TFIID TAF6-TAF9 complex formation involves the HEAT repeat-containing C-terminal domain of TAF6 and is modulated by TAF5 protein

Journal of Biological Chemistry

Volumn 287, Issue 33, 2012, Pages 27580-27592

  Scheer, Elisabeth ^a   Delbac, Frédéric ^b   Tora, Laszlo ^a   Moras, Dino ^a   Romier, Christophe ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b UNIVERSITÉ CLERMONT AUVERGNE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

C-TERMINAL DOMAINS; C-TERMINAL REGIONS; COMPLEX FORMATIONS; CORE PROMOTERS; HELA CELL; HETERODIMERIZATION; PREINITIATION COMPLEX; RNA POLYMERASE II; TRANSCRIPTION START SITE; TWO DOMAINS;

GENES; RNA; TRANSCRIPTION FACTORS;

TRANSCRIPTION;

HISTONE; TATA BINDING PROTEIN ASSOCIATED FACTOR; TATA BINDING PROTEIN ASSOCIATED FACTOR 5; TATA BINDING PROTEIN ASSOCIATED FACTOR 6; TATA BINDING PROTEIN ASSOCIATED FACTOR 9; TRANSCRIPTION FACTOR IID; UNCLASSIFIED DRUG;

ANTONOSPORA LOCUSTAE; ARTICLE; CARBOXY TERMINAL SEQUENCE; COMPLEX FORMATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; CRYSTALLIZATION; HELA CELL; HUMAN; IMMUNOPRECIPITATION; MOLECULAR CLONING; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN MOTIF; PROTEIN PURIFICATION; PROTOZOON; SEQUENCE ALIGNMENT; WESTERN BLOTTING;

HELA CELLS; HUMANS; MULTIPROTEIN COMPLEXES; MUTATION; PROTEIN STRUCTURE, TERTIARY; REPETITIVE SEQUENCES, AMINO ACID; TATA-BINDING PROTEIN ASSOCIATED FACTORS; TRANSCRIPTION FACTOR TFIID;

EID: 84864975153     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.379206     Document Type: Article

References (55)

