Architecture of the RNA polymerase II preinitiation complex and mechanism of ATP-dependent promoter opening
10.1038/nsmb.2334
Crossref journal-article
Springer Science and Business Media LLC
Nature Structural & Molecular Biology (297)
Bibliography

Grünberg, S., Warfield, L., & Hahn, S. (2012). Architecture of the RNA polymerase II preinitiation complex and mechanism of ATP-dependent promoter opening. Nature Structural & Molecular Biology, 19(8), 788–796.

Authors 3
  1. Sebastian Grünberg (first)
  2. Linda Warfield (additional)
  3. Steven Hahn (additional)
References 59 Referenced 120
  1. Hahn, S. & Young, E.T. Transcriptional regulation in Saccharomyces cerevisiae: transcription factor regulation and function, mechanisms of initiation, and roles of activators and coactivators. Genetics 189, 705–736 (2011). (10.1534/genetics.111.127019) / Genetics by S Hahn (2011)
  2. Thomas, M.C. & Chiang, C.M. The general transcription machinery and general cofactors. Crit. Rev. Biochem. Mol. Biol. 41, 105–178 (2006). (10.1080/10409230600648736) / Crit. Rev. Biochem. Mol. Biol. by MC Thomas (2006)
  3. Wang, W., Carey, M. & Gralla, J.D. Polymerase II promoter activation: closed complex formation and ATP-driven start site opening. Science 255, 450–453 (1992). (10.1126/science.1310361) / Science by W Wang (1992)
  4. Holstege, F.C.P., Fiedler, U. & Timmers, H.T.M. Three transitions in the RNA polymerase II transcription complex during initiation. EMBO J. 16, 7468–7480 (1997). (10.1093/emboj/16.24.7468) / EMBO J. by FCP Holstege (1997)
  5. 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, 696–703 (2007). (10.1038/nsmb1272) / Nat. Struct. Mol. Biol. by HT Chen (2007)
  6. Eichner, J., Chen, H.T., Warfield, L. & Hahn, S. Position of the general transcription factor TFIIF within the RNA polymerase II transcription preinitiation complex. EMBO J. 29, 706–716 (2010). (10.1038/emboj.2009.386) / EMBO J. by J Eichner (2010)
  7. Chen, Z.A. et al. Architecture of the RNA polymerase II-TFIIF complex revealed by cross-linking and mass spectrometry. EMBO J. 29, 717–726 (2010). (10.1038/emboj.2009.401) / EMBO J. by ZA Chen (2010)
  8. Fishburn, J. & Hahn, S. Architecture of the yeast RNA polymerase II open complex and regulation of activity by TFIIF. Mol. Cell Biol. 32, 12–25 (2012). (10.1128/MCB.06242-11) / Mol. Cell Biol. by J Fishburn (2012)
  9. Kostrewa, D. et al. RNA polymerase II-TFIIB structure and mechanism of transcription initiation. Nature 462, 323–330 (2009). (10.1038/nature08548) / Nature by D Kostrewa (2009)
  10. Liu, X., Bushnell, D.A., Wang, D., Calero, G. & Kornberg, R.D. Structure of an RNA polymerase II-TFIIB complex and the transcription initiation mechanism. Science 327, 206–209 (2010). (10.1126/science.1182015) / Science by X Liu (2010)
  11. Pan, G. & Greenblatt, J. Initiation of transcription by RNA Polymerase II is limited by melting of the promoter DNA in the region immediately upstream of the initiation site. J. Biol. Chem. 269, 30101–30104 (1994). (10.1016/S0021-9258(18)43780-5) / J. Biol. Chem. by G Pan (1994)
  12. Tantin, D. & Carey, M. A heteroduplex template circumvents the energetic requirement for ATP during activated transcription by RNA Pol II. J. Biol. Chem. 269, 17937–17400 (1994). (10.1016/S0021-9258(17)32452-3) / J. Biol. Chem. by D Tantin (1994)
  13. 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, 1666–1677 (1996). (10.1002/j.1460-2075.1996.tb00512.x) / EMBO J. by FC Holstege (1996)
  14. Ohkuma, Y. Multiple functions of general transcription factors TFIIE and TFIIH in transcription: possible points of regulation by trans-acting factors. J. Biochem. 122, 481–489 (1997). (10.1093/oxfordjournals.jbchem.a021777) / J. Biochem. by Y Ohkuma (1997)
