The STAGA subunit ADA2b Is an important regulator of human GCN5 catalysis

Molecular and Cellular Biology

Volumn 29, Issue 1, 2009, Pages 266-280

  Gamper, Armin M ^a   Kim, Jaehoon ^a   Roeder, Robert G ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL PROTEIN; HISTONE; HISTONE ACETYLTRANSFERASE GCN5; PROTEIN ADA2; PROTEIN ADA2A; PROTEIN ADA2B; PROTEIN ADA3; PROTEIN P53; PROTEIN STAGA; PROTEIN SUBUNIT; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; ADA2B PROTEIN, HUMAN; CARRIER PROTEIN; HISTONE ACETYLTRANSFERASE; HISTONE ACETYLTRANSFERASE PCAF; MULTIPROTEIN COMPLEX; P300-CBP-ASSOCIATED FACTOR; SIGNAL TRANSDUCING ADAPTOR PROTEIN; TADA2L PROTEIN, HUMAN; TADA3L PROTEIN, HUMAN;

ACETYLATION; ARTICLE; CHROMATIN; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME MECHANISM; HUMAN; HUMAN CELL; NUCLEOSOME; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN PROTEIN INTERACTION; AMINO ACID SEQUENCE; CATALYSIS; CHEMISTRY; ENZYME ACTIVE SITE; GENETICS; METABOLISM; MOLECULAR GENETICS; PROTEIN BINDING; PROTEIN TERTIARY STRUCTURE; TUMOR CELL LINE;

ACETYLATION; ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AMINO ACID SEQUENCE; CARRIER PROTEINS; CATALYSIS; CATALYTIC DOMAIN; CELL LINE, TUMOR; HISTONE ACETYLTRANSFERASES; HISTONES; HUMANS; MOLECULAR SEQUENCE DATA; MULTIPROTEIN COMPLEXES; NUCLEOSOMES; P300-CBP TRANSCRIPTION FACTORS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS; TRANSCRIPTION FACTORS; TUMOR SUPPRESSOR PROTEIN P53;

EID: 58149476940     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.00315-08     Document Type: Article

References (64)