1. Roeder, R. G. (1996) The role of general initiation factors in transcription by RNA polymerase II. Trends Biochem. Sci. 21, 327-335
2. Thomas, M. C., and Chiang, C. M. (2006) The general transcription machinery and general cofactors. Crit. Rev. Biochem. Mol. Biol. 41, 105-178
3. Burley, S. K., and Roeder, R. G. (1996) Biochemistry and structural biology of transcription factor IID (TFIID). Annu. Rev. Biochem. 65, 769-799
4. Cler, E., Papai, G., Schultz, P., and Davidson, I. (2009) Recent advances in understanding the structure and function of general transcription factor TFIID. Cell. Mol. Life Sci. 66, 2123-2134
5. Juven-Gershon, T., Hsu, J. Y., Theisen, J. W., and Kadonaga, J. T. (2008) The RNA polymerase II core promoter: the gateway to transcription. Curr. Opin. Cell Biol. 20, 253-259
6. Jacobson, R. H., Ladurner, A. G., King, D. S., and Tjian, R. (2000) Structure and function of a human TAFII250 double bromodomain module. Science 288, 1422-1425
7. Vermeulen, M., Mulder, K. W., Denissov, S., Pijnappel, W. W., van Schaik, F. M., Varier, R. A., Baltissen, M. P., Stunnenberg, H. G., Mann, M., and Timmers, H. T. (2007) Selective anchoring of TFIID to nucleosomes by trimethylation of histone H3 lysine 4. Cell 131, 58-69
8. Papai, G., Tripathi, M. K., Ruhlmann, C., Layer, J. H., Weil, P. A., and Schultz, P. (2010) TFIIA and the transactivator Rap1 cooperate to commit TFIID for transcription initiation. Nature 465, 956-960
9. Birck, C., Poch, O., Romier, C., Ruff, M., Mengus, G., Lavigne, A. C., Davidson, I., and Moras, D. (1998) Human TAFII28 and TAFII18 interact through a histone fold encoded by atypical evolutionary conserved motifs also found in the SPT3 family. Cell 94, 239-249
10. Lavigne, A. C., Gangloff, Y. G., Carré, L., Mengus, G., Birck, C., Poch, O., Romier, C., Moras, D., and Davidson, I. (1999) Synergistic transcriptional activation by TATA-binding protein and hTAFII28 requires specific amino acids of the hTAFII28 histone fold. Mol. Cell. Biol. 19, 5050-5060
11. Gangloff, Y. G., Pointud, J. C., Thuault, S., Carré, L., Romier, C., Muratoglu, S., Brand, M., Tora, L., Couderc, J. L., and Davidson, I. (2001) The TFIID components human TAFII140 and Drosophila BIP2 (TAFII155) are novel metazoan homologues of yeast TAFII47 containing a histone fold and a PHD finger. Mol. Cell. Biol. 21, 5109-5121
12. Gangloff, Y. G., Romier, C., Thuault, S., Werten, S., and Davidson, I. (2001) The histone fold is a key structural motif of transcription factor TFIID. Trends Biochem. Sci. 26, 250-257
13. Gangloff, Y. G., Sanders, S. L., Romier, C., Kirschner, D., Weil, P. A., Tora, L., and Davidson, I. (2001) Histone folds mediate selective heterodimerization of yeast TAFII25 with TFIID components yTAFII47 and yTAFII65 and with SAGA component ySPT7. Mol. Cell. Biol. 21, 1841-1853
14. Gangloff, Y. G., Werten, S., Romier, C., Carré, L., Poch, O., Moras, D., and Davidson, I. (2000) The human TFIID components TAFII135 and TAFII20 and the yeast SAGA components ADA1 and TAFII68 heterodimerize to form histone-like pairs. Mol. Cell. Biol. 20, 340-351
15. Werten, S., Mitschler, A., Romier, C., Gangloff, Y. G., Thuault, S., Davidson, I., and Moras, D. (2002) Crystal structure of a subcomplex of human transcription factor TFIID formed by TATA binding protein-associated factors hTAF4 (hTAFII135) and hTAF12 (hTAFII20). J. Biol. Chem. 277, 45502-45509
16. Thuault, S., Gangloff, Y. G., Kirchner, J., Sanders, S., Werten, S., Romier, C., Weil, P. A., and Davidson, I. (2002) Functional analysis of the TFIID-specific yeast TAF4 (yTAFII48) reveals an unexpected organization of its histone-fold domain. J. Biol. Chem. 277, 45510-45517
17. Xie, X., Kokubo, T., Cohen, S. L., Mirza, U. A., Hoffmann, A., Chait, B. T., Roeder, R. G., Nakatani, Y., and Burley, S. K. (1996) Structural similarity between TAFs and the heterotetrameric core of the histone octamer. Nature 380, 316-322