  15. Feaver, W.J. et al. Yeast TFIIE. Cloning, expression, and homology to vertebrate proteins. J. Biol. Chem. 269, 27549–27553 (1994). (10.1016/S0021-9258(18)47019-6) / J. Biol. Chem. by WJ Feaver (1994)
  16. Ohkuma, Y., Hashimoto, S., Wang, C.K., Horikoshi, M. & Roeder, R.G. Analysis of the role of TFIIE in basal transcription and TFIIH-mediated carboxy-terminal domain phosphorylation through structure-function studies of TFIIE-alpha. Mol. Cell Biol. 15, 4856–4866 (1995). (10.1128/MCB.15.9.4856) / Mol. Cell Biol. by Y Ohkuma (1995)
  17. Okuda, M. et al. A novel zinc finger structure in the large subunit of human general transcription factor TFIIE. J. Biol. Chem. 279, 51395–51403 (2004). (10.1074/jbc.M404722200) / J. Biol. Chem. by M Okuda (2004)
  18. 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, 5288–5298 (1997). (10.1128/MCB.17.9.5288) / Mol. Cell Biol. by NH Kuldell (1997)
  19. Sakurai, H., Ohishi, T. & Fukasawa, T. Promoter structure–dependent functioning of the general transcription factor IIE in Saccharomyces cerevisiae. J. Biol. Chem. 272, 15936–15942 (1997). (10.1074/jbc.272.25.15936) / J. Biol. Chem. by H Sakurai (1997)
  20. Aravind, L., Anantharaman, V., Balaji, S., Babu, M.M. & Iyer, L.M. The many faces of the helix-turn-helix domain: transcription regulation and beyond. FEMS Microbiol. Rev. 29, 231–262 (2005). (10.1016/j.fmrre.2004.12.008) / FEMS Microbiol. Rev. by L Aravind (2005)
  21. Meinhart, A., Blobel, J. & Cramer, P. An extended winged helix domain in general transcription factor E/IIEα. J. Biol. Chem. 278, 48267–48274 (2003). (10.1074/jbc.M307874200) / J. Biol. Chem. by A Meinhart (2003)
  22. Geiger, S.R. et al. RNA polymerase I contains a TFIIF-related DNA-binding subcomplex. Mol. Cell 39, 583–594 (2010). (10.1016/j.molcel.2010.07.028) / Mol. Cell by SR Geiger (2010)
  23. Okuda, M. et al. Structure of the central core domain of TFIIEβ with a novel double-stranded DNA-binding surface. EMBO J. 19, 1346–1356 (2000). (10.1093/emboj/19.6.1346) / EMBO J. by M Okuda (2000)
  24. Tanaka, A., Watanabe, T., Iida, Y., Hanaoka, F. & Ohkuma, Y. Central forkhead domain of human TFIIE beta plays a primary role in binding double-stranded DNA at transcription initiation. Genes Cells 14, 395–405 (2009). (10.1111/j.1365-2443.2008.01278.x) / Genes Cells by A Tanaka (2009)
  25. Shinkai, A. et al. The putative DNA-binding protein Sto12a from the thermoacidophilic archaeon Sulfolobus tokodaii contains intrachain and interchain disulfide bonds. J. Mol. Biol. 372, 1293–1304 (2007). (10.1016/j.jmb.2007.07.051) / J. Mol. Biol. by A Shinkai (2007)
  26. Jawhari, A. et al. Structure and oligomeric state of human transcription factor TFIIE. EMBO Rep. 7, 500–505 (2006). (10.1038/sj.embor.7400663) / EMBO Rep. by A Jawhari (2006)
  27. Luo, J., Fishburn, J., Hahn, S. & Ranish, J. An integrated chemical cross-linking and mass spectrometry approach to study protein complex architecture and function. Mol. Cell Proteomics 11, M111.008318 (2012). (10.1074/mcp.M111.008318) / Mol. Cell Proteomics by J Luo (2012)
  28. Kim, T.K., Ebright, R.H. & Reinberg, D. Mechanism of ATP-dependent promoter melting by transcription factor IIH. Science 288, 1418–1421 (2000). (10.1126/science.288.5470.1418) / Science by TK Kim (2000)
  29. 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, 603–610 (2006). (10.1038/nsmb1117) / Nat. Struct. Mol. Biol. by G Miller (2006)
  30. Grohmann, D. et al. The initiation factor TFE and the elongation factor Spt4/5 compete for the RNAP clamp during transcription initiation and elongation. Mol. Cell 43, 263–274 (2011). (10.1016/j.molcel.2011.05.030) / Mol. Cell by D Grohmann (2011)
