Crystal Structure of Human General Transcription Factor TFIIE at Atomic Resolution

Journal of Molecular Biology

Volumn 428, Issue 21, 2016, Pages 4258-4266

  Miwa, Kohei ^a   Kojima, Rieko ^b   Obita, Takayuki ^a   Ohkuma, Yoshiaki ^a   Tamura, Yasushi ^b   Mizuguchi, Mineyuki ^a  

^a UNIVERSITY OF TOYAMA   (Japan)

^b YAMAGATA UNIVERSITY   (Japan)

Author keywords

pre initiation complex; RNA polymerase II; TFIIE ; transcription; yeast

Indexed keywords

GENERAL TRANSCRIPTION FACTOR; MUTANT PROTEIN; TRANSCRIPTION FACTOR TFIIE ALPHA; TRANSCRIPTION FACTOR TFIIE BETA; UNCLASSIFIED DRUG; PROTEIN BINDING; TRANSCRIPTION FACTOR II; TRANSCRIPTION FACTOR TFIIE;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CRYSTAL STRUCTURE; FUNGUS GROWTH; HUMAN; IN VIVO STUDY; ISOTHERMAL TITRATION CALORIMETRY; NONHUMAN; OPTICAL RESOLUTION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN SUBUNIT; ZINC FINGER MOTIF; CALORIMETRY; CHEMISTRY; DNA MUTATIONAL ANALYSIS; GENETICS; METABOLISM; MOLECULAR MODEL; PROTEIN CONFORMATION; X RAY CRYSTALLOGRAPHY;

CALORIMETRY; CRYSTALLOGRAPHY, X-RAY; DNA MUTATIONAL ANALYSIS; HUMANS; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN CONFORMATION; TRANSCRIPTION FACTORS, TFII;

EID: 84991461470     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2016.09.008     Document Type: Article

References (49)