1. An, W., J. Kim, and R. G. Roeder. 2004. Ordered cooperative functions of PRMT1, p300, and CARM1 in transcriptional activation by p53. Cell 117:735-748.
2. Aravind, L., and L. M. Iyer. 2002. The SWIRM domain: a conserved module found in chromosomal proteins points to novel chromatin-modifying activities. Genome Biol. 3:RESEARCH0039.
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. Barlev, N. A., A. V. Emelyanov, P. Castagnino, P. Zegerman, A. J. Bannister, M. A. Sepulveda, F. Robert, L. Tora, T. Kouzarides, B. K. Birshtein, and S. L. Berger. 2003. A novel human Ada2 homologue functions with Gcn5 or Brg1 to coactivate transcription. Mol. Cell. Biol. 23:6944-6957.
5. Barlev, N. A., L. Liu, N. H. Chehab, K. Mansfield, K. G. Harris, T. D. Halazonetis, and S. L. Berger. 2001. Acetylation of p53 activates transcription through recruitment of coactivators/histone acetyltransferases. Mol. Cell 8:1243-1254.
6. Black, J. C., J. E. Choi, S. R. Lombardo, and M. Carey. 2006. A mechanism for coordinating chromatin modification and preinitiation complex assembly. Mol. Cell 23:809-818.
7. Boyer, L. A., M. R. Langer, K. A. Crowley, S. Tan, J. M. Denu, and C. L. Peterson. 2002. Essential role for the SANT domain in the functioning of multiple chromatin remodeling enzymes. Mol. Cell 10:935-942.
8. Brand, M., J. G. Moggs, M. Oulad-Abdelghani, F. Lejeune, F. J. Dilworth, J. Stevenin, G. Almouzni, and L. Tora. 2001. UV-damaged DNA-binding protein in the TFTC complex links DNA damage recognition to nucleosome acetylation. EMBO J. 20:3187-3196.
9. 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.
10. Bu, P., Y. A. Evrard, G. Lozano, and S. Y. Dent. 2007. Loss of Gcn5 acetyltransferase activity leads to neural tube closure defects and exencephaly in mouse embryos. Mol. Cell. Biol. 27:3405-3416.
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. 271:5237-5245.
12. Candau, R., P. A. Moore, L. Wang, N. Barlev, C. Y. Ying, C. A. Rosen, and S. L. Berger. 1996. Identification of human proteins functionally conserved with the yeast putative adaptors ADA2 and GCN5. Mol. Cell. Biol. 16:593-602.
13. Chen, Y., Y. Yang, F. Wang, K. Wan, K. Yamane, Y. Zhang, and M. Lei. 2006. Crystal structure of human histone lysine-specific demethylase 1 (LSD1). Proc. Natl. Acad. Sci. USA 103:13956-13961.
14. Ciurciu, A., O. Komonyi, T. Pankotai, and I. M. Boros. 2006. The Drosophila histone acetyltransferase Gcn5 and transcriptional adaptor Ada2a are involved in nucleosomal histone H4 acetylation. Mol. Cell. Biol. 26:9413-9423.
15. Cote, J., R. T. Utley, and J. L. Workman. 1995. Basic analysis of transcription factor binding to nucleosomes. Methods Mol. Genet. 6:108-120.
16. Da, G., J. Lenkart, K. Zhao, R. Shiekhattar, B. R. Cairns, and R. Marmorstein. 2006. Structure and function of the SWIRM domain, a conserved protein module found in chromatin regulatory complexes. Proc. Natl. Acad. Sci. USA 103:2057-2062.
17. Dignam, J. D., R. M. Lebovitz, and R. G. Roeder. 1983. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 11:1475-1489.
18. 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.
19. el-Deiry, W. S., T. Tokino, T. Waldman, J. D. Oliner, V. E. Velculescu, M. Burrell, D. E. Hill, E. Healy, J. L. Rees, S. R. Hamilton, et al. 1995. Topological control of p21WAF1/CIP1 expression in normal and neoplastic tissues. Cancer Res. 55:2910-2919.
20. Espinosa, J. M., and B. M. Emerson. 2001. Transcriptional regulationbyp53 through intrinsic DNA/chromatin binding and site-directed cofactor recruitment. Mol. Cell 8:57-69.
21. Fuchs, M., J. Gerber, R. Drapkin, S. Sif, T. Ikura, V. Ogryzko, W. S. Lane, Y. Nakatani, and D. M. Livingston. 2001. The p400 complex is an essential E1A transformation target. Cell 106:297-307.
22. Gamper, A. M., and R. G. Roeder. 2008. Multivalent binding of p53 to the STAGA complex mediates coactivator recruitment after UV damage. Mol. Cell. Biol. 28:2517-2527.
23. Grant, P. A., L. Duggan, J. Cote, 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.