  31. Grünberg, S., Bartlett, M.S., Naji, S. & Thomm, M. Transcription factor E is a part of transcription elongation complexes. J. Biol. Chem. 282, 35482–35490 (2007). (10.1074/jbc.M707371200) / J. Biol. Chem. by S Grünberg (2007)
  32. Coin, F., Bergmann, E., Tremeau-Bravard, A. & Egly, J.M. Mutations in XPB and XPD helicases found in xeroderma pigmentosum patients impair the transcription function of TFIIH. EMBO J. 18, 1357–1366 (1999). (10.1093/emboj/18.5.1357) / EMBO J. by F Coin (1999)
  33. Lin, Y.C., Choi, W.S. & Gralla, J.D. TFIIH XPB mutants suggest a unified bacterial-like mechanism for promoter opening but not escape. Nat. Struct. Mol. Biol. 12, 603–607 (2005). (10.1038/nsmb949) / Nat. Struct. Mol. Biol. by YC Lin (2005)
  34. Datwyler, S.A. & Meares, C.F. Protein-protein interactions mapped by artificial proteases: where sigma factors bind to RNA polymerase. Trends Biochem. Sci. 25, 408–414 (2000). (10.1016/S0968-0004(00)01652-2) / Trends Biochem. Sci. by SA Datwyler (2000)
  35. Chen, H.T. & Hahn, S. Binding of TFIIB to RNA polymerase II: Mapping the binding site for the TFIIB zinc ribbon domain within the preinitiation complex. Mol. Cell 12, 437–447 (2003). (10.1016/S1097-2765(03)00306-X) / Mol. Cell by HT Chen (2003)
  36. Ranish, J.A., Yudkovsky, N. & Hahn, S. Intermediates in formation and activity of the RNA polymerase II preinitiation complex: holoenzyme recruitment and a postrecruitment role for the TATA box and TFIIB. Genes Dev. 13, 49–63 (1999). (10.1101/gad.13.1.49) / Genes Dev. by JA Ranish (1999)
  37. Liu, X., Bushnell, D.A., Silva, D.A., Huang, X. & Kornberg, R.D. Initiation complex structure and promoter proofreading. Science 333, 633–637 (2011). (10.1126/science.1206629) / Science by X Liu (2011)
  38. Douziech, M. et al. Mechanism of promoter melting by the xeroderma pigmentosum complementation group B helicase of transcription factor IIH revealed by protein-DNA photo-cross-linking. Mol. Cell Biol. 20, 8168–8177 (2000). (10.1128/MCB.20.21.8168-8177.2000) / Mol. Cell Biol. by M Douziech (2000)
  39. Caruthers, J.M. & McKay, D.B. Helicase structure and mechanism. Curr. Opin. Struct. Biol. 12, 123–133 (2002). (10.1016/S0959-440X(02)00298-1) / Curr. Opin. Struct. Biol. by JM Caruthers (2002)
  40. Goel, S., Krishnamurthy, S. & Hampsey, M. Mechanism of start site selection by RNA polymerase II: interplay between TFIIB and Ssl2/XPB helicase subunit of TFIIH. J. Biol. Chem. 287, 557–567 (2012). (10.1074/jbc.M111.281576) / J. Biol. Chem. by S Goel (2012)
  41. Chin, J.W. et al. An expanded eukaryotic genetic code. Science 301, 964–967 (2003). (10.1126/science.1084772) / Science by JW Chin (2003)
  42. Kettenberger, H., Armache, K.J. & Cramer, P. Complete RNA polymerase II elongation complex structure and its interactions with NTP and TFIIS. Mol. Cell 16, 955–965 (2004). (10.1016/j.molcel.2004.11.040) / Mol. Cell by H Kettenberger (2004)
  43. 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, 11047–11057 (2007). (10.1074/jbc.M611674200) / J. Biol. Chem. by S Naji (2007)
  44. Werner, F. & Grohmann, D. Evolution of multisubunit RNA polymerases in the three domains of life. Nat. Rev. Microbiol. 9, 85–98 (2011). (10.1038/nrmicro2507) / Nat. Rev. Microbiol. by F Werner (2011)
  45. Vannini, A. & Cramer, P. Conservation between the RNA Polymerase I, II, and III Transcription Initiation Machineries. Mol. Cell 45, 439–446 (2012). (10.1016/j.molcel.2012.01.023) / Mol. Cell by A Vannini (2012)
  46. Bischler, N. et al. Localization of the yeast RNA polymerase I–specific subunits. EMBO J. 21, 4136–4144 (2002). (10.1093/emboj/cdf392) / EMBO J. by N Bischler (2002)
