone acetylation. J. Biol. Chem. 277:7989-7995.
4. Belotserkovskaya, R., D. E. Sterner, M. Deng, M. H. Sayre, P. M. Lieberman, and S. L. Berger. 2000. Inhibition of TATA-binding protein function by SAGA subunits Spt3 and Spt8 at Gcn4-activated promoters. Mol. Cell. Biol. 20:634-647.
5. Bhaumik, S. R., and M. R. Green. 2001. SAGA is an essential in vivo target of the yeast acidic activator Ga14p. Genes Dev. 288:1935-1945.
6. Brand, M., K. Yamamoto, A. Staub, and L. Tora. 1999. Identification of TATA-binding protein-free TAFII-containing complex subunits suggests a role in nucleosome acetylation and signal transduction. J. Biol. Chem. 274:18285-18289.
7. Brown, C. E., L. Howe, K. Sousa, S. C. Alley, M. J. Carrozza, S. Tan, and J. L. Workman. 2001. Recruitment of HAT complexes by direct activator interactions with the ATM-related Tra1 subunit. Science 292:2333-2337.
8. 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 homolog to yeast Gcn5p linking histone acetylation to gene activation. Cell 84:843-851.
9. Dudley, A. M., L. J. Gansheroff, and F. Winston. 1999. Specific components of the SAGA complex are required for Gcn4- and Gcr1-mediated activation of the his4-912delta promoter in Saccharomyces cerevisiae. Genetics 151:1365-1378.
10. Dudley, A. M., C. Rougeulle, and F. Winston. 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.
11. Eberharter, A., D. E. Sterner, D. Schieltz, A. Hassan, J. R. Yates, S. L. Berger, and J. L. Workman. 1999. The ADA complex is a distinct histone acetyltransferase complex in Saccharomyces cerevisiae. Mol. Cell. Biol. 19:6621-6631.
12. Eisenmann, D. M., K. M. Arnt, 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.
13. 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.
14. Epstein, C. B., J. A. Waddle, W. Hale, V. Dave, J. Thornton, T. L. Macatee, H. R. Garner, and R. A. Butow. 2001. Genome-wide responses to mitochondrial dysfunction. Mol. Biol. Cell 12:297-308.
15. 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.
16. Grant, P. A. 2001. A tale of histone modifications. Genome Biol. 2:0003.1-0003.5.
17. Grant, P. A., and S. L. Berger. 1999. Histone acetyltransferase complexes. Semin. Cell Dev. Biol. 10:169-177.
18. Grant, P. A., S. L. Berger, and J. L. Workman. 1999. Identification and analysis of native nucleosomal histone acetyltransferase complexes. Methods Mol. Biol. 119:311-317.
19. 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.
20. Grant, P. A., A. Eberharter, S. John, R. G. Cook, B. M. Turner, and J. L. Workman. 1999. Expanded lysine acetylation specificity of Gcn5 in native complexes. J. Biol. Chem. 274:5895-5900.
21. 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 TAFIIs are integral components of the SAGA complex required for nucleosome acetylation and transcription stimulation. Cell 94:45-53.
22. Grant, P. A., D. Schieltz, M. G. Pray-Grant, J. R. Yates, and J. L. Workman. 1998. The ATM-related cofactor Tra1 is a component of the purified SAGA complex. Mol. Cell 2:863-867.
23. 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.
24. Holstege, F. C. P., E. G. Jennings, J. J. Wyrick, T. I. Lee, C. J. Hengartner, M. R. Green, T. R. Golub, E. S. Lander, and R. A. Young. 1998. Dissecting the regulatory circuitry of a eukaryotic genome. Cell 95:717-728.
25. 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.
26. Jia, Y., B. Rothermel, J. Thornton, and R. A. Butow. 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.
27. John, S., L. Howe, S. T. Tafrov, P. A. Grant, R. Sternglanz, and J. L. Workman. 2000. The something about silencing protein, Sas3, is the catalytic subunit of NuA3, a yTAF(II)30-containing HAT complex that interacts with the Spt16 subunit of the yeast CP (Cdc68/Pob3)-FACT complex. Genes Dev. 14:1196-1208.
