Skip to main content
SpringerLink
Log in

The Structures of Eukaryotic Transcription Pre-initiation Complexes and Their Functional Implications

  • Chapter
  • First Online:
Book cover Macromolecular Protein Complexes II: Structure and Function

Part of the book series: Subcellular Biochemistry ((SCBI,volume 93))

Abstract

Transcription is a highly regulated process that supplies living cells with coding and non-coding RNA molecules. Failure to properly regulate transcription is associated with human pathologies, including cancers. RNA polymerase II is the enzyme complex that synthesizes messenger RNAs that are then translated into proteins. In spite of its complexity, RNA polymerase requires a plethora of general transcription factors to be recruited to the transcription start site as part of a large transcription pre-initiation complex, and to help it gain access to the transcribed strand of the DNA. This chapter reviews the structure and function of these eukaryotic transcription pre-initiation complexes, with a particular emphasis on two of its constituents, the multisubunit complexes TFIID and TFIIH. We also compare the overall architecture of the RNA polymerase II pre-initiation complex with those of RNA polymerases I and III, involved in transcription of ribosomal RNA and non-coding RNAs such as tRNAs and snRNAs, and discuss the general, conserved features that are applicable to all eukaryotic RNA polymerase systems.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.00
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Abascal-Palacios G, Ramsay EP, Beuron F, Morris E, Vannini A (2018) Structural basis of RNA polymerase III transcription initiation. Nature 553:301–306

    Article  CAS  PubMed  Google Scholar 

  • Abdulrahman W et al (2013) ARCH domain of XPD, an anchoring platform for CAK that conditions TFIIH DNA repair and transcription activities. Proc Natl Acad Sci USA 110:E633–642

    Article  PubMed  PubMed Central  Google Scholar 

  • Alekseev S, Nagy Z, Sandoz J, Weiss A, Egly J-M, Le May N, Coin F (2017) Transcription without XPB establishes a unified helicase-independent mechanism of promoter opening in eukaryotic gene expression. Mol Cell 65:504–513.e505

    Article  CAS  PubMed  Google Scholar 

  • Anandapadamanaban M et al (2013) High-resolution structure of TBP with TAF1 reveals anchoring patterns in transcriptional regulation. Nat Struct Mol Biol 20:1008–1014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Andel F, Ladurner AG, Inouye C, Tjian R, Nogales E (1999) Three-dimensional structure of the human TFIID-IIA-IIB complex. Science 286:2153–2156

    Article  CAS  PubMed  Google Scholar 

  • Andersen G et al (1997) The structure of cyclin H: common mode of kinase activation and specific features. EMBO J 16:958–967

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arimbasseri AG, Maraia RJ (2015) Mechanism of transcription termination by RNA polymerase III utilizes a non-template strand sequence-specific signal element. Mol Cell 58:1124–1132

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Asturias FJ, Jiang YW, Myers LC, Gustafsson CM, Kornberg RD (1999) Conserved structures of mediator and RNA polymerase II holoenzyme. Science 283:985–987

    Article  CAS  PubMed  Google Scholar 

  • Baek HJ, Malik S, Qin J, Roeder RG (2002) Requirement of TRAP/mediator for both activator-independent and activator-dependent transcription in conjunction with TFIID-associated TAF(II)s. Mol Cell Biol 22:2842–2852

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bancerek J et al (2013) CDK8 kinase phosphorylates transcription factor STAT1 to selectively regulate the interferon response. Immunity 38:250–262

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bardeleben C, Kassavetis GA, Geiduschek EP (1994) Encounters of Saccharomyces cerevisiae RNA polymerase III with its transcription factors during RNA chain elongation. J Mol Biol 235:1193–1205

    Article  CAS  PubMed  Google Scholar 

  • Barnes CO et al (2015) Crystal structure of a transcribing RNA polymerase II complex reveals a complete transcription bubble. Mol Cell 59:258–269

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bedwell GJ, Appling FD, Anderson SJ, Schneider DA (2012) Efficient transcription by RNA polymerase I using recombinant core factor. Gene 492:94–99

    Article  CAS  PubMed  Google Scholar 

  • Berico P, Coin F (2017) Is TFIIH the new Achilles heel of cancer cells? Transcription 9:47–51

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bieniossek C et al (2013) The architecture of human general transcription factor TFIID core complex. Nature 493:699–702

    Article  CAS  PubMed  Google Scholar 

  • Bienstock RJ, Skorvaga M, Mandavilli BS, Van Houten B (2003) Structural and functional characterization of the human DNA repair helicase XPD by comparative molecular modeling and site-directed mutagenesis of the bacterial repair protein UvrB. J Biol Chem 278:5309–5316

    Article  CAS  PubMed  Google Scholar 

  • Bier M, Fath S, Tschochner H (2004) The composition of the RNA polymerase I transcription machinery switches from initiation to elongation mode. FEBS Lett 564:41–46

    Article  CAS  PubMed  Google Scholar 

  • Bleichenbacher M, Tan S, Richmond TJ (2003) Novel interactions between the components of human and yeast TFIIA/TBP/DNA complexes. J Mol Biol 332:783–793

    Article  CAS  PubMed  Google Scholar 

  • Bordi L, Cioci F, Camilloni G (2001) In vivo binding and hierarchy of assembly of the yeast RNA polymerase I transcription factors. Mol Biol Cell 12:753–760

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Borggrefe T, Yue X (2011) Interactions between subunits of the Mediator complex with gene-specific transcription factors. Semin Cell Dev Biol 22:759–768

    Article  CAS  PubMed  Google Scholar 

  • Borggrefe T, Davis R, Erdjument-Bromage H, Tempst P, Kornberg RD (2002) A complex of the Srb8, -9, -10, and -11 transcriptional regulatory proteins from yeast. J Biol Chem 277:44202–44207

    Article  CAS  PubMed  Google Scholar 

  • Botta E, Nardo T, Lehmann AR, Egly J-M, Pedrini AM, Stefanini M (2002) Reduced level of the repair/transcription factor TFIIH in trichothiodystrophy. Hum Mol Genet 11:2919–2928

