The essential gene wda encodes a WD40 repeat subunit of Drosophila SAGA required for histone H3 acetylation

Molecular and Cellular Biology

Volumn 26, Issue 19, 2006, Pages 7178-7189

  Guelman, Sebastián ^a   Suganuma, Tamaki ^a   Florens, Laurence ^a   Weake, Vikki ^a   Swanson, Selene K ^a   Washburn, Michael P ^a   Abmayr, Susan M ^a   Workman, Jerry L ^a  

^a STOWERS INSTITUTE FOR MEDICAL RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DROSOPHILA PROTEIN; HISTONE ACETYLTRANSFERASE; HISTONE ACETYLTRANSFERASE GCN5; HISTONE H3; PROTEIN ADA2; PROTEIN ADA3; PROTEIN SPT3; PROTEIN SUBUNIT; PROTEIN TRA1; PROTEIN WDA; TRANSCRIPTION FACTOR SAGA; UNCLASSIFIED DRUG;

ACETYLATION; ALLELE; ARTICLE; CELL DIFFERENTIATION; CHROMATIN STRUCTURE; CONTROLLED STUDY; DEVELOPMENT; DROSOPHILA MELANOGASTER; ESSENTIAL GENE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN FUNCTION; PROTEOMICS; SACCHAROMYCES CEREVISIAE; TRANSCRIPTION REGULATION; TRANSCRIPTION REPRESSION; WDA GENE;

ACETYLATION; AMINO ACID SEQUENCE; ANIMALS; CHROMATOGRAPHY, AFFINITY; CONSERVED SEQUENCE; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EMBRYO, NONMAMMALIAN; GENE DELETION; GENES, ESSENTIAL; GENES, INSECT; HISTONE ACETYLTRANSFERASES; HISTONES; HOMOZYGOTE; MULTIPROTEIN COMPLEXES; PROTEIN BINDING; PROTEIN SUBUNITS; REPETITIVE SEQUENCES, AMINO ACID; TRANS-ACTIVATORS;

DROSOPHILA MELANOGASTER; EUKARYOTA; MAMMALIA; SACCHAROMYCES CEREVISIAE;

EID: 33749182474     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.00130-06     Document Type: Article

References (59)