1. [1] Dvir, A., Conaway, J.W., Conaway, R.C., Mechanism of transcription initiation and promoter escape by RNA polymerase II. Curr. Opin . Genet. Dev. 11 (2001), 209–214.
2. [2] Liu, X., Bushnell, D.A., Silva, D.A., Huang, X., Kornberg, R.D., Initiation complex structure and promoter proofreading. Science 333 (2011), 633–637.
3. [3] Murakami, K., Elmlund, H., Kalisman, N., Bushnell, D.A., Adams, C.M., Azubel, M., Elmlund, D., Levi-Kalisman, Y., Liu, X., Gibbons, B.J., Levitt, M., Kornberg, R.D., Architecture of an RNA polymerase II transcription pre-initiation complex. Science, 342, 2013, 1,238,724.
4. [4] He, Y., Fang, J., Taatjes, D.J., Nogales, E., Structural visualization of key steps in human transcription initiation. Nature 495 (2013), 481–486.
5. [5] Sainsbury, S., Niesser, J., Cramer, P., Structure and function of the initially transcribing RNA polymerase II–TFIIB complex. Nature 493 (2013), 437–440.
6. [6] Murakami, K., Tsai, K.L., Kalisman, N., Bushnell, D.A., Asturias, F.J., Kornberg, R.D., Structure of an RNA polymerase II preinitiation complex. Proc. Natl. Acad. Sci. U. S. A. 112 (2015), 13,543–13,548.
7. [7] Louder, R.K., He, Y., Lopez-Blanco, J.R., Fang, J., Chacon, P., Nogales, E., Structure of promoter-bound TFIID and model of human pre-initiation complex assembly. Nature 531 (2016), 604–609.
8. [8] Bernecky, C., Herzog, F., Baumeister, W., Plitzko, J.M., Cramer, P., Structure of transcribing mammalian RNA polymerase II. Nature 529 (2016), 551–554.
9. [9] Parvin, J.D., Sharp, P.A., DNA topology and a minimal set of basal factors for transcription by RNA polymerase II. Cell 73 (1993), 533–540.
10. [10] Tyree, C.M., George, C.P., Lira-DeVito, L.M., Wampler, S.L., Dahmus, M.E., Zawel, L., Kadonaga, J.T., Identification of a minimal set of proteins that is sufficient for accurate initiation of transcription by RNA polymerase II. Genes Dev. 7 (1993), 1254–1265.
11. [11] Holstege, F.C., Tantin, D., Carey, M., van der Vliet, P.C., Timmers, H.T., The requirement for the basal transcription factor IIE is determined by the helical stability of promoter DNA. EMBO J. 14 (1995), 810–819.
12. [12] Holstege, F.C., van der Vliet, P.C., Timmers, H.T., Opening of an RNA polymerase II promoter occurs in two distinct steps and requires the basal transcription factors IIE and IIH. EMBO J. 15 (1996), 1666–1677.
13. [13] Ohkuma, Y., Sumimoto, H., Horikoshi, M., Roeder, R.G., Factors involved in specific transcription by mammalian RNA polymerase II: purification and characterization of general transcription factor TFIIE. Proc. Natl. Acad. Sci. U. S. A. 87 (1990), 9163–9167.
14. [14] Feaver, W.J., Henry, N.L., Bushnell, D.A., Sayre, M.H., Brickner, J.H., Gileadi, O., Kornberg, R.D., Yeast TFIIE. Cloning, expression, and homology to vertebrate proteins. J. Biol. Chem. 269 (1994), 27,549–27,553.
15. [15] Kuldell, N.H., Buratowski, S., Genetic analysis of the large subunit of yeast transcription factor IIE reveals two regions with distinct functions. Mol. Cell. Biol. 17 (1997), 5288–5298.
16. [16] Sakurai, H., Ohishi, T., Fukasawa, T., Promoter structure-dependent functioning of the general transcription factor IIE in Saccharomyces cerevisiae. J. Biol. Chem. 272 (1997), 15,936–15,942.
17. [17] Ohkuma, Y., Multiple functions of general transcription factors TFIIE and TFIIH in transcription: possible points of regulation by trans-acting factors. J. Biochem. 122 (1997), 481–489.
18. [18] Okuda, M., Tanaka, A., Arai, Y., Satoh, M., Okamura, H., Nagadoi, A., Hanaoka, F., Ohkuma, Y., Nishimura, Y., A novel zinc finger structure in the large subunit of human general transcription factor TFIIE. J. Biol. Chem. 279 (2004), 51,395–51,403.
19. [19] Okuda, M., Tanaka, A., Satoh, M., Mizuta, S., Takazawa, M., Ohkuma, Y., Nishimura, Y., Structural insight into the TFIIE–TFIIH interaction: TFIIE and p53 share the binding region on TFIIH. EMBO J. 27 (2008), 1161–1171.
20. [20] Di Lello, P., Miller Jenkins, L.M., Mas, C., Langlois, C., Malitskaya, E., Fradet-Turcotte, A., Archambault, J., Legault, P., Omichinski, J.G., p53 and TFIIEalpha share a common binding site on the Tfb1/p62 subunit of TFIIH. Proc. Natl. Acad. Sci. U. S. A. 105 (2008), 106–111.
21. [21] Sumimoto, H., Ohkuma, Y., Sinn, E., Kato, H., Shimasaki, S., Horikoshi, M., Roeder, R.G., Conserved sequence motifs in the small subunit of human general transcription factor TFIIE. Nature 354 (1991), 401–404.
22. [22] Chen, H.T., Warfield, L., Hahn, S., The positions of TFIIF and TFIIE in the RNA polymerase II transcription preinitiation complex. Nat. Struct. Mol. Biol. 14 (2007), 696–703.
23. [23] Meinhart, A., Blobel, J., Cramer, P., An extended winged helix domain in general transcription factor E/IIE alpha. J. Biol. Chem. 278 (2003), 48,267–48,274.
24. [24] Grohmann, D., Nagy, J., Chakraborty, A., Klose, D., Fielden, D., Ebright, R.H., Michaelis, J., Werner, F., The initiation factor TFE and the elongation factor Spt4/5 compete for the RNAP clamp during transcription initiation and elongation. Mol. Cell 43 (2011), 263–274.
25. [25] Kim, T.K., Ebright, R.H., Reinberg, D., Mechanism of ATP-dependent promoter melting by transcription factor IIH. Science 288 (2000), 1418–1422.