    Article  CAS  PubMed  Google Scholar 

  • Brand M, Leurent C, Mallouh V, Tora L, Schultz P (1999) Three-dimensional structures of the TAFII-containing complexes TFIID and TFTC. Science 286:2151–2153

    Article  CAS  PubMed  Google Scholar 

  • Brun I, Sentenac A, Werner M (1997) Dual role of the C34 subunit of RNA polymerase III in transcription initiation. EMBO J 16:5730–5741

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brzovic PS et al (2011) The acidic transcription activator Gcn4 binds the mediator subunit Gal11/Med15 using a simple protein interface forming a fuzzy complex. Mol Cell 44:942–953

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Buechner CN, Heil K, Michels G, Carell T, Kisker C, Tessmer I (2014) Strand-specific recognition of DNA damages by XPD provides insights into nucleotide excision repair substrate versatility. J Biol Chem 289:3613–3624

    Article  CAS  PubMed  Google Scholar 

  • Buratowski S, Hahn S, Guarente L, Sharp PA (1989) Five intermediate complexes in transcription initiation by RNA polymerase II. Cell 56:549–561

    Article  CAS  PubMed  Google Scholar 

  • Burke TW, Kadonaga JT (1996) Drosophila TFIID binds to a conserved downstream basal promoter element that is present in many TATA-box-deficient promoters. Genes Dev 10:711–724

    Article  CAS  PubMed  Google Scholar 

  • Burke TW, Kadonaga JT (1997) The downstream core promoter element, DPE, is conserved from Drosophila to humans and is recognized by TAFII60 of Drosophila. Genes Dev 11:3020–3031

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bushnell DA, Westover KD, Davis RE, Kornberg RD (2004) Structural basis of transcription: an RNA polymerase II-TFIIB cocrystal at 4.5 Angstroms. Science 303:983–988

    Article  CAS  PubMed  Google Scholar 

  • Busso D, Keriel A, Sandrock B, Poterszman A, Gileadi O, Egly JM (2000) Distinct regions of MAT1 regulate cdk7 kinase and TFIIH transcription activities. J Biol Chem 275:22815–22823

    Article  CAS  PubMed  Google Scholar 

  • Cabarcas S, Schramm L (2011) RNA polymerase III transcription in cancer: the BRF2 connection. Mol Cancer 10:47

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cabart P, Murphy S (2001) BRFU, a TFIIB-like factor, is directly recruited to the TATA-box of polymerase III small nuclear RNA gene promoters through its interaction with TATA-binding protein. J Biol Chem 276:43056–43064

    Article  CAS  PubMed  Google Scholar 

  • Cai G, Imasaki T, Takagi Y, Asturias FJ (2009) Mediator structural conservation and implications for the regulation mechanism. Structure 17:559–567

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carninci P et al (2006) Genome-wide analysis of mammalian promoter architecture and evolution. Nat Genet 38:626–635

    Article  CAS  PubMed  Google Scholar 

  • Chalkley GE, Verrijzer CP (1999) DNA binding site selection by RNA polymerase II TAFs: a TAF(II)250-TAF(II)150 complex recognizes the initiator. EMBO J 18:4835–4845

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chang WH, Kornberg RD (2000) Electron crystal structure of the transcription factor and DNA repair complex, core TFIIH. Cell 102:609–613

    Article  CAS  PubMed  Google Scholar 

  • Chen W, Struhl K (1985) Yeast mRNA initiation sites are determined primarily by specific sequences, not by the distance from the TATA element. EMBO J 4:3273–3280

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen X, Farmer G, Zhu H, Prywes R, Prives C (1993) Cooperative DNA binding of p53 with TFIID (TBP): a possible mechanism for transcriptional activation. Genes Dev 7:1837–1849

    Article  CAS  PubMed  Google Scholar 

  • Chen JL, Attardi LD, Verrijzer CP, Yokomori K, Tjian R (1994) Assembly of recombinant TFIID reveals differential coactivator requirements for distinct transcriptional activators. Cell 79:93–105

    Article  CAS  PubMed  Google Scholar 

  • Cheung ACM, Cramer P (2011) Structural basis of RNA polymerase II backtracking, arrest and reactivation. Nature 471:249–253

    Article  CAS  PubMed  Google Scholar 

  • Cianfrocco MA, Kassavetis GA, Grob P, Fang J, Juven-Gershon T, Kadonaga JT, Nogales E (2013) Human TFIID binds to core promoter DNA in a reorganized structural state. Cell 152:120–131

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cleaver JE, Thompson LH, Richardson AS, States JC (1999) A summary of mutations in the UV-sensitive disorders: xeroderma pigmentosum, Cockayne syndrome, and trichothiodystrophy. Hum Mutat 14:9–22

    Article  CAS  PubMed  Google Scholar 

  • Coin F, Marinoni JC, Rodolfo C, Fribourg S, Pedrini AM, Egly JM (1998) 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

    Article  CAS  PubMed  Google Scholar 

  • Coin F, Oksenych V, Egly J-M (2007) Distinct roles for the XPB/p52 and XPD/p44 subcomplexes of TFIIH in damaged DNA opening during nucleotide excision repair. Mol Cell 26:245–256

    Article  CAS  PubMed  Google Scholar 

  • Colbert T, Hahn S (1992) A yeast TFIIB-related factor involved in RNA polymerase III transcription. Genes Dev 6:1940–1949

    Article  CAS  PubMed  Google Scholar 

  • Comai L, Tanese N, Tjian R (1992) The TATA-binding protein and associated factors are integral components of the RNA polymerase I transcription factor, SL1. Cell 68:965–976

    Article  CAS  PubMed  Google Scholar 

  • Compe E, Egly J-M (2012) TFIIH: when transcription met DNA repair. Nat Rev Mol Cell Biol 13:343–354

    Article  CAS  PubMed  Google Scholar 

  • Conesa C, Swanson RN, Schultz P, Oudet P, Sentenac A (1993) On the subunit composition, stoichiometry, and phosphorylation of the yeast transcription factor TFIIIC/tau. J Biol Chem 268:18047–18052

    CAS  PubMed  Google Scholar 

  • Cramer P et al (2000) Architecture of RNA polymerase II and implications for the transcription mechanism. Science 288:640–649