1. 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.
2. Birck, C., O. Poch, C. Romier, M. Ruff, G. Mengus, A. C. Lavigne, I. Davidson, and D. Moras. 1998. Human TAF(II)28 and TAF(II)18 interact through a histone fold encoded by atypical evolutionary conserved motifs also found in the SPT3 family. Cell 94:239-249.
3. Brand, A. H., and N. Perrimon. 1993. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118:401-415.
4. 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.
5. 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.
6. 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.
7. Candido, E. P., R. Reeves, and J. R. Davie. 1978. Sodium butyrate inhibits histone deacetylation in cultured cells. Cell 14:105-113.
8. Carre, C., D. Szymczak, J. Pidoux, and C. Antoniewski. 2005. The histone H3 acetylase dGcn5 is a key player in Drosophila melanogaster metamorphosis. Mol. Cell. Biol. 25:8228-8238.
9. Carrozza, M. J., R. T. Utley, J. L. Workman, and J. Cote. 2003. The diverse functions of histone acetyltransferase complexes. Trends Genet. 19:321-329.
10. Celniker, S. E., and G. M. Rubin. 2003. The Drosophila melanogaster genome. Annu. Rev. Genomics Hum. Genet. 4:89-117.
11. Celniker, S. E., D. A. Wheeler, B. Kronmiller, J. W. Carlson, A. Halpern, S. Patel, M. Adams, M. Champe, S. P. Dugan, E. Frise, A. Hodgson, R. A. George, R. A. Hoskins, T. Laverty, D. M. Muzny, C. R. Nelson, J. M. Pacleb, S. Park, B. D. Pfeiffer, S. Richards, E. J. Sodergren, R. Svirskas, P. E. Tabor, K. Wan, M. Stapleton, G. G. Sutton, C. Venter, G. Weinstock, S. E. Scherer, E. W. Myers, R. A. Gibbs, and G. M. Rubin. 2002. Finishing a whole-genome shotgun: release 3 of the Drosophila melanogaster euchromatic genome sequence. Genome Biol. 3:RESEARCH0079.
12. Chen, G., and A. J. Courey. 2000. Groucho/TLE family proteins and transcriptional repression. Gene 249:1-16.
13. Cheng, H., X. He, and C. Moore. 2004. The essential WD repeat protein Swd2 has dual functions in RNA polymerase II transcription termination and lysine 4 methylation of histone H3. Mol. Cell. Biol. 24:2932-2943.
14. Durso, R. J., A. K. Fisher, T. J. Albright-Frey, and J. C. Reese. 2001. Analysis of TAF90 mutants displaying allele-specific and broad defects in transcription. Mol. Cell. Biol. 21:7331-7344.
15. Eberharter, A., S. John, P. A. Grant, R. T. Utley, and J. L. Workman. 1998. Identification and analysis of yeast nucleosomal histone acetyltransferasc complexes. Methods 15:315-321.
16. Fischle, W., Y. Wang, and C. D. Allis. 2003. Histone and chromatin cross-talk. Curr. Opin. Cell Biol. 15:172-183.
17. Furlong, E. E., D. Profitt, and M. P. Scott. 2001. Automated sorting of live transgenic embryos. Nat. Biotechnol. 19:153-156.
18. Gangloff, Y. G., C. Romier, S. Thuault, S. Werten, and I. Davidson. 2001. The histone fold is a key structural motif of transcription factor TFIID. Trends Biochem. Sci. 26:250-257.
19. Gangloff, Y. G., S. L. Sanders, C. Romier, D. Kirschner, P. A. Weil, L. Tora, and I. Davidson. 2001. Histone folds mediate selective heterodimerization of yeast TAF(II)25 with TFIID components yTAF(II)47 and yTAF(II)65 and with SAGA component ySPT7. Mol. Cell. Biol. 21:1841-1853.
20. Gangloff, Y. G., S. Werten, C. Romier, L. Carre, O. Poch, D. Moras, and I. Davidson. 2000. The human TFIID components TAF(II)135 and TAF(II)20 and the yeast SAGA components ADA1 and TAF(II)68 heterodimerize to form histone-like pairs. Mol. Cell. Biol. 20:340-351.
21. Garcia-Higuera, I., J. Fenoglio, Y. Li, C. Lewis, M. P. Panchenko, O. Reiner, T. F. Smith, and E. J. Neer. 1996. Folding of proteins with WD-repeats: comparison of six members of the WD-repeat superfamily to the G protein beta subunit. Biochemistry 35:13985-13994.
22. 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.
23. 11s are integral components of the SAGA complex required for nucleosome acetylation and transcriptional stimulation. Cell 94:45-53.
24. Grant, P. A., D. Schieltz, M. G. Pray-Grant, J. R. Yates III, and J. L. Workman. 1998. The ATM-related cofactor Tra1 is a component of the purified SAGA complex. Mol. Cell 2:863-867.
25. 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.
26. Hiller, M. A., T. Y. Lin, C. Wood, and M. T. Fuller. 2001. Developmental regulation of transcription by a tissue-specific TAF homolog. Genes Dev. 15:1021-1030.
27. Hollmann, M., E. Simmerl, U. Schafer, and M. A. Schafer. 2002. The essential Drosophila melanogaster gene wds (will die slowly) codes for a WD-repeat protein with seven repeats. Mol. Genet. Genomics 268:425-433.
28. Ikeda, K., D. J. Steger, A. Eberharter, and J. L. Workman. 1999. Activation domain-specific and general transcription stimulation by native histone acetyltransferase complexes. Mol. Cell. Biol. 19:855-863.
