1932

Abstract

Eukaryotic gene transcription requires the assembly at the promoter of a large preinitiation complex (PIC) that includes RNA polymerase II (Pol II) and the general transcription factors TFIID, TFIIA, TFIIB, TFIIF, TFIIE, and TFIIH. The size and complexity of Pol II, TFIID, and TFIIH have precluded their reconstitution from heterologous systems, and purification relies on scarce endogenous sources. Together with their conformational flexibility and the transient nature of their interactions, these limitations had precluded structural characterization of the PIC. In the last few years, however, progress in cryo–electron microscopy (cryo-EM) has made possible the visualization, at increasingly better resolution, of large PIC assemblies in different functional states. These structures can now be interpreted in near-atomic detail and provide an exciting structural framework for past and future functional studies, giving us unique mechanistic insight into the complex process of transcription initiation.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-biophys-070816-033751
2017-05-22
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/biophys/46/1/annurev-biophys-070816-033751.html?itemId=/content/journals/10.1146/annurev-biophys-070816-033751&mimeType=html&fmt=ahah

Literature Cited

  1. Akoulitchev S, Mäkelä TP, Weinberg RA, Reinberg D. 1.  1995. Requirement for TFIIH kinase activity in transcription by RNA polymerase II. Nature 377:557–60 [Google Scholar]
  2. Albright SR, Tjian R. 2.  2000. TAFs revisited: More data reveal new twists and confirm old ideas. Gene 242:1–13 [Google Scholar]
  3. Andel F III, Ladurner AG, Inouye C, Tjian R, Nogales E. 3.  1999. Three-dimensional structure of the human TFIID-IIA-IIB complex. Science 286:2153–56 [Google Scholar]
  4. Bernecky C, Grob P, Ebmeier CC, Nogales E, Taatjes DJ. 4.  2011. Molecular architecture of the human Mediator–RNA polymerase II–TFIIF assembly. PLOS Biol 9:e1000603 [Google Scholar]
  5. Bieniossek C, Papai G, Schaffitzel C, Garzoni F, Chaillet M. 5.  et al. 2013. The architecture of human general transcription factor TFIID core complex. Nature 493:699–702 [Google Scholar]
  6. Bleichenbacher M, Tan S, Richmond TJ. 6.  2003. Novel interactions between the components of human and yeast TFIIA/TBP/DNA complexes. J. Mol. Biol. 332:783–93 [Google Scholar]
  7. Brand M, Leurent C, Mallouh V, Tora L, Schultz P. 7.  1999. Three-dimensional structures of the TAFII-containing complexes TFIID and TFTC. Science 286:2151–53 [Google Scholar]
  8. Buratowski S, Hahn S, Guarente L, Sharp PA. 8.  1989. Five intermediate complexes in transcription initiation by RNA polymerase II. Cell 56:549–61 [Google Scholar]
  9. Buratowski S, Sopta M, Greenblatt J, Sharp PA. 9.  1991. RNA polymerase II-associated proteins are required for a DNA conformation change in the transcription initiation complex. PNAS 88:7509–13 [Google Scholar]
  10. Burke TW, Kadonaga JT. 10.  1997. The downstream core promoter element, DPE, is conserved from Drosophila to humans and is recognized by TAFII60 of Drosophila. Genes Dev. 11:3020–31 [Google Scholar]
  11. Burley SK, Roeder RG. 11.  1996. Biochemistry and structural biology of transcription factor IID (TFIID). Annu. Rev. Biochem. 65:769–99 [Google Scholar]
  12. Bushnell DA, Westover KD, Davis RE, Kornberg RD. 12.  2004. Structural basis of transcription: an RNA polymerase II-TFIIB cocrystal at 4.5 angstroms. Science 303:983–88 [Google Scholar]