    Article  CAS  PubMed  Google Scholar 

  • Cramer P, Bushnell DA, Kornberg RD (2001) Structural basis of transcription: RNA polymerase II at 2.8 angstrom resolution. Science 292:1863–1876

    Article  CAS  PubMed  Google Scholar 

  • Davis JA, Takagi Y, Kornberg RD, Asturias FA (2002) Structure of the yeast RNA polymerase II holoenzyme: mediator conformation and polymerase interaction. Mol Cell 10:409–415

    Article  CAS  PubMed  Google Scholar 

  • Deng W, Roberts SGE (2005) A core promoter element downstream of the TATA box that is recognized by TFIIB. Genes Dev 19:2418–2423

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Denissov S et al (2007) Identification of novel functional TBP-binding sites and general factor repertoires. EMBO J 26:944–954

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Devault A et al (1995) MAT1 (‘menage à trois’) a new RING finger protein subunit stabilizing cyclin H-cdk7 complexes in starfish and Xenopus CAK. EMBO J 14:5027–5036

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dieci G, Sentenac A (1996) Facilitated recycling pathway for RNA polymerase III. Cell 84:245–252

    Article  CAS  PubMed  Google Scholar 

  • Dieci G, Bosio MC, Fermi B, Ferrari R (2013) Transcription reinitiation by RNA polymerase III. Biochim Biophys Acta 1829:331–341

    Article  CAS  PubMed  Google Scholar 

  • Dienemann C, Schwalb B, Schilbach S, Cramer P (2018) Promoter distortion and opening in the RNA polymerase II cleft. Mol Cell 73:97–106.e4

    Google Scholar 

  • Donner AJ, Ebmeier CC, Taatjes DJ, Espinosa JM (2010) CDK8 is a positive regulator of transcriptional elongation within the serum response network. Nat Struct Mol Biol 17:194–201

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dotson MR et al (2000) Structural organization of yeast and mammalian mediator complexes. Proc Natl Acad Sci USA 97:14307–14310

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Drapkin R, Reardon JT, Ansari A, Huang J-C, Zawel L, Ahn KJ, Sancar A, Reinberg D (1994) Dual role of TFIIH in DNA excision repair and in transcription by RNA polymerase II. Nature 368:769–772

    Google Scholar 

  • Dubaele S, Proietti De Santis L, Bienstock RJ, Keriel A, Stefanini M, Van Houten B, Egly J-M (2003) Basal transcription defect discriminates between xeroderma pigmentosum and trichothiodystrophy in XPD patients. Mol Cell 11:1635–1646

    Article  CAS  PubMed  Google Scholar 

  • Dubrovskaya V, Lavigne AC, Davidson I, Acker J, Staub A, Tora L (1996) Distinct domains of hTAFII100 are required for functional interaction with transcription factor TFIIF beta (RAP30) and incorporation into the TFIID complex. EMBO J 15:3702–3712

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ducrot C, Lefebvre O, Landrieux E, Guirouilh-Barbat J, Sentenac A, Acker J (2006) Reconstitution of the yeast RNA polymerase III transcription system with all recombinant factors. J Biol Chem 281:11685–11692

    Article  CAS  PubMed  Google Scholar 

  • Ehara H, Yokoyama T, Shigematsu H, Yokoyama S, Shirouzu M, Sekine S-I (2017) Structure of the complete elongation complex of RNA polymerase II with basal factors. Science 357:921–924

    Article  CAS  PubMed  Google Scholar 

  • Elmlund H et al (2009) Cryo-EM reveals promoter DNA binding and conformational flexibility of the general transcription factor TFIID. Structure 17:1442–1452

    Article  CAS  PubMed  Google Scholar 

  • Engel C, Sainsbury S, Cheung AC, Kostrewa D, Cramer P (2013) RNA polymerase I structure and transcription regulation. Nature 502:650–655

    Article  CAS  PubMed  Google Scholar 

  • Engel C, Plitzko J, Cramer P (2016) RNA polymerase I-Rrn3 complex at 4.8 Å resolution. Nat Commun 7:12129

    Google Scholar 

  • Engel C et al (2017) Structural basis of RNA polymerase I transcription initiation. Cell 169:120–131.e22

    Article  CAS  PubMed  Google Scholar 

  • Engel C, Neyer S, Cramer P (2018) Distinct mechanisms of transcription initiation by RNA polymerases I and II. Annu Rev Biophys 47:425–446

    Article  CAS  PubMed  Google Scholar 

  • Fan L, Arvai AS, Cooper PK, Iwai S, Hanaoka F, Tainer JA (2006) Conserved XPB core structure and motifs for DNA unwinding: implications for pathway selection of transcription or excision repair. Mol Cell 22:27–37

    Article  CAS  PubMed  Google Scholar 

  • Fan L et al (2008) XPD helicase structures and activities: insights into the cancer and aging phenotypes from XPD mutations. Cell 133:789–800

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fernández-Tornero C et al (2013) Crystal structure of the 14-subunit RNA polymerase I. Nature 502:644–649

    Article  CAS  PubMed  Google Scholar 

  • Firestein R et al (2008) CDK8 is a colorectal cancer oncogene that regulates beta-catenin activity. Nature 455:547–551

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fishburn J, Tomko E, Galburt E, Hahn S (2015) Double-stranded DNA translocase activity of transcription factor TFIIH and the mechanism of RNA polymerase II open complex formation. Proc Natl Acad Sci USA 112:3961–3966

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fisher RP (2018) Cdk7: a kinase at the core of transcription and in the crosshairs of cancer drug discovery. Transcription 10:47–56

    Google Scholar 

  • Fisher RP, Morgan DO (1994) A novel cyclin associates with MO15/CDK7 to form the CDK-activating kinase. Cell 78:713–724

    Article  CAS  PubMed  Google Scholar 

  • Fisher RP, Jin P, Chamberlin HM, Morgan DO (1995) Alternative mechanisms of CAK assembly require an assembly factor or an activating kinase. Cell 83:47–57

    Article  CAS  PubMed  Google Scholar 

  • Flanagan PM, Kelleher RJ, Sayre MH, Tschochner H, Kornberg RD (1991) A mediator required for activation of RNA polymerase II transcription in vitro. Nature 350:436–438