28. Komeili, A., K. P. Wedaman, E. K. O'Shea, and T. Powers. 2000. Mechanism of metabolic control. Target of rapamycin signaling links nitrogen quality to the activity of the Rtg1 and Rtg3 transcription factors. J. Cell Biol. 13:863-878.
29. Krebs, J. E., C. J. Fry, M. L. Samuels, and C. L. Peterson. 2000. Global role for chromatin remodeling enzymes in mitotic gene expression. Cell 102:587-598.
30. Kuo, M.-H., and C. D. Allis. 1999. In vivo cross-linking and immunoprecipitation for studying dynamic protein:DNA associations in a chromatin environment. Methods 19:425-433.
31. 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.
32. Larschan, E., and F. Winston. 2001. The S. cerevisiae SAGA complex functions in vivo as a coactivator for transcriptional activation by Ga14. Genes Dev. 15:1946-1956.
33. Lechner, T., M. J. Carrozza, Y. Yu, P. A. Grant, A. Eberharter, D. Vannier, G. Brosch, D. J. Stillman, D. Shore, and J. L. Workman. 2000. Sds3 (suppressor of defective silencing 3) is an integral component of the yeast Sin3·Rpd3 histone deacetylase complex and is required for histone deacetylase activity. J. Biol. Chem. 275:40961-40966.
34. Lee, T. I., H. C. Causton, F. C. Holstege, W. C. Shen, N. Hannett, E. G. Jennings, F. Winston, M. R. Green, and R. A. Young. 2000. Redundant roles for the TFIID and SAGA complexes in global transcription. Nature 405:701-704.
35. Liao, X., and R. A. Butow. 1993. RTG1 and RTG2: Two yeast genes required for a novel path of communication from mitochondria to the nucleus. Cell 72:61-71.
36. 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.
37. Martinez, E., T. K. Kundu, J. Fu, and R. G. Roeder. 1998. A human SPT3TAFII31-GCN5-L acetylase complex distinct from transcription factor IID. J. Biol. Chem. 273:23781-23785.
38. Massari, M. E., P. A. Grant, M. G. Pray-Grant, S. L. Berger, J. L. Workman, and C. Murre. 1999. A conserved motif present in a class of helix-loop-helix proteins activates transcription by direct recruitment of the SAGA complex. Mol. Cell 4:63-73.
39. McMahon, S. B., H. A. Van Buskirk, K. A. Dugan, T. D. Copeland, and M. D. Cole. 1998. The novel ATM-related protein TRRAP is an essential cofactor for the c-Myc and E2F oncoproteins. Cell 94:363-374.
40. Ogryzko, V. V., T. Kotani, X. Zhang, R. L. Schiltz, T. Howard, X.-J. Yang, B. H. Howard, J. Qin, and Y. Nakatani. 1998. Histone-like TAFs within the PCAF histone acetylase complex. Cell 94:35-44.
41. Park, J., S. Kunjibettu, S. B. McMahon, and M. D. Cole. 2001. The ATM-related domain of TRRAP is required for histone acetyltransferase recruitment and Myc-dependent oncogenesis. Genes Dev. 15:1619-1624.
42. Peterson, C. L., A. Dingwall, and M. P. Scott. 1994. Five SWI/SNF gene products are components of a large multisubunit complex required for transcriptional enhancement. Proc. Natl. Acad. Sci. USA 91:2905-2908.
43. 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.
44. Rigaut, G., A. Shevchenko, B. Rutz, M. Wilm, M. Mann, and B. Séraphin. 1999. A generic protein purification method for protein complex characterization and proteome exploration. Nat. Biotechnol. 17:1030-1032.
45. Roberts, S. M., and F. Winston. 1997. Essential functional interaction of SAGA, a Saccharomyces cerevisiae complex of Spt, Ada, Gcn5 proteins, with the Snf/Swi and Srb/mediator complexes. Genetics 147:451-465.