29. Keller, C. A., M. A. Grill, and S. M. Abmayr. 1998. A role for nautilus in the differentiation of muscle precursors. Dev. Biol. 202:157-171.
30. Khorasanizadeh, S. 2004. The nucleosome: from genomic organization to genomic regulation. Cell 116:259-272.
31. 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.
32. Lee, K. K., L. Florens, S. K. Swanson, M. P. Washburn, and J. L. Workman. 2005. The deubiquitylation activity of Ubp8 is dependent upon Sgf11 and its association with the SAGA complex. Mol. Cell. Biol. 25:1173-1182.
33. 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.
34. Li, D., and R. Roberts. 2001. WD-repeat proteins: structure characteristics, biological function, and their involvement in human diseases. Cell. Mol. Life Sci. 58:2085-2097.
35. 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.
36. Martinez-Balbas, M. A., T. Tsukiyama, D. Gdula, and C. Wu. 1998. Drosophila NURF-55, a WD repeat protein involved in histone metabolism. Proc. Natl. Acad. Sci. USA 95:132-137.
37. McMahon, S. J., M. G. Pray-Grant, D. Schieltz, J. R. Yates III, and P. A. Grant. 2005. Polyglutamine-expanded spinocerebellar ataxia-7 protein disrupts normal SAGA and SLIK histone acetyltransferase activity. Proc. Natl. Acad. Sci. USA 102:8478-8482.
38. Noland, B. J., J. M. Hardin, and G. R. Shepherd. 1971. Histone acetyltransferase activity in synchronized mammalian cells. Biochim. Biophys. Acta 246:263-268.
39. Ogryzko, V. V., T. Kotani, X. Zhang, R. L. Schlitz, 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.
40. Palhan, V. B., S. Chen, G. H. Peng, A. Tjernberg, A. M. Gamper, Y. Fan, B. T. Chait, A. R. La Spada, and R. G. Roeder. 2005. Polyglutamine-expanded ataxin-7 inhibits STAGA histone acetyltransferase activity to produce retinal degeneration. Proc. Natl. Acad. Sci. USA 102:8472-8477.
41. 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.
42. 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.
43. Powell, D. W., C. M. Weaver, J. L. Jennings, K. J. McAfee, Y. He, P. A. Weil, and A. J. Link. 2004. Cluster analysis of mass spectrometry data reveals a novel component of SAGA. Mol. Cell. Biol. 24:7249-7259.
44. Qi, D., J. Larsson, and M. Mannervik. 2004. Drosophila Ada2b is required for viability and normal histone H3 acetylation. Mol. Cell. Biol. 24:8080-8089.
45. Rorth, P. 1998. Gal4 in the Drosophila female germline. Mech. Dev. 78:113-118.
46. Sanders, S. L., J. Jennings, A. Canutescu, A. J. Link, and P. A. Weil. 2002. Proteomics of the eukaryotic transcription machinery: identification of proteins associated with components of yeast TFIID by multidimensional mass spectrometry. Mol. Cell. Biol. 22:4723-4738.
47. Selleck, W., R. Howley, Q. Fang, V. Podolny, M. G. Fried, S. Buratowski, and S. Tan. 2001. A histone fold TAF octamer within the yeast TFIID transcriptional coactivator. Nat. Struct. Biol. 8:695-700.
48. 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.
49. Smith, E. R., A. Pannuti, W. Gu, A. Steurnagel, R. G. Cook, C. D. Allis, and J. C. Lucchesi. 2000. The Drosophila MSL complex acetylates histone H4 at lysine 16, a chromatin modification linked to dosage compensation. Mol. Cell. Biol. 20:312-318.
50. Smith, T. F., C. Gaitatzes, K. Saxena, and E. J. Neer. 1999. The WD repeat: a common architecture for diverse functions. Trends Biochem. Sci. 24:181-185.
51. Sterner, D. E., and S. L. Berger. 2000. Acetylation of histones and transcription-related factors. Microbiol. Mol. Biol. Rev. 64:435-459.
52. 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.
53. Strahl, B. D., and C. D. Allis. 2000. The language of covalent histone modifications. Nature 403:41-45.
54. 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.
55. Vlachonasios, K. E., M. F. Thomashow, and S. J. Triezenberg. 2003. Disruption mutations of ADA2b and GCN5 transcriptional adaptor genes dramatically affect Arabidopsis growth, development, and gene expression. Plant Cell. 15:626-638.
56. Wang, L., C. Mizzen, C. Ying, R. Candau, N. Barlev, J. Brownell, C. D. Allis, and S. L. Berger. 1997. Histone acetyltransferase activity is conserved between yeast and human GCN5 and is required for complementation of growth and transcriptional activation. Mol. Cell. Biol. 17:519-527.
57. Wu, P. Y., C. Ruhlmann, F. Winston, and P. Schultz. 2004. Molecular architecture of the S. cerevisiae SAGA complex. Mol. Cell 15:199-208.
58. Wysocka, J., T. Swigut, T. A. Milne, Y. Dou, X. Zhang, A. L. Burlingame, R. G. Roeder, A. H. Brivanlou, and C. D. Allis. 2005. WDR5 associates with histone H3 methylated at K4 and is essential for H3 K4 methylation and vertebrate development. Cell 121:859-872.
59. 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.