    Article  CAS  PubMed  Google Scholar 

  • Friedrich JK, Panov KI, Cabart P, Russell J, Zomerdijk JCBM (2005) TBP-TAF complex SL1 directs RNA polymerase I pre-initiation complex formation and stabilizes upstream binding factor at the rDNA promoter. J Biol Chem 280:29551–29558

    Article  CAS  PubMed  Google Scholar 

  • Gannon F et al (1979) Organisation and sequences at the 5′ end of a cloned complete ovalbumin gene. Nature 278:428–434

    Article  CAS  PubMed  Google Scholar 

  • Gegonne A, Weissman JD, Zhou M, Brady JN, Singer DS (2006) TAF7: a possible transcription initiation check-point regulator. Proc Natl Acad Sci USA 103:602–607

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gervais V et al (2018) Small molecule-based targeting of TTD-A dimerization to control TFIIH transcriptional activity represents a potential strategy for anticancer therapy. J Biol Chem 293:14974–14988

    Article  PubMed  PubMed Central  Google Scholar 

  • Ghazy MA, Brodie SA, Ammerman ML, Ziegler LM, Ponticelli AS (2004) Amino acid substitutions in yeast TFIIF confer upstream shifts in transcription initiation and altered interaction with RNA polymerase II. Mol Cell Biol 24:10975–10985

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gibbons BJ et al (2012) Subunit architecture of general transcription factor TFIIH. Proc Natl Acad Sci USA 109:1949–1954

    Article  PubMed  PubMed Central  Google Scholar 

  • Giglia-Mari G et al (2004) A new, tenth subunit of TFIIH is responsible for the DNA repair syndrome trichothiodystrophy group A. Nat Genet 36:714–719

    Article  CAS  PubMed  Google Scholar 

  • Gnatt AL, Cramer P, Fu J, Bushnell DA, Kornberg RD (2001) Structural basis of transcription: an RNA polymerase II elongation complex at 3.3 A resolution. Science 292:1876–1882

    Article  CAS  PubMed  Google Scholar 

  • Gorski JJ, Pathak S, Panov K, Kasciukovic T, Panova T, Russell J, Zomerdijk JCBM (2007) A novel TBP-associated factor of SL1 functions in RNA polymerase I transcription. EMBO J 26:1560–1568

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gouge J et al (2015) Redox signaling by the RNA polymerase III TFIIB-related factor Brf2. Cell 163:1375–1387

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gouge J et al (2017) Molecular mechanisms of Bdp1 in TFIIIB assembly and RNA polymerase III transcription initiation. Nat Commun 8:130

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Greber BJ, Nguyen THD, Fang J, Afonine PV, Adams PD, Nogales E (2017) The cryo-electron microscopy structure of human transcription factor IIH. Nature 549:414–417

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Greber BJ, Toso D, Fang J, Nogales E (2019) The complete structure of the human TFIIH core complex. eLife 8:e44771

    Google Scholar 

  • Grob P, Cruse MJ, Inouye C, Peris M, Penczek PA, Tjian R, Nogales E (2006) Cryo-electron microscopy studies of human TFIID: conformational breathing in the integration of gene regulatory cues. Structure 14:511–520

    Article  CAS  PubMed  Google Scholar 

  • Grünberg S, Warfield L, Hahn S (2012) Architecture of the RNA polymerase II preinitiation complex and mechanism of ATP-dependent promoter opening. Nat Struct Mol Biol 19:788–796

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guzder SN, Sung P, Bailly V, Prakash L, Prakash S (1994) RAD25 is a DNA helicase required for DNA repair and RNA polymerase II transcription. Nature 369:578–581

    Article  CAS  PubMed  Google Scholar 

  • Han Y, Yan C, Nguyen THD, Jackobel AJ, Ivanov I, Knutson BA, He Y (2017) Structural mechanism of ATP-independent transcription initiation by RNA polymerase I. Elife 6:e27414

    Google Scholar 

  • Han Y, Yan C, Fishbain S, Ivanov I, He Y (2018) Structural visualization of RNA polymerase III transcription machineries. Cell Discov 4:40

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • He Y, Fang J, Taatjes DJ, Nogales E (2013) Structural visualization of key steps in human transcription initiation. Nature 495:481–486

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • He Y, Yan C, Fang J, Inouye C, Tjian R, Ivanov I, Nogales E (2016) Near-atomic resolution visualization of human transcription promoter opening. Nature 533:359–365

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Henry RW, Sadowski CL, Kobayashi R, Hernandez N (1995) A TBP-TAF complex required for transcription of human snRNA genes by RNA polymerase II and III. Nature 374:653–656

    Article  CAS  PubMed  Google Scholar 

  • Herrera-Moyano E, Moriel-Carretero M, Montelone BA, Aguilera A (2014) The rem mutations in the ATP-binding groove of the Rad3/XPD helicase lead to Xeroderma pigmentosum-Cockayne syndrome-like phenotypes. PLoS Genet 10:e1004859

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hoffmann A, Chiang CM, Oelgeschläger T, Xie X, Burley SK, Nakatani Y, Roeder RG (1996) A histone octamer-like structure within TFIID. Nature 380:356–359

    Article  CAS  PubMed  Google Scholar 

  • Hoffmann NA et al (2015) Molecular structures of unbound and transcribing RNA polymerase III. Nature 528:231–236

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hontz RD, French SL, Oakes ML, Tongaonkar P, Nomura M, Beyer AL, Smith JS (2008) Transcription of multiple yeast ribosomal DNA genes requires targeting of UAF to the promoter by Uaf30. Mol Cell Biol 28:6709–6719

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Horikoshi M, Carey MF, Kakidani H, Roeder RG (1988) Mechanism of action of a yeast activator: direct effect of GAL4 derivatives on mammalian TFIID-promoter interactions. Cell 54:665–669

    Article  CAS  PubMed  Google Scholar 

  • Iben JR, Mazeika JK, Hasson S, Rijal K, Arimbasseri AG, Russo AN, Maraia RJ (2011) Point mutations in the Rpb9-homologous domain of Rpc11 that impair transcription termination by RNA polymerase III. Nucleic Acids Res 39:6100–6113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Imasaki T et al (2011) Architecture of the Mediator head module. Nature 475:240–243