46. 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.
47. Roth, S. Y., J. M. Denu, and C. D. Allis. 2001. Histone acetyltransferases. Annu. Rev. Biochem. 70:81-120.
48. Rothermel, B. A., J. L. Thornton, and R. A. Butow. 1997. Rtg3p, a basic helix-loop-helix/leucine zipper protein that functions in mitochondrial-induced changes in gene expression, contains independent activation domains. J. Biol. Chem. 272:19801-19807.
49. Ruiz-Garcia, 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.
50. Saleh, A., V. Lang, R. Cook, and C. J. Brandl. 1997. Identification of native complexes containing the yeast coactivator/repressor proteins NGG1/ADA3 and ADA2. J. Biol. Chem. 272:5571-5578.
51. Sekito, T., J. Thornton, and R. A. Butow. 2000. Mitochondria-to-nuclear signaling is regulated by the subcellular localization of the transcription factors Rtg1p and Rtg3p. Mol. Biol. Cell 11:103-115.
52. Sendra, R., C. Tse, and J. C. Hansen. 2000. The yeast histone acetyltransferase A2 complex, but not free Gcn5p, binds stably to nucleosomal arrays. J. Biol. Chem. 275:24928-24934.
53. Sobel, R. E., R. G. Cook, and C. D. Allis. 1994. Non-random acetylation of histone H4 by cytoplasmic acetyltransferase as determined by novel methodology. J. Biol. Chem. 28:18576-18582.
54. Steger, D. J., A. Eberharter, S. John, P. A. Grant, and J. L. Workman. 1998. Purified histone acetyltransferases stimulate HIV-1 transcription from preassembled nucleosomal arrays. Proc. Natl. Acad. Sci. USA 95:12924-12929.
55. Sterner, D. E., P. A. Grant, S. M. Roberts, L. J. Duggan, R. Belotserkovskaya, L. A. Pacella, F. Winston, J. L. Workman, and S. L. Berger. 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.
56. Strahl, B. D., and C. D. Allis. 2000. The language of covalent histone modifications. Nature 403:41-45.
57. Struhl, K., and Z. Moqtaderi. 1998. The TAFs in the HAT. Cell 94:1-4.
58. Syntichaki, P., and G. Thireos. 1998. The Gcn5.Ada complex potentiates the histone acetyltransferase activity of Gcn5. J. Biol. Chem. 273:24414-24419.
59. Tse, C., T. Sera, A. P. Wolffe, and J. C. Hansen. 1998. Disruption of higherorder folding by core histone acetylation dramatically enhances transcription of nucleosomal arrays by RNA polymerase III. Mol. Cell. Biol. 18:4629-4638.
60. van den Berg, M. A., P. de Jong-Gubbels, and H. Y. Steensma. 1998. Transient mRNA responses in chemostat cultures as a method of defining putative regulatory elements: Application to genes involved in Saccharomyces cerevisiae acetyl-coenzyme A metabolism. Yeast 14:1089-1104.
61. 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.
62. Winston, F., C. Dollard, E. A. Malone, J. Clare, J. G. Kapakos, P. Farabaugh, and P. L. Minehart. 1987. Three genes are required for transactivation of Ty transcription in yeast. Genetics 115:649-656.
63. Winston, F., and P. Sudarsanam. 1998. The SAGA of Spt proteins and transcriptional analysis in yeast: Past, present, and future. Cold Spring Harbor Symp. Quant. Biol. 63:553-561.
64. Wu, P. Y., and F. Winston. 2002. Analysis of Spt7 function in the Saccharomyces cerevisiae SAGA coactivator complex. Mol. Cell. Biol. 22:5367-5379.
65. Zhang, W., J. R. Bone, D. G. Edmondson, B. M. Turner, and S. Y. Roth. 1998. Essential and redundant functions of histone acetylation revealed by mutation of target lysines and loss of the Gcn5p acetyltransferase. EMBO J. 17:3155-3167.