Human TFIID binds to core promoter DNA in a reorganized structural state

Cell

Volumn 152, Issue 1-2, 2013, Pages 120-131

  Cianfrocco, Michael A ^a   Kassavetis, George A ^b   Grob, Patricia ^a   Fang, Jie ^a   Juven Gershon, Tamar ^c   Kadonaga, James T ^b   Nogales, Eva ^a,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b SECTION OF MOLECULAR BIOLOGY   (United States)

^c BAR ILAN UNIVERSITY   (Israel)

^d LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR IID;

ARTICLE; DNA FOOTPRINTING; DNA STRUCTURE; ELECTRON MICROSCOPY; GENE EXPRESSION REGULATION; GENE REARRANGEMENT; HUMAN; PRIORITY JOURNAL; PROMOTER DNA; PROMOTER REGION; PROTEIN CONFORMATION; PROTEIN DNA BINDING; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PURIFICATION; TRANSCRIPTION INITIATION;

EID: 84872505828     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2012.12.005     Document Type: Article

References (65)

1. F. Andel III, A.G. Ladurner, C. Inouye, R. Tjian, and E. Nogales Three-dimensional structure of the human TFIID-IIA-IIB complex Science 286 1999 2153 2156 (Pubitemid 129516289)
2. S. Bagby, T.K. Mal, D. Liu, E. Raddatz, Y. Nakatani, and M. Ikura TFIIA-TAF regulatory interplay: NMR evidence for overlapping binding sites on TBP FEBS Lett. 468 2000 149 154 (Pubitemid 30110785)
3. S. Bhattacharya, S. Takada, and R.H. Jacobson Structural analysis and dimerization potential of the human TAF5 subunit of TFIID Proc. Natl. Acad. Sci. USA 104 2007 1189 1194 (Pubitemid 46183980)
4. M. Brand, C. Leurent, V. Mallouh, L. Tora, and P. Schultz Three-dimensional structures of the TAFII-containing complexes TFIID and TFTC Science 286 1999 2151 2153 (Pubitemid 129516288)
5. S. Buratowski, S. Hahn, L. Guarente, and P.A. Sharp Five intermediate complexes in transcription initiation by RNA polymerase II Cell 56 1989 549 561
6. T.W. Burke, and J.T. Kadonaga The downstream core promoter element, DPE, is conserved from Drosophila to humans and is recognized by TAFII60 of Drosophila Genes Dev. 11 1997 3020 3031 (Pubitemid 27508512)
7. S.K. Burley, and R.G. Roeder Biochemistry and structural biology of transcription factor IID (TFIID) Annu. Rev. Biochem. 65 1996 769 799 (Pubitemid 26250625)
8. G.E. Chalkley, and C.P. Verrijzer DNA binding site selection by RNA polymerase II TAFs: a TAF(II)250-TAF(II)150 complex recognizes the initiator EMBO J. 18 1999 4835 4845 (Pubitemid 29415536)
9. J.Z. Chen, and N. Grigorieff SIGNATURE: a single-particle selection system for molecular electron microscopy J. Struct. Biol. 157 2007 168 173 (Pubitemid 44895517)
10. T. Chi, and M. Carey Assembly of the isomerized TFIIA - TFIID - TATA ternary complex is necessary and sufficient for gene activation Genes Dev. 10 1996 2540 2550 (Pubitemid 26357221)
11. H. Elmlund, V. Baraznenok, T. Linder, Z. Szilagyi, R. Rofougaran, A. Hofer, H. Hebert, M. Lindahl, and C.M. Gustafsson Cryo-EM reveals promoter DNA binding and conformational flexibility of the general transcription factor TFIID Structure 17 2009 1442 1452
12. K.H. Emami, A. Jain, and S.T. Smale Mechanism of synergy between TATA and initiator: synergistic binding of TFIID following a putative TFIIA-induced isomerization Genes Dev. 11 1997 3007 3019 (Pubitemid 27508511)
13. J. Frank, M. Radermacher, P. Penczek, J. Zhu, Y. Li, M. Ladjadj, and A. Leith SPIDER and WEB: processing and visualization of images in 3D electron microscopy and related fields J. Struct. Biol. 116 1996 190 199 (Pubitemid 26093143)