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ishiguro A, Kassavetis GA, Geiduschek EP (2002) Essential roles of Bdp1, a subunit of RNA polymerase III initiation factor TFIIIB, in transcription and tRNA processing. Mol Cell Biol 22:3264–3275

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Izban MG, Luse DS (1992) The RNA polymerase II ternary complex cleaves the nascent transcript in a 3′–5′ direction in the presence of elongation factor SII. Genes Dev 6:1342–1356

    Article  CAS  PubMed  Google Scholar 

  • Jacobson RH, Ladurner AG, King DS, Tjian R (2000) Structure and function of a human TAFII250 double bromodomain module. Science 288:1422–1425

    Article  CAS  PubMed  Google Scholar 

  • Jawhari A et al (2002) p52 Mediates XPB function within the transcription/repair factor TFIIH. J Biol Chem 277:31761–31767

    Article  CAS  PubMed  Google Scholar 

  • Jeronimo C, Langelier M-F, Bataille AR, Pascal JM, Pugh BF, Robert F (2016) Tail and kinase modules differently regulate core mediator recruitment and function in vivo. Mol Cell 64:455–466

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang Y, Gralla JD (1993) Uncoupling of initiation and reinitiation rates during HeLa RNA polymerase II transcription in vitro. Mol Cell Biol 13:4572–4577

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Johnson SAS, Dubeau L, Johnson DL (2008) Enhanced RNA polymerase III-dependent transcription is required for oncogenic transformation. J Biol Chem 283:19184–19191

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Joo YJ, Ficarro SB, Soares LM, Chun Y, Marto JA, Buratowski S (2017) Downstream promoter interactions of TFIID TAFs facilitate transcription reinitiation. Genes Dev 31:2162–2174

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Juo ZS, Kassavetis GA, Wang J, Geiduschek EP, Sigler PB (2003) Crystal structure of a transcription factor IIIB core interface ternary complex. Nature 422:534–539

    Article  CAS  PubMed  Google Scholar 

  • Juven-Gershon T, Kadonaga JT (2010) Regulation of gene expression via the core promoter and the basal transcriptional machinery. Dev Biol 339:225–229

    Article  CAS  PubMed  Google Scholar 

  • Juven-Gershon T, Cheng S, Kadonaga JT (2006) Rational design of a super core promoter that enhances gene expression. Nat Meth 3:917–922

    Article  CAS  Google Scholar 

  • Kainov DE, Vitorino M, Cavarelli J, Poterszman A, Egly J-M (2008) Structural basis for group A trichothiodystrophy. Nat Struct Mol Biol 15:980–984

    Article  CAS  PubMed  Google Scholar 

  • Kaplan CD (2013) Basic mechanisms of RNA polymerase II activity and alteration of gene expression in Saccharomyces cerevisiae. Biochim Biophys Acta 1829:39–54

    Article  CAS  PubMed  Google Scholar 

  • Kassavetis GA, Braun BR, Nguyen LH, Geiduschek EP (1990) S. cerevisiae TFIIIB is the transcription initiation factor proper of RNA polymerase III, while TFIIIA and TFIIIC are assembly factors. Cell 60:235–245

    Article  CAS  PubMed  Google Scholar 

  • Kassavetis GA, Nguyen ST, Kobayashi R, Kumar A, Geiduschek EP, Pisano M (1995) Cloning, expression, and function of TFC5, the gene encoding the B″ component of the Saccharomyces cerevisiae RNA polymerase III transcription factor TFIIIB. Proc Natl Acad Sci USA 92:9786–9790

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kassavetis GA, Letts GA, Geiduschek EP (1999) A minimal RNA polymerase III transcription system. EMBO J 18:5042–5051

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kassavetis GA, Letts GA, Geiduschek EP (2001) The RNA polymerase III transcription initiation factor TFIIIB participates in two steps of promoter opening. EMBO J 20:2823–2834

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kassavetis GA, Soragni E, Driscoll R, Geiduschek EP (2005) Reconfiguring the connectivity of a multiprotein complex: fusions of yeast TATA-binding protein with Brf1, and the function of transcription factor IIIB. Proc Natl Acad Sci USA 102:15406–15411

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kassavetis GA, Prakash P, Shim E (2010) The C53/C37 subcomplex of RNA polymerase III lies near the active site and participates in promoter opening. J Biol Chem 285:2695–2706

    Article  CAS  PubMed  Google Scholar 

  • Keener J, Josaitis CA, Dodd JA, Nomura M (1998) Reconstitution of yeast RNA polymerase I transcription in vitro from purified components. TATA-binding protein is not required for basal transcription. J Biol Chem 273:33795–33802

    Article  CAS  PubMed  Google Scholar 

  • Kettenberger H, Armache K-J, Cramer P (2003) Architecture of the RNA polymerase II-TFIIS complex and implications for mRNA cleavage. Cell 114:347–357

    Article  CAS  PubMed  Google Scholar 

  • Keys DA, Vu L, Steffan JS, Dodd JA, Yamamoto RT, Nogi Y, Nomura M (1994) RRN6 and RRN7 encode subunits of a multiprotein complex essential for the initiation of rDNA transcription by RNA polymerase I in Saccharomyces cerevisiae. Genes Dev 8:2349–2362

    Article  CAS  PubMed  Google Scholar 

  • Keys DA et al (1996) Multiprotein transcription factor UAF interacts with the upstream element of the yeast RNA polymerase I promoter and forms a stable preinitiation complex. Genes Dev 10:887–903

    Article  CAS  PubMed  Google Scholar 

  • Khatter H, Vorländer MK, Müller CW (2017) RNA polymerase I and III: similar yet unique. Cur Opin Struct Biol 47:88–94

    Article  CAS  Google Scholar 

  • Khoo B, Brophy B, Jackson SP (1994) Conserved functional domains of the RNA polymerase III general transcription factor BRF. Genes Dev 8:2879–2890

    Article  CAS  PubMed  Google Scholar 

  • Khoo S-K, Wu C-C, Lin Y-C, Lee J-C, Chen H-T (2014) Mapping the protein interaction network for TFIIB-related factor Brf1 in the RNA polymerase III preinitiation complex. Mol Cell Biol 34:551–559