24. Grau, B., C. Popescu, L. Torroja, D. Ortuno-Sahagun, I. Boros, and A. Ferrus. 2008. Transcriptional adaptor ADA3 of Drosophila melanogaster is required for histone modification, position effect variegation, and transcription. Mol. Cell. Biol. 28:376-385.
25. Gu, W., and R. G. Roeder. 1997. Activation of p53 sequence-specific DNA binding by acetylation of the p53 C-terminal domain. Cell 90:595-606.
26. Guelman, S., T. Suganuma, L. Florens, S. K. Swanson, C. L. Kiesecker, T. Kusch, S. Anderson, J. R. Yates III, M. P. Washburn, S. M. Abmayr, and J. L. Workman. 2006. Host cell factor and an uncharacterized SANT domain protein are stable components of ATAC, a novel dAda2A/dGcn5-containing histone acetyltransferase complex in Drosophila. Mol. Cell. Biol. 26:871-882.
27. Hakimi, M. A., Y. Dong, W. S. Lane, D. W. Speicher, and R. Shiekhattar. 2003. A candidate X-linked mental retardation gene is a component of a new family of histone deacetylase-containing complexes. J. Biol. Chem. 278:7234-7239.
28. Herrera, J. E., K. L. West, R. L. Schiltz, Y. Nakatani, and M. Bustin. 2000. Histone H1 is a specific repressor of core histone acetylation in chromatin. Mol. Cell. Biol. 20:523-529.
29. 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.
30. Ikura, T., V. V. Ogryzko, M. Grigoriev, R. Groisman, J. Wang, M. Horikoshi, R. Scully, J. Qin, and Y. Nakatani. 2000. Involvement of the TIP60 histone acetylase complex in DNA repair and apoptosis. Cell 102:463-473.
31. Karanam, B., L. Wang, D. Wang, X. Liu, R. Marmorstein, R. Cotter, and P. A. Cole. 2007. Multiple roles for acetylation in the interaction of p300 HAT with ATF-2. Biochemistry 46:8207-8216.
32. Kastan, M. B., Q. Zhan, W. S. el-Deiry, F. Carrier, T. Jacks, W. V. Walsh, B. S. Plunkett, B. Vogelstein, and A. J. Fornace, Jr. 1992. A mammalian cell cycle checkpoint pathway utilizing p53 and GADD45 is defective in ataxia-telangiectasia. Cell 71:587-597.
33. Kouzarides, T. 2007. Chromatin modifications and their function. Cell 128:693-705.
34. Kusch, T., S. Guelman, S. M. Abmayr, and J. L. Workman. 2003. Two Drosophila Ada2 homologues function in different multiprotein complexes. Mol. Cell. Biol. 23:3305-3319.
35. Langer, M. R., K. G. Tanner, and J. M. Denu. 2001. Mutational analysis of conserved residues in the GCN5 family of histone acetyltransferases. J. Biol. Chem. 276:31321-31331.
36. Lee, K. K., and J. L. Workman. 2007. Histone acetyltransferase complexes: one size doesn't fit all. Nat. Rev. Mol. Cell Biol. 8:284-295.
37. Li, B., M. Carey, and J. L. Workman. 2007. The role of chromatin during transcription. Cell 128:707-719.
38. Liu, X., M. Vorontchikhina, Y. L. Wang, F. Faiola, and E. Martinez. 2008. STAGA recruits Mediator to the MYC oncoprotein to stimulate transcription and cell proliferation. Mol. Cell. Biol. 28:108-121.
39. Martinez, E., T. K. Kundu, J. Fu, and R. G. Roeder. 1998. A human SPT3-TAFII31-GCN5-L acetylase complex distinct from transcription factor IID. J. Biol. Chem. 273:23781-23785.
40. Martinez, E., V. B. Palhan, A. Tjernberg, E. S. Lymar, A. M. Gamper, T. K. Kundu, B. T. Chait, and R. G. Roeder. 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.
41. McKay, B. C., F. Chen, S. T. Clarke, H. E. Wiggin, L. M. Harley, and M. Ljungman. 2001. UV light-induced degradation of RNA polymerase II is dependent on the Cockayne's syndrome A and B proteins but not p53 or MLH1. Mutat. Res. 485:93-105.
42. 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.
43. Pankotai, T., O. Komonyi, L. Bodai, Z. Ujfaludi, S. Muratoglu, A. Ciurciu, L. Tora, J. Szabad, and I. Boros. 2005. The homologous Drosophila transcriptional adaptors ADA2a and ADA2b are both required for normal development but have different functions. Mol. Cell. Biol. 25:8215-8227.
44. Park, J. H., and R. G. Roeder. 2006. GAS41 is required for repression of the p53 tumor suppressor pathway during normal cellular proliferation. Mol. Cell. Biol. 26:4006-4016.
45. Qian, C., Q. Zhang, S. Li, L. Zeng, M. J. Walsh, and M. M. Zhou. 2005. Structure and chromosomal DNA binding of the SWIRM domain. Nat. Struct. Mol. Biol. 12:1078-1085.