  13. Cai G, Chaban YL, Imasaki T, Kovacs JA, Calero G. 13.  et al. 2012. Interaction of the mediator head module with RNA polymerase II. Structure 20:899–910 [Google Scholar]
  14. Chakraborty A, Wang D, Ebright YW, Korlann Y, Kortkhonjia E. 14.  et al. 2012. Opening and closing of the bacterial RNA polymerase clamp. Science 337:591–95 [Google Scholar]
  15. Chen H-T, Warfield L, Hahn S. 15.  2007. The positions of TFIIF and TFIIE in the RNA polymerase II transcription preinitiation complex. Nat. Struct. Mol. Biol. 14:696–703 [Google Scholar]
  16. Cheung AC, Cramer P. 16.  2011. Structural basis of RNA polymerase II backtracking, arrest and reactivation. Nature 471:249–53 [Google Scholar]
  17. Chung W-H, Craighead JL, Chang W-H, Ezeokonkwo C, Bareket-Samish A. 17.  et al. 2003. RNA polymerase II/TFIIF structure and conserved organization of the initiation complex. Mol. Cell 12:1003–13 [Google Scholar]
  18. Cianfrocco MA, Kassavetis GA, Grob P, Fang J, Juven-Gershon T. 18.  et al. 2013. Human TFIID binds to core promoter DNA in a reorganized structural state. Cell 152:120–31 [Google Scholar]
  19. Cianfrocco MA, Nogales E. 19.  2013. Regulatory interplay between TFIID's conformational transitions and its modular interaction with core promoter DNA. Transcription 4:120–26 [Google Scholar]
  20. Conaway RC, Conaway JW. 20.  1993. General initiation factors for RNA polymerase II. Annu. Rev. Biochem. 62:161–90 [Google Scholar]
  21. Cramer P. 21.  2014. A tale of chromatin and transcription in 100 structures. Cell 159:985–94 [Google Scholar]
  22. Cramer P, Bushnell DA, Fu J, Gnatt AL, Maier-Davis B. 22.  et al. 2000. Architecture of RNA polymerase II and implications for the transcription mechanism. Science 288:640–49 [Google Scholar]
  23. Cramer P, Bushnell DA, Kornberg RD. 23.  2001. Structural basis of transcription: RNA polymerase II at 2.8 Ångstrom resolution. Science 292:1863–76 [Google Scholar]
  24. Dotson MR, Yuan CX, Roeder RG, Myers LC, Gustafsson CM. 24.  et al. 2000. Structural organization of yeast and mammalian mediator complexes. PNAS 97:14307–10 [Google Scholar]
  25. Dubrovskaya V, Lavigne AC, Davidson I, Acker J, Staub A, Tora L. 25.  1996. Distinct domains of hTAFII100 are required for functional interaction with transcription factor TFIIF beta (RAP30) and incorporation into the TFIID complex. EMBO J 15:3702–12 [Google Scholar]
  26. Dvir A, Conaway JW, Conaway RC. 26.  2001. Mechanism of transcription initiation and promoter escape by RNA polymerase II. Curr. Opin. Genet. Dev. 11:209–14 [Google Scholar]
  27. Ebright RH. 27.  2000. RNA polymerase: structural similarities between bacterial RNA polymerase and eukaryotic RNA polymerase II. J. Mol. Biol. 304:687–98 [Google Scholar]
  28. Gaiser F, Tan S, Richmond TJ. 28.  2000. Novel dimerization fold of RAP30/RAP74 in human TFIIF at 1.7 Å resolution. J. Mol. Biol. 302:1119–27 [Google Scholar]
  29. Gibbons BJ, Brignole EJ, Azubel M, Murakami K, Voss NR. 29.  et al. 2012. Subunit architecture of general transcription factor TFIIH. PNAS 109:1949–54 [Google Scholar]
  30. Gnatt AL, Cramer P, Fu J, Bushnell DA, Kornberg RD. 30.  2001. Structural basis of transcription: an RNA polymerase II elongation complex at 3.3 Å resolution. Science 292:1876–82 [Google Scholar]