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khoo S-K, Wu C-C, Lin Y-C, Chen H-T (2018) The TFIIE-related Rpc82 subunit of RNA polymerase III interacts with the TFIIB-related transcription factor Brf1 and the polymerase cleft for transcription initiation. Nucleic Acids Res 46:1157–1166

    Article  CAS  PubMed  Google Scholar 

  • Killeen MT, Greenblatt JF (1992) The general transcription factor RAP30 binds to RNA polymerase II and prevents it from binding nonspecifically to DNA. Mol Cell Biol 12:30–37

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim YJ, Björklund S, Li Y, Sayre MH, Kornberg RD (1994) A multiprotein mediator of transcriptional activation and its interaction with the C-terminal repeat domain of RNA polymerase II. Cell 77:599–608

    Article  CAS  PubMed  Google Scholar 

  • Kim KK, Chamberlin HM, Morgan DO, Kim SH (1996) Three-dimensional structure of human cyclin H, a positive regulator of the CDK-activating kinase. Nat Struct Biol 3:849–855

    Article  CAS  PubMed  Google Scholar 

  • Kim TK, Ebright RH, Reinberg D (2000) Mechanism of ATP-dependent promoter melting by transcription factor IIH. Science 288:1418–1422

    Article  CAS  PubMed  Google Scholar 

  • Kim JS, Saint-André C, Lim HS, Hwang C-S, Egly J-M, Cho Y (2015) Crystal structure of the Rad3/XPD regulatory domain of Ssl1/p44. J Biol Chem 290:8321–8330

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Knuesel MT, Meyer KD, Bernecky C, Taatjes DJ (2009) The human CDK8 subcomplex is a molecular switch that controls Mediator coactivator function. Genes Dev 23:439–451

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Knutson BA, Hahn S (2011) Yeast Rrn7 and human TAF1B are TFIIB-related RNA polymerase I general transcription factors. Science 333:1637–1640

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koch SC, Simon N, Ebert C, Carell T (2016) Molecular mechanisms of xeroderma pigmentosum (XP) proteins. Q Rev Biophys 49:e5

    Article  PubMed  Google Scholar 

  • Kokubo T, Gong DW, Yamashita S, Horikoshi M, Roeder RG, Nakatani Y (1993) Drosophila 230-kD TFIID subunit, a functional homolog of the human cell cycle gene product, negatively regulates DNA binding of the TATA box-binding subunit of TFIID. Genes Dev 7:1033–1046

    Article  CAS  PubMed  Google Scholar 

  • Kokubo T, Yamashita S, Horikoshi M, Roeder RG, Nakatani Y (1994) Interaction between the N-terminal domain of the 230-kDa subunit and the TATA box-binding subunit of TFIID negatively regulates TATA-box binding. Proc Natl Acad Sci USA 91:3520–3524

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kolesnikova O, Ben-Shem A, Luo J, Ranish J, Schultz P, Papai G (2018) Molecular structure of promoter-bound yeast TFIID. Nat Commun 9:4666

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Korkhin Y et al (2009) Evolution of complex RNA polymerases: the complete archaeal RNA polymerase structure. PLoS Biol 7:e1000102–1000110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kostrewa D, Zeller ME, Armache K-J, Seizl M, Leike K, Thomm M, Cramer P (2009) RNA polymerase II-TFIIB structure and mechanism of transcription initiation. Nature 462:323–330

    Article  CAS  PubMed  Google Scholar 

  • Kuper J et al (2014) In TFIIH, XPD helicase is exclusively devoted to DNA repair. PLoS Biol 12:e1001954

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kutach AK, Kadonaga JT (2000) The downstream promoter element DPE appears to be as widely used as the TATA box in Drosophila core promoters. Mol Cell Biol 20:4754–4764

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lagrange T, Kapanidis AN, Tang H, Reinberg D, Ebright RH (1998) New core promoter element in RNA polymerase II-dependent transcription: sequence-specific DNA binding by transcription factor IIB. Genes Dev 12:34–44

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lalo D, Steffan JS, Dodd JA, Nomura M (1996) RRN11 encodes the third subunit of the complex containing Rrn6p and Rrn7p that is essential for the initiation of rDNA transcription by yeast RNA polymerase I. J Biol Chem 271:21062–21067

    Article  CAS  PubMed  Google Scholar 

  • Landrieux E, Alic N, Ducrot C, Acker J, Riva M, Carles C (2006) A subcomplex of RNA polymerase III subunits involved in transcription termination and reinitiation. EMBO J 25:118–128

    Article  CAS  PubMed  Google Scholar 

  • Lariviere L, Plaschka C, Seizl M, Wenzeck L, Kurth F, Cramer P (2012a) Structure of the Mediator head module. Nature 492:448–451

    Article  CAS  PubMed  Google Scholar 

  • Lariviere L, Seizl M, Cramer P (2012b) A structural perspective on Mediator function. Curr Opin Cell Biol 24:305–313

    Article  CAS  PubMed  Google Scholar 

  • Lariviere L, Plaschka C, Seizl M, Petrotchenko EV, Wenzeck L, Borchers CH, Cramer P (2013) Model of the Mediator middle module based on protein cross-linking. Nucleic Acids Res 41:9266–9273

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Learned RM, Cordes S, Tjian R (1985) Purification and characterization of a transcription factor that confers promoter specificity to human RNA polymerase I. Mol Cell Biol 5:1358–1369

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee YC, Park JM, Min S, Han SJ, Kim YJ (1999) An activator binding module of yeast RNA polymerase II holoenzyme. Mol Cell Biol 19:2967–2976

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee D-H, Gershenzon N, Gupta M, Ioshikhes IP, Reinberg D, Lewis BA (2005) Functional characterization of core promoter elements: the downstream core element is recognized by TAF1. Mol Cell Biol 25:9674–9686

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lenhard B, Sandelin A, Carninci P (2012) Metazoan promoters: emerging characteristics and insights into transcriptional regulation. Nat Rev Genet 13:233–245

    Article  CAS  PubMed  Google Scholar 

  • Leurent C et al (2002) Mapping histone fold TAFs within yeast TFIID. EMBO J 21:3424–3433