14. J.H. Geiger, S. Hahn, S. Lee, and P.B. Sigler Crystal structure of the yeast TFIIA/TBP/DNA complex Science 272 1996 830 836 (Pubitemid 26154587)
15. N. Grigorieff FREALIGN: high-resolution refinement of single particle structures J. Struct. Biol. 157 2007 117 125 (Pubitemid 44880784)
16. P. Grob, M.J. Cruse, C. Inouye, M. Peris, P.A. Penczek, R. Tjian, and E. Nogales Cryo-electron microscopy studies of human TFIID: conformational breathing in the integration of gene regulatory cues Structure 14 2006 511 520 (Pubitemid 43363484)
17. R.P. Hertzberg, and P.B. Dervan Cleavage of DNA with methidiumpropyl- EDTA-iron(II): reaction conditions and product analyses Biochemistry 23 1984 3934 3945
18. M. Hohn, G. Tang, G. Goodyear, P.R. Baldwin, Z. Huang, P.A. Penczek, C. Yang, R.M. Glaeser, P.D. Adams, and S.J. Ludtke SPARX, a new environment for Cryo-EM image processing J. Struct. Biol. 157 2007 47 55 (Pubitemid 44880795)
19. R.H. Jacobson, A.G. Ladurner, D.S. King, and R. Tjian Structure and function of a human TAFII250 double bromodomain module Science 288 2000 1422 1425 (Pubitemid 30366328)
20. T. Juven-Gershon, and J.T. Kadonaga Regulation of gene expression via the core promoter and the basal transcriptional machinery Dev. Biol. 339 2010 225 229
21. T. Juven-Gershon, S. Cheng, and J.T. Kadonaga Rational design of a super core promoter that enhances gene expression Nat. Methods 3 2006 917 922 (Pubitemid 44614727)
22. J.L. Kim, D.B. Nikolov, and S.K. Burley Co-crystal structure of TBP recognizing the minor groove of a TATA element Nature 365 1993 520 527 (Pubitemid 23317771)
23. Y. Kim, J.H. Geiger, S. Hahn, and P.B. Sigler Crystal structure of a yeast TBP/TATA-box complex Nature 365 1993 512 520 (Pubitemid 23317770)
24. G.C. Lander, S.M. Stagg, N.R. Voss, A. Cheng, D. Fellmann, J. Pulokas, C. Yoshioka, C. Irving, A. Mulder, and P.W. Lau Appion: an integrated, database-driven pipeline to facilitate EM image processing J. Struct. Biol. 166 2009 95 102
25. A.E. Leschziner, and E. Nogales The orthogonal tilt reconstruction method: an approach to generating single-class volumes with no missing cone for ab initio reconstruction of asymmetric particles J. Struct. Biol. 153 2006 284 299 (Pubitemid 43238321)
26. A.E. Leschziner, and E. Nogales Visualizing flexibility at molecular resolution: analysis of heterogeneity in single-particle electron microscopy reconstructions Annu. Rev. Biophys. Biomol. Struct. 36 2007 43 62 (Pubitemid 46998109)
27. C. Leurent, S. Sanders, C. Ruhlmann, V. Mallouh, P.A. Weil, D.B. Kirschner, L. Tora, and P. Schultz Mapping histone fold TAFs within yeast TFIID EMBO J. 21 2002 3424 3433 (Pubitemid 34760574)
28. C. Leurent, S.L. Sanders, M.A. Demény, K.A. Garbett, C. Ruhlmann, P.A. Weil, L. Tora, and P. Schultz Mapping key functional sites within yeast TFIID EMBO J. 23 2004 719 727 (Pubitemid 38418740)
29. M. Levine Paused RNA polymerase II as a developmental checkpoint Cell 145 2011 502 511
30. M. Levine, and R. Tjian Transcription regulation and animal diversity Nature 424 2003 147 151 (Pubitemid 36858677)
31. P.M. Lieberman, and A.J. Berk A mechanism for TAFs in transcriptional activation: activation domain enhancement of TFIID-TFIIA - promoter DNA complex formation Genes Dev. 8 1994 995 1006 (Pubitemid 24145664)