  31. Goodrich JA, Cutler G, Tjian R. 31.  1996. Contacts in context: promoter specificity and macromolecular interactions in transcription. Cell 84:825–30 [Google Scholar]
  32. Goodrich JA, Tjian R. 32.  1994. Transcription factors IIE and IIH and ATP hydrolysis direct promoter clearance by RNA polymerase II. Cell 77:145–56 [Google Scholar]
  33. Grob P, Cruse MJ, Inouye C, Peris M, Penczek PA. 33.  et al. 2006. Cryo-electron microscopy studies of human TFIID: conformational breathing in the integration of gene regulatory cues. Structure 14:511–20 [Google Scholar]
  34. Groft CM, Uljon SN, Wang R, Werner MH. 34.  1998. Structural homology between the Rap30 DNA-binding domain and linker histone H5: implications for preinitiation complex assembly. PNAS 95:9117–22 [Google Scholar]
  35. Grunberg S, Warfield L, Hahn S. 35.  2012. Architecture of the RNA polymerase II preinitiation complex and mechanism of ATP-dependent promoter opening. Nat. Struct. Mol. Biol. 19:788–96 [Google Scholar]
  36. He Y, Fang J, Taatjes DJ, Nogales E. 36.  2013. Structural visualization of key steps in human transcription initiation. Nature 495:481–86 [Google Scholar]
  37. He Y, Yan C, Fang J, Inouye C, Tjian R. 37.  et al. 2016. Near-atomic resolution visualization of human transcription promoter opening. Nature 533:359–65 [Google Scholar]
  38. Hisatake K, Ohta T, Takada R, Guermah M, Horikoshi M. 38.  et al. 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. PNAS 92:8195–99 [Google Scholar]
  39. Holstege FC, Tantin D, Carey M, van der Vliet PC, Timmers HT. 39.  1995. The requirement for the basal transcription factor IIE is determined by the helical stability of promoter DNA. EMBO J 14:810–19 [Google Scholar]
  40. Kim T-K, Ebright RH, Reinberg D. 40.  2000. Mechanism of ATP-dependent promoter melting by transcription factor IIH. Science 288:1418–22 [Google Scholar]
  41. Kokubo T, Swanson MJ, Nishikawa J-I, Hinnebusch AG, Nakatani Y. 41.  1998. The yeast TAF145 inhibitory domain and TFIIA competitively bind to TATA-binding protein. Mol. Cell. Biol. 18:1003–12 [Google Scholar]
  42. Kostrewa D, Zeller ME, Armache K-J, Seizl M, Leike K. 42.  et al. 2009. RNA polymerase II–TFIIB structure and mechanism of transcription initiation. Nature 462:323–30 [Google Scholar]
  43. Lariviere L, Plaschka C, Seizl M, Wenzeck L, Kurth F, Cramer P. 43.  2012. Structure of the Mediator head module. Nature 492:448–51 [Google Scholar]
  44. Lariviere L, Seizl M, Cramer P. 44.  2012. A structural perspective on Mediator function. Curr. Opin. Cell Biol. 24:305–13 [Google Scholar]
  45. Lee D-H, Gershenzon N, Gupta M, Ioshikhes IP, Reinberg D, Lewis BA. 45.  2005. Functional characterization of core promoter elements: the downstream core element is recognized by TAF1. Mol. Cell. Biol. 25:9674–86 [Google Scholar]
  46. Leschziner AE, Nogales E. 46.  2006. 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. 153:284–99 [Google Scholar]
  47. Leurent C, Sanders SL, Demeny MA, Garbett KA, Ruhlmann C. 47.  et al. 2004. Mapping key functional sites within yeast TFIID. EMBO J 23:719–27 [Google Scholar]
  48. Leurent C, Sanders SL, Ruhlmann C, Mallouh V, Weil PA. 48.  et al. 2002. Mapping histone fold TAFs within yeast TFIID. EMBO J 21:3424–33 [Google Scholar]
  49. Liu W-L, Coleman RA, Grob P, King DS, Florens L. 49.  et al. 2008. Structural changes in TAF4b-TFIID correlate with promoter selectivity. Mol. Cell 29:81–91 [Google Scholar]