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li C-L, Golebiowski FM, Onishi Y, Samara NL, Sugasawa K, Yang W (2015) Tripartite DNA lesion recognition and verification by XPC, TFIIH, and XPA in nucleotide excision repair. Mol Cell 59:1025–1034

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lim CY, Santoso B, Boulay T, Dong E, Ohler U, Kadonaga JT (2004) The MTE, a new core promoter element for transcription by RNA polymerase II. Genes Dev 18:1606–1617

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lin CW, Moorefield B, Payne J, Aprikian P, Mitomo K, Reeder RH (1996) A novel 66-kilodalton protein complexes with Rrn6, Rrn7, and TATA-binding protein to promote polymerase I transcription initiation in Saccharomyces cerevisiae. Mol Cell Biol 16:6436–6443

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu H et al (2008) Structure of the DNA repair helicase XPD. Cell 133:801–812

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu X, Bushnell DA, Wang D, Calero G, Kornberg RD (2010) Structure of an RNA polymerase II-TFIIB complex and the transcription initiation mechanism. Science 327:206–209

    Article  CAS  PubMed  Google Scholar 

  • Lobo SM, Tanaka M, Sullivan ML, Hernandez N (1992) A TBP complex essential for transcription from TATA-less but not TATA-containing RNA polymerase III promoters is part of the TFIIIB fraction. Cell 71:1029–1040

    Article  CAS  PubMed  Google Scholar 

  • Lockwood WW et al (2010) Integrative genomic analyses identify BRF2 as a novel lineage-specific oncogene in lung squamous cell carcinoma. PLoS Med 7:e1000315

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lolli G, Lowe ED, Brown NR, Johnson LN (2004) The crystal structure of human CDK7 and its protein recognition properties. Structure 12:2067–2079

    Article  CAS  PubMed  Google Scholar 

  • López-De-León A, Librizzi M, Puglia K, Willis IM (1992) PCF4 encodes an RNA polymerase III transcription factor with homology to TFIIB. Cell 71:211–220

    Article  PubMed  Google Scholar 

  • Louder RK, He Y, López-Blanco JR, Fang J, Chacón P, Nogales E (2016) Structure of promoter-bound TFIID and model of human pre-initiation complex assembly. Nature 531:604–609

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Luo J et al (2015) Architecture of the human and yeast general transcription and DNA repair factor TFIIH. Mol Cell 59:794–806

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Male G et al (2015) Architecture of TFIIIC and its role in RNA polymerase III pre-initiation complex assembly. Nat Commun 6:7387

    Article  CAS  PubMed  Google Scholar 

  • Marteijn JA, Lans H, Vermeulen W, Hoeijmakers JHJ (2014) Understanding nucleotide excision repair and its roles in cancer and ageing. Nat Rev Mol Cell Biol 15:465–481

    Article  CAS  PubMed  Google Scholar 

  • Mathieu N, Kaczmarek N, Rüthemann P, Luch A, Naegeli H (2013) DNA quality control by a lesion sensor pocket of the xeroderma pigmentosum group D helicase subunit of TFIIH. Curr Biol 23:204–212

    Article  CAS  PubMed  Google Scholar 

  • Maxon ME, Goodrich JA, Tjian R (1994) Transcription factor IIE binds preferentially to RNA polymerase IIa and recruits TFIIH: a model for promoter clearance. Genes Dev 8:515–524

    Article  CAS  PubMed  Google Scholar 

  • Milkereit P, Tschochner H (1998) A specialized form of RNA polymerase I, essential for initiation and growth-dependent regulation of rRNA synthesis, is disrupted during transcription. EMBO J 17:3692–3703

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Milkereit P, Schultz P, Tschochner H (1997) Resolution of RNA polymerase I into dimers and monomers and their function in transcription. Biol Chem 378:1433–1443

    Article  CAS  PubMed  Google Scholar 

  • Mital R, Kobayashi R, Hernandez N (1996) RNA polymerase III transcription from the human U6 and adenovirus type 2 VAI promoters has different requirements for human BRF, a subunit of human TFIIIB. Mol Cell Biol 16:7031–7042

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Monté D et al (2018) Crystal structure of human Mediator subunit MED23. Nat Commun 9:3389

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moriel-Carretero M, Herrera-Moyano E, Aguilera A (2015) A unified model for the molecular basis of Xeroderma pigmentosum-Cockayne Syndrome. Rare Dis 3:e1079362

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Murakami K et al (2013) Architecture of an RNA polymerase II transcription pre-initiation complex. Science 342:1238724

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Murakami K, Tsai K-L, Kalisman N, Bushnell DA, Asturias FJ, Kornberg RD (2015) Structure of an RNA polymerase II preinitiation complex. Proc Natl Acad Sci USA 112:13543–13548

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Naegeli H, Bardwell L, Friedberg EC (1993) Inhibition of Rad3 DNA helicase activity by DNA adducts and abasic sites: implications for the role of a DNA helicase in damage-specific incision of DNA. Biochemistry 32:613–621

    Article  CAS  PubMed  Google Scholar 

  • Naidu S, Friedrich JK, Russell J, Zomerdijk JCBM (2011) TAF1B is a TFIIB-like component of the basal transcription machinery for RNA polymerase I. Science 333:1640–1642

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Natarajan K, Jackson BM, Zhou H, Winston F, Hinnebusch AG (1999) Transcriptional activation by Gcn4p involves independent interactions with the SWI/SNF complex and the SRB/mediator. Mol Cell 4:657–664

    Article  CAS  PubMed  Google Scholar 

  • Neyer S et al (2016) Structure of RNA polymerase I transcribing ribosomal DNA genes. Nature 540:607–610

    Article  CAS  PubMed  Google Scholar 

  • Nikolov DB et al (1992) Crystal structure of TFIID TATA-box binding protein. Nature 360:40–46

    Article  CAS  PubMed  Google Scholar 

  • Nikolov DB et al (1995) Crystal structure of a TFIIB-TBP-TATA-element ternary complex. Nature 377:119–128

    Article  CAS  PubMed  Google Scholar 

  • Nikolov DB, Chen H, Halay ED, Hoffman A, Roeder RG, Burley SK (1996) Crystal structure of a human TATA box-binding protein/TATA element complex. Proc Natl Acad Sci USA 93:4862–4867