26. [26] Miller, G., Hahn, S., A DNA-tethered cleavage probe reveals the path for promoter DNA in the yeast preinitiation complex. Nat. Struct. Mol. Biol. 13 (2006), 603–610.
27. [27] Lin, Y.C., Gralla, J.D., Stimulation of the XPB ATP-dependent helicase by the beta subunit of TFIIE. Nucleic Acids Res. 33 (2005), 3072–3081.
28. [28] Okamoto, T., Yamamoto, S., Watanabe, Y., Ohta, T., Hanaoka, F., Roeder, R.G., Ohkuma, Y., Analysis of the role of TFIIE in transcriptional regulation through structure–function studies of the TFIIEbeta subunit. J. Biol. Chem. 273 (1998), 19,866–19,876.
29. [29] Kojima, R., Obita, T., Onoue, K., Mizuguchi, M., Structural fine-tuning of MIT-interacting motif 2 (MIM2) and allosteric regulation of ESCRT-III by Vps4 in yeast. J. Mol. Biol. 428 (2016), 2392–2404.
30. [31] Teo, H., Gill, D.J., Sun, J., Perisic, O., Veprintsev, D.B., Vallis, Y., Emr, S.D., Williams, R.L., ESCRT-I core and ESCRT-II GLUE domain structures reveal role for GLUE in linking to ESCRT-I and membranes. Cell 125 (2006), 99–111.
31. [32] Krishna, S.S., Majumdar, I., Grishin, N.V., Structural classification of zinc fingers: survey and summary. Nucleic Acids Res. 31 (2003), 532–550.
32. [33] Watanabe, T., Hayashi, K., Tanaka, A., Furumoto, T., Hanaoka, F., Ohkuma, Y., The carboxy terminus of the small subunit of TFIIE regulates the transition from transcription initiation to elongation by RNA polymerase II. Mol. Cell. Biol. 23 (2003), 2914–2926.
33. [34] Grunberg, S., Warfield, L., Hahn, S., Architecture of the RNA polymerase II preinitiation complex and mechanism of ATP-dependent promoter opening. Nat. Struct. Mol. Biol. 19 (2012), 788–796.
34. [35] Hirtreiter, A., Grohmann, D., Werner, F., Molecular mechanisms of RNA polymerase—the F/E (RPB4/7) complex is required for high processivity in vitro. Nucleic Acids Res. 38 (2010), 585–596.
35. [36] Naji, S., Grunberg, S., Thomm, M., The RPB7 orthologue E' is required for transcriptional activity of a reconstituted archaeal core enzyme at low temperatures and stimulates open complex formation. J. Biol. Chem. 282 (2007), 11,047–11,057.
36. [37] Blombach, F., Smollett, K.L., Grohmann, D., Werner, F., Molecular mechanisms of transcription initiation—structure, function, and evolution of TFE/TFIIE-like factors and open complex formation. J. Mol. Biol. 428 (2016), 2592–2606.
37. [38] Blombach, F., Salvadori, E., Fouqueau, T., Yan, J., Reimann, J., Sheppard, C., Smollett, K.L., Albers, S.V., Kay, C.W., Thalassinos, K., Werner, F., Archaeal TFEalpha/beta is a hybrid of TFIIE and the RNA polymerase III subcomplex hRPC62/39. eLife, 4, 2015, e08378.
38. [39] He, Y., Yan, C., Fang, J., Inouye, C., Tjian, R., Ivanov, I., Nogales, E., Near-atomic resolution visualization of human transcription promoter opening. Nature 533 (2016), 359–365.
39. [40] Plaschka, C., Hantsche, M., Dienemann, C., Burzinski, C., Plitzko, J., Cramer, P., Transcription initiation complex structures elucidate DNA opening. Nature 533 (2016), 353–358.
40. [41] Tan, S., A modular polycistronic expression system for overexpressing protein complexes in Escherichia coli. Protein Expr. Purif. 21 (2001), 224–234.
41. [42] Battye, T.G., Kontogiannis, L., Johnson, O., Powell, H.R., Leslie, A.G., iMOSFLM: a new graphical interface for diffraction-image processing with MOSFLM. Acta Crystallogr. D Biol. Crystallogr. 67 (2011), 271–281.
42. [43] Winn, M.D., Ballard, C.C., Cowtan, K.D., Dodson, E.J., Emsley, P., Evans, P.R., Keegan, R.M., Krissinel, E.B., Leslie, A.G., McCoy, A., McNicholas, S.J., Murshudov, G.N., Pannu, N.S., Potterton, E.A., Powell, H.R., Read, R.J., Vagin, A., Wilson, K.S., Overview of the CCP4 suite and current developments. Acta Crystallogr. D Biol. Crystallogr. 67 (2011), 235–242.
43. [44] Uson, I., Schmidt, B., von Bulow, R., Grimme, S., von Figura, K., Dauter, M., Rajashankar, K.R., Dauter, Z., Sheldrick, G.M., Locating the anomalous scatterer substructures in halide and sulfur phasing. Acta Crystallogr. D Biol. Crystallogr. 59 (2003), 57–66.
44. [45] Ness, S.R., de Graaff, R.A., Abrahams, J.P., Pannu, N.S., CRANK: new methods for automated macromolecular crystal structure solution. Structure 12 (2004), 1753–1761.
45. [46] Cowtan, K., The buccaneer software for automated model building. 1. Tracing protein chains. Acta Crystallogr. D Biol. Crystallogr. 62 (2006), 1002–1011.
46. [47] Emsley, P., Lohkamp, B., Scott, W.G., Cowtan, K., Features and development of coot. Acta Crystallogr. D Biol. Crystallogr. 66 (2010), 486–501.
47. [48] Adams, P.D., Afonine, P.V., Bunkoczi, G., Chen, V.B., Davis, I.W., Echols, N., Headd, J.J., Hung, L.W., Kapral, G.J., Grosse-Kunstleve, R.W., McCoy, A.J., Moriarty, N.W., Oeffner, R., Read, R.J., Richardson, D.C., Richardson, J.S., Terwilliger, T.C., Zwart, P.H., PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66 (2010), 213–221.
48. [49] Winston, F., Dollard, C., Ricupero-Hovasse, S.L., Construction of a set of convenient Saccharomyces cerevisiae strains that are isogenic to S288C. Yeast 11 (1995), 53–55.
49. [50] Boeke, J.D., Trueheart, J., Natsoulis, G., Fink, G.R., 5-fluoroorotic acid as a selective agent in yeast molecular genetics. Methods Enzymol. 154 (1987), 164–175.