  50. Liu W-L, Coleman RA, Ma E, Grob P, Yang JL. 50.  et al. 2009. Structures of three distinct activator–TFIID complexes. Genes Dev 23:1510–21 [Google Scholar]
  51. Liu X, Bushnell DA, Wang D, Calero G, Kornberg RD. 51.  2010. Structure of an RNA polymerase II–TFIIB complex and the transcription initiation mechanism. Science 327:206–9 [Google Scholar]
  52. Louder RK, He Y, López-Blanco JR, Fang J, Chacón P, Nogales E. 52.  2016. Structure of promoter-bound TFIID and model of human pre-initiation complex assembly. Nature 531:604–9 [Google Scholar]
  53. Luo J, Cimermancic P, Viswanath S, Ebmeier CC, Kim B. 53.  et al. 2015. Architecture of the human and yeast general transcription and DNA repair factor TFIIH. Mol. Cell 59:794–806 [Google Scholar]
  54. Matsui T, Segall J, Weil PA, Roeder RG. 54.  1980. Multiple factors required for accurate initiation of transcription by purified RNA polymerase II. J. Biol. Chem. 255:11992–96 [Google Scholar]
  55. McMullan G, Faruqi AR, Henderson R. 55.  2016. Direct electron detectors. Methods Enzymol 579:1–17 [Google Scholar]
  56. Mühlbacher W, Sainsbury S, Hemann M, Hantsche M, Neyer S. 56.  et al. 2014. Conserved architecture of the core RNA polymerase II initiation complex. Nat. Commun. 5:4310 [Google Scholar]
  57. Murakami K, Elmlund H, Kalisman N, Bushnell DA, Adams CM. 57.  et al. 2013. Architecture of an RNA polymerase II transcription pre-initiation complex. Science 342:1238724 [Google Scholar]
  58. Murakami K, Tsai KL, Kalisman N, Bushnell DA, Asturias FJ, Kornberg RD. 58.  2015. Structure of an RNA polymerase II preinitiation complex. PNAS 112:13543–48 [Google Scholar]
  59. Nogales E. 59.  2016. The development of cryo-EM into a mainstream structural biology technique. Nat. Methods 13:24–27 [Google Scholar]
  60. Nogales E, Louder RK, He Y. 60.  2016. Cryo-EM in the study of challenging systems: the human transcription pre-initiation complex. Curr. Opin. Struct. Biol. 40:120–27 [Google Scholar]
  61. Nogales E, Scheres SH. 61.  2015. Cryo-EM: a unique tool for the visualization of macromolecular complexity. Mol. Cell 58:677–89 [Google Scholar]
  62. Papai G, Tripathi MK, Ruhlmann C, Werten S, Crucifix C. 62.  et al. 2009. Mapping the initiator binding Taf2 subunit in the structure of hydrated yeast TFIID. Structure 17:363–73 [Google Scholar]
  63. Plaschka C, Hantsche M, Dienemann C, Burzinski C, Plitzko J, Cramer P. 63.  2016. Transcription initiation complex structures elucidate DNA opening. Nature 533:353–58 [Google Scholar]
  64. Plaschka C, Larivière L, Wenzeck L, Seizl M, Hemann M. 64.  et al. 2015. Architecture of the RNA polymerase II–Mediator core initiation complex. Nature 518:376–80 [Google Scholar]
  65. Poss ZC, Ebmeier CC, Taatjes DJ. 65.  2013. The Mediator complex and transcription regulation. Crit. Rev. Biochem. Mol. Biol. 48:575–608 [Google Scholar]
  66. Robinson PJ, Bushnell DA, Trnka MJ, Burlingame AL, Kornberg RD. 66.  2012. Structure of the Mediator Head module bound to the carboxy-terminal domain of RNA polymerase II. PNAS 109:17931–35 [Google Scholar]
  67. Robinson PJ, Trnka MJ, Bushnell DA, Davis RE, Mattei P-J. 67.  et al. 2016. Structure of a complete Mediator-RNA polymerase II pre-initiation complex. Cell 166:1411–22e16 [Google Scholar]