46. Sadowski, H. B., and M. Z. Gilman. 1993. Cell-free activation of a DNA-binding protein by epidermal growth factor. Nature 362:79-83.
47. Shi, Y., F. Lan, C. Matson, P. Mulligan, J. R. Whetstine, P. A. Cole, R. A. Casero, and Y. Shi. 2004. Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 119:941-953.
48. Shukla, A., P. Bajwa, and S. R. Bhaumik. 2006. 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.
49. Stavropoulos, P., G. Blobel, and A. Hoelz. 2006. Crystal structure and mechanism of human lysine-specific demethylase-1. Nat. Struct. Mol. Biol. 13:626-632.
50. Sterner, D. E., X. Wang, M. H. Bloom, G. M. Simon, and S. L. Berger. 2002. The SANT domain of Ada2 is required for normal acetylation of histones by the yeast SAGA complex. J. Biol. Chem. 277:8178-8186.
51. Suganuma, T., J. L. Gutierrez, B. Li, L. Florens, S. K. Swanson, M. P. Washburn, S. M. Abmayr, and J. L. Workman. 2008. ATAC is a double histone acetyltransferase complex that stimulates nucleosome sliding. Nat. Struct. Mol. Biol. 15:364-372.
52. Tochio, N., T. Umehara, S. Koshiba, M. Inoue, T. Yabuki, M. Aoki, E. Seki, S. Watanabe, Y. Tomo, M. Hanada, M. Ikari, M. Sato, T. Terada, T. Nagase, O. Ohara, M. Shirouzu, A. Tanaka, T. Kigawa, and S. Yokoyama. 2006. Solution structure of the SWIRM domain of human histone demethylase LSD1. Structure 14:457-468.
53. Tremethick, D. J. 2007. Higher-order structures of chromatin: the elusive 30 nm fiber. Cell 128:651-654.
54. Vassilev, A., J. Yamauchi, T. Kotani, C. Prives, M. L. Avantaggiati, J. Qin, and Y. Nakatani. 1998. The 400 kDa subunit of the PCAF histone acetylase complex belongs to the ATM superfamily. Mol. Cell 2:869-875.
55. Wang, W., Y. Xue, S. Zhou, A. Kuo, B. R. Cairns, and G. R. Crabtree. 1996. Diversity and specialization of mammalian SWI/SNF complexes. Genes Dev. 10:2117-2130.
56. Wieczorek, E., M. Brand, X. Jacq, and L. Tora. 1998. Function of TAF(II)-containing complex without TBP in transcription by RNA polymerase II. Nature 393:187-191.
57. Xu, W., D. G. Edmondson, Y. A. Evrard, M. Wakamiya, R. R. Behringer, and S. Y. Roth. 2000. Loss of Gcn512 leads to increased apoptosis and mesodermal defects during mouse development. Nat. Genet. 26:229-232.
58. Xu, W., D. G. Edmondson, and S. Y. Roth. 1998. Mammalian GCN5 and P/CAF acetyltransferases have homologous amino-terminal domains important for recognition of nucleosomal substrates. Mol. Cell. Biol. 18:5659-5669.
59. Yamauchi, T., J. Yamauchi, T. Kuwata, T. Tamura, T. Yamashita, N. Bae, H. Westphal, K. Ozato, and Y. Nakatani. 2000. Distinct but overlapping roles of histone acetylase PCAF and of the closely related PCAF-B/GCN5 in mouse embryogenesis. Proc. Natl. Acad. Sci. USA 97:11303-11306.
60. 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 oncoprotein E1A. Nature 382:319-324.
61. Yoneyama, M., N. Tochio, T. Umehara, S. Koshiba, M. Inoue, T. Yabuki, M. Aoki, E. Seki, T. Matsuda, S. Watanabe, Y. Tomo, Y. Nishimura, T. Harada, T. Terada, M. Shirouzu, Y. Hayashizaki, O. Ohara, A. Tanaka, T. Kigawa, and S. Yokoyama. 2007. Structural and functional differences of SWIRM domain subtypes. J. Mol. Biol. 369:222-238.
62. Zhang, X. Y., M. Varthi, S. M. Sykes, C. Phillips, C. Warzecha, W. Zhu, A. Wyce, A. W. Thorne, S. L. Berger, and S. B. McMahon. 2008. The putative cancer stem cell marker USP22 is a subunit of the human SAGA complex required for activated transcription and cell-cycle progression. Mol. Cell 29:102-111.
63. Zhao, Y., G. Lang, S. Ito, J. Bonnet, E. Metzger, S. Sawatsubashi, E. Suzuki, X. Le Guezennec, H. G. Stunnenberg, A. Krasnov, S. G. Georgieva, R. Schule, K. Takeyama, S. Kato, L. Tora, and D. Devys. 2008. A TFTC/STAGA module mediates histone H2A and H2B deubiquitination, coactivates nuclear receptors, and counteracts heterochromatin silencing. Mol. Cell 29:92-101.
64. Zhu, P., W. Zhou, J. Wang, J. Puc, K. A. Ohgi, H. Erdjument-Bromage, P. Tempst, C. K. Glass, and M. G. Rosenfeld. 2007. A histone H2A deubiquitinase complex coordinating histone acetylation and H1 dissociation in transcriptional regulation. Mol. Cell 27:609-621.