32. D. Liu, R. Ishima, K.I. Tong, S. Bagby, T. Kokubo, D.R. Muhandiram, L.E. Kay, Y. Nakatani, and M. Ikura Solution structure of a TBP-TAF(II)230 complex: protein mimicry of the minor groove surface of the TATA box unwound by TBP Cell 94 1998 573 583 (Pubitemid 28427576)
33. W.L. Liu, R.A. Coleman, P. Grob, D.S. King, L. Florens, M.P. Washburn, K.G. Geles, J.L. Yang, V. Ramey, E. Nogales, and R. Tjian Structural changes in TAF4b-TFIID correlate with promoter selectivity Mol. Cell 29 2008 81 91
34. W.L. Liu, R.A. Coleman, E. Ma, P. Grob, J.L. Yang, Y. Zhang, G. Dailey, E. Nogales, and R. Tjian Structures of three distinct activator-TFIID complexes Genes Dev. 23 2009 1510 1521
35. S.J. Ludtke, P.R. Baldwin, and W. Chiu EMAN: semiautomated software for high-resolution single-particle reconstructions J. Struct. Biol. 128 1999 82 97 (Pubitemid 30013436)
36. J.A. Mindell, and N. Grigorieff Accurate determination of local defocus and specimen tilt in electron microscopy J. Struct. Biol. 142 2003 334 347 (Pubitemid 36638267)
37. D.B. Nikolov, H. Chen, E.D. Halay, A.A. Usheva, K. Hisatake, D.K. Lee, R.G. Roeder, and S.K. Burley Crystal structure of a TFIIB-TBP-TATA-element ternary complex Nature 377 1995 119 128
38. T. Ogura, K. Iwasaki, and C. Sato Topology representing network enables highly accurate classification of protein images taken by cryo electron-microscope without masking J. Struct. Biol. 143 2003 185 200 (Pubitemid 37297859)
39. G. Papai, M.K. Tripathi, C. Ruhlmann, S. Werten, C. Crucifix, P.A. Weil, and P. Schultz Mapping the initiator binding Taf2 subunit in the structure of hydrated yeast TFIID Structure 17 2009 363 373
40. G. Papai, M.K. Tripathi, C. Ruhlmann, J.H. Layer, P.A. Weil, and P. Schultz TFIIA and the transactivator Rap1 cooperate to commit TFIID for transcription initiation Nature 465 2010 956 960
41. G. Papai, P.A. Weil, and P. Schultz New insights into the function of transcription factor TFIID from recent structural studies Curr. Opin. Genet. Dev. 21 2011 219 224
42. A.G. Papavassiliou Chemical nucleases as probes for studying DNA-protein interactions Biochem. J. 305 1995 345 357
43. H.S. Rhee, and B.F. Pugh Genome-wide structure and organization of eukaryotic pre-initiation complexes Nature 483 2012 295 301
44. S.L. Sanders, K.A. Garbett, and P.A. Weil Molecular characterization of Saccharomyces cerevisiae TFIID Mol. Cell. Biol. 22 2002 6000 6013 (Pubitemid 34815846)
45. M. Sawadogo, and R.G. Roeder Interaction of a gene-specific transcription factor with the adenovirus major late promoter upstream of the TATA box region Cell 43 1985 165 175 (Pubitemid 16199703)
46. C.O. Sorzano, R. Marabini, J. Velázquez-Muriel, J.R. Bilbao-Castro, S.H. Scheres, J.M. Carazo, and A. Pascual-Montano XMIPP: a new generation of an open-source image processing package for electron microscopy J. Struct. Biol. 148 2004 194 204 (Pubitemid 39346008)
47. C. Suloway, J. Pulokas, D. Fellmann, A. Cheng, F. Guerra, J. Quispe, S. Stagg, C.S. Potter, and B. Carragher Automated molecular microscopy: the new Leginon system J. Struct. Biol. 151 2005 41 60 (Pubitemid 40848375)
48. X. Sun, D. Ma, M. Sheldon, K. Yeung, and D. Reinberg Reconstitution of human TFIIA activity from recombinant polypeptides: a role in TFIID-mediated transcription Genes Dev. 8 1994 2336 2348 (Pubitemid 24314295)