  68. Roeder RG. 68.  1996. Nuclear RNA polymerases: role of general initiation factors and cofactors in eukaryotic transcription. Methods Enzymol 273:165–71 [Google Scholar]
  69. Roeder RG. 69.  1996. The role of general initiation factors in transcription by RNA polymerase II. Trends Biochem. Sci. 21:327–35 [Google Scholar]
  70. Ruppert S, Tjian R. 70.  1995. Human TAFII250 interacts with RAP74: implications for RNA polymerase II initiation. Genes Dev 9:2747–55 [Google Scholar]
  71. Scheres SH. 71.  2016. Processing of structurally heterogeneous cryo-EM data in RELION. Methods Enzymol 579:125–57 [Google Scholar]
  72. Schultz P, Fribourg S, Poterszman A, Mallouh V, Moras D, Egly JM. 72.  2000. Molecular structure of human TFIIH. Cell 102:599–607 [Google Scholar]
  73. Struhl K. 73.  1987. Promoters, activator proteins, and the mechanism of transcriptional initiation in yeast. Cell 49:295–97 [Google Scholar]
  74. Taatjes DJ, Näär AM, Andel F III, Nogales E, Tjian R. 74.  2002. Structure, function, and activator-induced conformations of the CRSP coactivator. Science 295:1058–62 [Google Scholar]
  75. Theisen JW, Lim CY, Kadonaga JT. 75.  2010. Three key subregions contribute to the function of the downstream RNA polymerase II core promoter. Mol. Cell. Biol. 30:3471–79 [Google Scholar]
  76. Thomas MC, Chiang C-M. 76.  2006. The general transcription machinery and general cofactors. Crit. Rev. Biochem. Mol. Biol. 41:105–78 [Google Scholar]
  77. Trowitzsch S, Viola C, Scheer E, Conic S, Chavant V. 77.  et al. 2015. Cytoplasmic TAF2–TAF8–TAF10 complex provides evidence for nuclear holo–TFIID assembly from preformed submodules. Nat. Commun. 6:6011 [Google Scholar]
  78. Tsai FT, Sigler PB. 78.  2000. Structural basis of preinitiation complex assembly on human pol II promoters. EMBO J 19:25–36 [Google Scholar]
  79. Tsai KL, Tomomori-Sato C, Sato S, Conaway RC, Conaway JW, Asturias FJ. 79.  2014. Subunit architecture and functional modular rearrangements of the transcriptional mediator complex. Cell 157:1430–44 [Google Scholar]
  80. Verrijzer CP, Chen J-L, Yokomori K, Tjian R. 80.  1995. Binding of TAFs to core elements directs promoter selectivity by RNA polymerase II. Cell 81:1115–25 [Google Scholar]
  81. Wang D, Bushnell DA, Westover KD, Kaplan CD, Kornberg RD. 81.  2006. Structural basis of transcription: role of the trigger loop in substrate specificity and catalysis. Cell 127:941–54 [Google Scholar]
  82. Wang H, Curran EC, Hinds TR, Wang EH, Zheng N. 82.  2014. Crystal structure of a TAF1-TAF7 complex in human transcription factor IID reveals a promoter binding module. Cell Res 24:1433–44 [Google Scholar]
  83. Wu S-Y, Chiang C-M. 83.  2001. TATA-binding protein-associated factors enhance the recruitment of RNA polymerase II by transcriptional activators. J. Biol. Chem. 276:34235–43 [Google Scholar]
  84. Yakovchuk P, Gilman B, Goodrich JA, Kugel JF. 84.  2010. RNA polymerase II and TAFs undergo a slow isomerization after the polymerase is recruited to promoter-bound TFIID. J. Mol. Biol. 397:57–68 [Google Scholar]
  85. Zhang Z, Boskovic Z, Hussain MM, Hu W, Inouye C. 85.  et al. 2015. Chemical perturbation of an intrinsically disordered region of TFIID distinguishes two modes of transcription initiation. eLife 4:e07777 [Google Scholar]
/content/journals/10.1146/annurev-biophys-070816-033751
Loading
/content/journals/10.1146/annurev-biophys-070816-033751
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error