18. Hoffmann, A., Chiang, C. M., Oelgeschläger, T., Xie, X., Burley, S. K., Nakatani, Y., and Roeder, R. G. (1996) A histone octamer-like structure within TFIID. Nature 380, 356-359
19. Selleck, W., Howley, R., Fang, Q., Podolny, V., Fried, M. G., Buratowski, S., and Tan, S. (2001) A histone fold TAF octamer within the yeast TFIID transcriptional coactivator. Nat. Struct. Biol. 8, 695-700
20. Leurent, C., Sanders, S., Ruhlmann, C., Mallouh, V., Weil, P. A., Kirschner, D. B., Tora, L., and Schultz, P. (2002) Mapping histone fold TAFs within yeast TFIID. EMBO J. 21, 3424-3433
21. Sanders, S. L., Garbett, K. A., and Weil, P. A. (2002) Molecular characterization of Saccharomyces cerevisiae TFIID. Mol. Cell. Biol. 22, 6000-6013
22. Leurent, C., Sanders, S. L., Demény, M. A., Garbett, K. A., Ruhlmann, C., Weil, P. A., Tora, L., and Schultz, P. (2004) Mapping key functional sites within yeast TFIID. EMBO J. 23, 719-727
23. Demény, M. A., Soutoglou, E., Nagy, Z., Scheer, E., Jànoshàzi, A., Richardot, M., Argentini, M., Kessler, P., and Tora, L. (2007) Identification of a small TAF complex and its role in the assembly of TAF-containing complexes. PLoS One 2, e316
24. Grant, P. A., Schieltz, D., Pray-Grant, M. G., Steger, D. J., Reese, J. C., Yates, J. R., 3rd, and Workman, J. L. (1998) A subset of TAFIIs are integral components of the SAGA complex required for nucleosome acetylation and transcriptional stimulation. Cell 94, 45-53
25. Nagy, Z., and Tora, L. (2007) Distinct GCN5/PCAF-containing complexes function as co-activators and are involved in transcription factor and global histone acetylation. Oncogene 26, 5341-5357
26. Wright, K. J., Marr, M. T., 2nd, and Tjian, R. (2006) TAF4 nucleates a core subcomplex of TFIID and mediates activated transcription from a TATA-less promoter. Proc. Natl. Acad. Sci. U.S.A. 103, 12347-12352
27. Bell, B., Scheer, E., and Tora, L. (2001) Identification of hTAFII80δ links apoptotic signaling pathways to transcription factor TFIID function. Mol. Cell 8, 591-600
28. Diebold, M. L., Fribourg, S., Koch, M., Metzger, T., and Romier, C. (2011) Deciphering correct strategies for multiprotein complex assembly by coexpression: application to complexes as large as the histone octamer. J. Struct. Biol. 175, 178-188
29. Otwinowski, Z., and Minor, W. (1997) Processing of x-ray diffraction data collected in oscillation mode. Method Enzymol. 276, 307-326
30. Weeks, C. M., and Miller, R. (1999) The design and implementation of SnB v2.0. J. Appl. Crystallogr. 32, 120-124
31. Vonrhein, C., Blanc, E., Roversi, P., and Bricogne, G. (2007) Automated structure solution with autoSHARP. Methods Mol. Biol. 364, 215-230
32. Abrahams, J. P., and Leslie, A. G. (1996) Methods used in the structure determination of bovine mitochondrial F1-ATPase. Acta Crystallogr. D Biol. Crystallogr. 52, 30-42
33. Langer, G., Cohen, S. X., Lamzin, V. S., and Perrakis, A. (2008) Automated macromolecular model building for x-ray crystallography using ARP/wARP version 7. Nat. Protoc. 3, 1171-1179
34. Emsley, P., and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132
35. Collaborative Computational Project, Number 4 (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50, 760-763
36. Blanc, E., Roversi, P., Vonrhein, C., Flensburg, C., Lea, S. M., and Bricogne, G. (2004) Refinement of severely incomplete structures with maximum likelihood in BUSTER-TNT. Acta Crystallogr. D Biol. Crystallogr. 60, 2210-2221
37. Sali, A., Potterton, L., Yuan, F., van Vlijmen, H., and Karplus, M. (1995) Evaluation of comparative protein modeling by MODELLER. Proteins 23, 318-326
38. Dubrovskaya, V., Lavigne, A. C., Davidson, I., Acker, J., Staub, A., and Tora, L. (1996) Distinct domains of hTAFII100 are required for functional interaction with transcription factor TFIIF β (RAP30) and incorporation into the TFIID complex. EMBO J. 15, 3702-3712