  47. Wu, C.C., Lin, Y.C. & Chen, H.T. The TFIIF-like Rpc37/53 dimer lies at the center of a protein network to connect TFIIIC, Bdp1, and the RNA polymerase III active center. Mol. Cell Biol. 31, 2715–2728 (2011). (10.1128/MCB.05151-11) / Mol. Cell Biol. by CC Wu (2011)
  48. Jennebach, S., Herzog, F., Aebersold, R. & Cramer, P. Crosslinking-MS analysis reveals RNA polymerase I domain architecture and basis of rRNA cleavage. Nucleic Acids Res. published online, doi:10.1093/nar/gks220 (6 March 2012). (10.1093/nar/gks220)
  49. Okamoto, T. et al. Analysis of the role of TFIIE in transcriptional regulation through structure-function studies of the TFIIEβ subunit. J. Biol. Chem. 273, 19866–19876 (1998). (10.1074/jbc.273.31.19866) / J. Biol. Chem. by T Okamoto (1998)
  50. Brun, I., Sentenac, A. & Werner, M. Dual role of the C34 subunit of RNA polymerase III in transcription initiation. EMBO J. 16, 5730–5741 (1997). (10.1093/emboj/16.18.5730) / EMBO J. by I Brun (1997)
  51. Vannini, A. et al. Molecular basis of RNA polymerase III transcription repression by Maf1. Cell 143, 59–70 (2010). (10.1016/j.cell.2010.09.002) / Cell by A Vannini (2010)
  52. Coin, F. et al. Mutations in the XPD helicase gene result in XP and TTD phenotypes, preventing interaction between XPD and the p44 subunit of TFIIH. Nat. Genet. 20, 184–188 (1998). (10.1038/2491) / Nat. Genet. by F Coin (1998)
  53. Lin, Y.C. & Gralla, J.D. Stimulation of the XPB ATP-dependent helicase by the beta subunit of TFIIE. Nucleic Acids Res. 33, 3072–3081 (2005). (10.1093/nar/gki623) / Nucleic Acids Res. by YC Lin (2005)
  54. Treutlein, B. et al. Dynamic architecture of a minimal RNA polymerase II open promoter complex. Mol. Cell 46, 136–146 (2012). (10.1016/j.molcel.2012.02.008) / Mol. Cell by B Treutlein (2012)
  55. Söding, J., Biegert, A. & Lupas, A.N. The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res. 33, W244–W248 (2005). (10.1093/nar/gki408) / Nucleic Acids Res. by J Söding (2005)
  56. Eswar, N., Eramian, D., Webb, B., Shen, M.Y. & Sali, A. Protein structure modeling with MODELLER. Methods Mol. Biol. 426, 145–159 (2008). (10.1007/978-1-60327-058-8_8) / Methods Mol. Biol. by N Eswar (2008)
  57. Colovos, C. & Yeates, T.O. Verification of protein structures: patterns of nonbonded atomic interactions. Protein Sci. 2, 1511–1519 (1993). (10.1002/pro.5560020916) / Protein Sci. by C Colovos (1993)
  58. Lüthy, R., Bowie, J.U. & Eisenberg, D. Assessment of protein models with three-dimensional profiles. Nature 356, 83–85 (1992). (10.1038/356083a0) / Nature by R Lüthy (1992)
  59. Davis, I.W. et al. MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res. 35, W375–W383 (2007). (10.1093/nar/gkm216) / Nucleic Acids Res. by IW Davis (2007)
Dates
Type When
Created 13 years, 1 month ago (July 1, 2012, 1:53 p.m.)
Deposited 2 years, 3 months ago (May 19, 2023, 12:32 a.m.)
Indexed 3 months, 2 weeks ago (May 6, 2025, 3:47 a.m.)
Issued 13 years, 1 month ago (July 1, 2012)
Published 13 years, 1 month ago (July 1, 2012)
Published Online 13 years, 1 month ago (July 1, 2012)
Published Print 13 years ago (Aug. 1, 2012)
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@article{Gr_nberg_2012, title={Architecture of the RNA polymerase II preinitiation complex and mechanism of ATP-dependent promoter opening}, volume={19}, ISSN={1545-9985}, url={http://dx.doi.org/10.1038/nsmb.2334}, DOI={10.1038/nsmb.2334}, number={8}, journal={Nature Structural & Molecular Biology}, publisher={Springer Science and Business Media LLC}, author={Grünberg, Sebastian and Warfield, Linda and Hahn, Steven}, year={2012}, month=jul, pages={788–796} }