49. G. Tang, L. Peng, P.R. Baldwin, D.S. Mann, W. Jiang, I. Rees, and S.J. Ludtke EMAN2: an extensible image processing suite for electron microscopy J. Struct. Biol. 157 2007 38 46 (Pubitemid 44880785)
50. J.W. Theisen, C.Y. Lim, and J.T. Kadonaga Three key subregions contribute to the function of the downstream RNA polymerase II core promoter Mol. Cell. Biol. 30 2010 3471 3479
51. M.C. Thomas, and C.M. Chiang The general transcription machinery and general cofactors Crit. Rev. Biochem. Mol. Biol. 41 2006 105 178
52. K. Uchida, A.M. Pyle, T. Morii, and J.K. Barton High resolution footprinting of EcoRI and distamycin with Rh(phi)2(bpy)3+, a new photofootprinting reagent Nucleic Acids Res. 17 1989 10259 10279 (Pubitemid 20012184)
53. M.W. Van Dyke, R.P. Hertzberg, and P.B. Dervan Map of distamycin, netropsin, and actinomycin binding sites on heterogeneous DNA: DNA cleavage-inhibition patterns with methidiumpropyl-EDTA.Fe(II) Proc. Natl. Acad. Sci. USA 79 1982 5470 5474 (Pubitemid 13197665)
54. M.W. Van Dyke, R.G. Roeder, and M. Sawadogo Physical analysis of transcription preinitiation complex assembly on a class II gene promoter Science 241 1988 1335 1338
55. M. van Heel, G. Harauz, E.V. Orlova, R. Schmidt, and M. Schatz A new generation of the IMAGIC image processing system J. Struct. Biol. 116 1996 17 24 (Pubitemid 26093118)
56. S. Werten, A. Mitschler, C. Romier, Y.G. Gangloff, S. Thuault, I. Davidson, and D. Moras Crystal structure of a subcomplex of human transcription factor TFIID formed by TATA binding protein-associated factors hTAF4 (hTAF(II)135) and hTAF12 (hTAF(II)20) J. Biol. Chem. 277 2002 45502 45509 (Pubitemid 36159160)
57. K.J. Wright, M.T. Marr II, and R. Tjian TAF4 nucleates a core subcomplex of TFIID and mediates activated transcription from a TATA-less promoter Proc. Natl. Acad. Sci. USA 103 2006 12347 12352 (Pubitemid 44267262)
58. X. Xie, T. Kokubo, S.L. Cohen, U.A. Mirza, A. Hoffmann, B.T. Chait, R.G. Roeder, Y. Nakatani, and S.K. Burley Structural similarity between TAFs and the heterotetrameric core of the histone octamer Nature 380 1996 316 322 (Pubitemid 26097111)
59. Bradley, D.E. (1965). The Preparation of Specimen Support Films (Oxford: Blackwell Scientific Publications).
60. Chandramouli, P.; Hernandez-Lopez, R.; Wang, H.W.; and Leschziner, A.E. (2011). Validation of the orthogonal tilt reconstruction method with a biological test sample. J. Struct. Biol. 175, 85-96.
61. Iverson, B.L.; and Dervan, P.B. (1987). Adenine specific DNA chemical sequencing reaction. Nucleic Acids Res. 15, 7823-7830.
62. Leschziner, A. (2010). The orthogonal tilt reconstruction method. Methods Enzymol. 482, 237-262.
63. Näär, A.M.; Beaurang, P.A.; Robinson, K.M.; Oliner, J.D.; Avizonis, D.; Scheek, S.; Zwicker, J.; Kadonaga, J.T.; and Tjian, R. (1998). Chromatin, TAFs, and a novel multiprotein coactivator are required for synergistic activation by Sp1 and SREBP-1a in vitro. Genes Dev. 12, 3020-3031. (Pubitemid 28469304)
64. Sambrook, J.; Fritsch, E.F.; and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual, second edition, volume 3 (Cold Spring Harbor: Cold Spring Harbor Laboratory Press).
65. Saxton, W.O.; and Baumeister, W. (1982). The correlation averaging of a regularly arranged bacterial cell envelope protein. J. Microsc. 127, 127-138. (Pubitemid 12060892)