39. Frontini, M., Soutoglou, E., Argentini, M., Bole-Feysot, C., Jost, B., Scheer, E., and Tora, L. (2005) TAF9b (formerly TAF9L) is a bona fide TAF that has unique and overlapping roles with TAF9. Mol. Cell. Biol. 25, 4638-4649
40. Hisatake, K., Ohta, T., Takada, R., Guermah, M., Horikoshi, M., Nakatani, Y., and Roeder, R. G. (1995) Evolutionary conservation of human TATA-binding-polypeptide-associated factors TAFII31 and TAFII80 and interactions of TAFII80 with other TAFs and with general transcription factors. Proc. Natl. Acad. Sci. U.S.A. 92, 8195-8199
41. Kokubo, T., Gong, D. W., Wootton, J. C., Horikoshi, M., Roeder, R. G., and Nakatani, Y. (1994) Molecular cloning of Drosophila TFIID subunits. Nature 367, 484-487
42. Weinzierl, R. O., Ruppert, S., Dynlacht, B. D., Tanese, N., and Tjian, R. (1993) Cloning and expression of Drosophila TAFII60 and human TAFII70 reveal conserved interactions with other subunits of TFIID. EMBO J. 12, 5303-5309
43. Katinka, M. D., Duprat, S., Cornillot, E., Méténier, G., Thomarat, F., Prensier, G., Barbe, V., Peyretaillade, E., Brottier, P., Wincker, P., Delbac, F., El Alaoui, H., Peyret, P., Saurin, W., Gouy, M., Weissenbach, J., and Vivarès, C. P. (2001) Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi. Nature 414, 450-453
44. Diebold, M. L., Koch, M., Loeliger, E., Cura, V., Winston, F., Cavarelli, J., and Romier, C. (2010) The structure of an Iws1/Spt6 complex reveals an interaction domain conserved in TFIIS, Elongin A, and Med26. EMBO J. 29, 3979-3991
45. Diebold, M. L., Loeliger, E., Koch, M., Winston, F., Cavarelli, J., and Romier, C. (2010) Noncanonical tandem SH2 enables interaction of elongation factor Spt6 with RNA polymerase II. J. Biol. Chem. 285, 38389-38398
46. Romier, C., James, N., Birck, C., Cavarelli, J., Vivarès, C., Collart, M. A., and Moras, D. (2007) Crystal structure, biochemical, and genetic characterization of yeast and E. cuniculi TAFII5 N-terminal domain: implications for TFIID assembly. J. Mol. Biol. 368, 1292-1306
47. Andrade, M. A., Petosa, C., O'Donoghue, S. I., Müller, C. W., and Bork, P. (2001) Comparison of ARM and HEAT protein repeats. J. Mol. Biol. 309, 1-18
48. Zhou, J., Zwicker, J., Szymanski, P., Levine, M., and Tjian, R. (1998) TAFII mutations disrupt Dorsal activation in the Drosophila embryo. Proc. Natl. Acad. Sci. U.S.A. 95, 13483-13488
49. van Ingen, H., van Schaik, F. M., Wienk, H., Ballering, J., Rehmann, H., Dechesne, A. C., Kruijzer, J. A., Liskamp, R. M., Timmers, H. T., and Boelens, R. (2008) Structural insight into the recognition of the H3K4me3 mark by the TFIID subunit TAF3. Structure 16, 1245-1256
50. Wang, X., Truckses, D. M., Takada, S., Matsumura, T., Tanese, N., and Jacobson, R. H. (2007) Conserved region I of human coactivator TAF4 binds to a short hydrophobic motif present in transcriptional regulators. Proc. Natl. Acad. Sci. U.S.A. 104, 7839-7844
51. Wright, K. J., and Tjian, R. (2009) Wnt signaling targets ETO coactivation domain of TAF4/TFIID in vivo. Proc. Natl. Acad. Sci. U.S.A. 106, 55-60
52. Wollmann, P., Cui, S., Viswanathan, R., Berninghausen, O., Wells, M. N., Moldt, M., Witte, G., Butryn, A., Wendler, P., Beckmann, R., Auble, D. T., and Hopfner, K. P. (2011) Structure and mechanism of the Swi2/Snf2 remodeller Mot1 in complex with its substrate TBP. Nature 475, 403-407
53. Bond, C. S., and Schüttelkopf, A. W. (2009) ALINE: a WYSIWYG protein-sequence alignment editor for publication-quality alignments. Acta Crystallogr. D Biol. Crystallogr. 65, 510-512
54. Nicholls, A., Sharp, K. A., and Honig, B. (1991) Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins 11, 281-296
55. DeLano, W. L. (2010) The PyMOL Molecular Graphics System, version 1.3r1, Schrödinger, LLC, New York