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nogales E, Fang J, Louder RK (2017a) Structural dynamics and DNA interaction of human TFIID. Transcription 8:55–60

    Article  CAS  PubMed  Google Scholar 

  • Nogales E, Louder RK, He Y (2017b) Structural insights into the eukaryotic transcription initiation machinery. Annu Rev Biophys 46:59–83

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nogales E, Patel AB, Louder RK (2017c) Towards a mechanistic understanding of core promoter recognition from cryo-EM studies of human TFIID. Curr Opin Struct Biol 47:60–66

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nozawa K, Schneider TR, Cramer P (2017) Core Mediator structure at 3.4 Å extends model of transcription initiation complex. Nature 545:248–251

    Article  CAS  PubMed  Google Scholar 

  • Ohkuma Y, Roeder RG (1994) Regulation of TFIIH ATPase and kinase activities by TFIIE during active initiation complex formation. Nature 368:160–163

    Google Scholar 

  • Okuda M, Tanaka A, Satoh M, Mizuta S, Takazawa M, Ohkuma Y, Nishimura Y (2008) Structural insight into the TFIIE-TFIIH interaction: TFIIE and p53 share the binding region on TFIIH. EMBO J 27:1161–1171

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Papai G, Tripathi MK, Ruhlmann C, Werten S, Crucifix C, Weil PA, Schultz P (2009) Mapping the initiator binding Taf2 subunit in the structure of hydrated yeast TFIID. Structure 17:363–373

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Patel AB et al (2018) Structure of human TFIID and mechanism of TBP loading onto promoter DNA. Science 362(6421):eaau8872

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE (2004) UCSF Chimera–a visualization system for exploratory research and analysis. J Comput Chem 25:1605–1612

    Article  CAS  PubMed  Google Scholar 

  • Pilsl M et al (2016) Structure of the initiation-competent RNA polymerase I and its implication for transcription. Nat Commun 7:12126

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Plaschka C et al (2015) Architecture of the RNA polymerase II-Mediator core initiation complex. Nature 518:376–380

    Article  CAS  PubMed  Google Scholar 

  • Plaschka C, Hantsche M, Dienemann C, Burzinski C, Plitzko J, Cramer P (2016) Transcription initiation complex structures elucidate DNA opening. Nature 533:353–358

    Article  CAS  PubMed  Google Scholar 

  • Pugh BF, Tjian R (1990) Mechanism of transcriptional activation by Sp1: evidence for coactivators. Cell 61:1187–1197

    Article  CAS  PubMed  Google Scholar 

  • Pugh BF, Tjian R (1991) Transcription from a TATA-less promoter requires a multisubunit TFIID complex. Genes Dev 5:1935–1945

    Article  CAS  PubMed  Google Scholar 

  • Rani PG, Ranish JA, Hahn S (2004) RNA polymerase II (Pol II)-TFIIF and Pol II-mediator complexes: the major stable Pol II complexes and their activity in transcription initiation and reinitiation. Mol Cell Biol 24:1709–1720

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rapin I (2013) Disorders of nucleotide excision repair. Handb Clin Neurol 113:1637–1650

    Article  PubMed  Google Scholar 

  • Reines D (1992) Elongation factor-dependent transcript shortening by template-engaged RNA polymerase II. J Biol Chem 267:3795–3800

    CAS  PubMed  Google Scholar 

  • Rijal K, Maraia RJ (2013) RNA polymerase III mutants in TFIIFα-like C37 that cause terminator readthrough with no decrease in transcription output. Nucleic Acids Res 41:139–155

    Article  CAS  PubMed  Google Scholar 

  • Roberts S, Colbert T, Hahn S (1995) TFIIIC determines RNA polymerase III specificity at the TATA-containing yeast U6 promoter. Genes Dev 9:832–842

    Article  CAS  PubMed  Google Scholar 

  • Robinson PJJ, Bushnell DA, Trnka MJ, Burlingame AL, Kornberg RD (2012) Structure of the mediator head module bound to the carboxy-terminal domain of RNA polymerase II. Proc Natl Acad Sci USA 109:17931–17935

    Article  PubMed  PubMed Central  Google Scholar 

  • Robinson PJ et al (2015) Molecular architecture of the yeast Mediator complex. Elife 4:e08719

    Article  PubMed  PubMed Central  Google Scholar 

  • Robinson PJ, Trnka MJ, Bushnell DA, Davis RE, Mattei P-J, Burlingame AL, Kornberg RD (2016) Structure of a complete mediator-RNA polymerase II pre-initiation complex. Cell 166:1411–1422.e1416

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roeder RG (1996) The role of general initiation factors in transcription by RNA polymerase II. Trends Biochem Sci 21:327–335

    Article  CAS  PubMed  Google Scholar 

  • Roeder RG, Rutter WJ (1969) Multiple forms of DNA-dependent RNA polymerase in eukaryotic organisms. Nature 224:234–237

    Article  CAS  PubMed  Google Scholar 

  • Roeder RG, Rutter WJ (1970) Specific nucleolar and nucleoplasmic RNA polymerases. Proc Natl Acad Sci USA 65:675–682

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rossignol M, Kolb-Cheynel I, Egly JM (1997) Substrate specificity of the cdk-activating kinase (CAK) is altered upon association with TFIIH. EMBO J 16:1628–1637

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roy AL, Singer DS (2015) Core promoters in transcription: old problem, new insights. Trends Biochem Sci 40:165–171

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roy K, Gabunilas J, Gillespie A, Ngo D, Chanfreau GF (2016) Common genomic elements promote transcriptional and DNA replication roadblocks. Genome Res 26:1363–1375

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ruan W, Lehmann E, Thomm M, Kostrewa D, Cramer P (2011) Evolution of two modes of intrinsic RNA polymerase transcript cleavage. J Biol Chem 286:18701–18707

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ruppert S, Tjian R (1995) Human TAFII250 interacts with RAP74: implications for RNA polymerase II initiation. Genes Dev 9:2747–2755

    Article  CAS  PubMed  Google Scholar 

  • Sadian Y et al (2017) Structural insights into transcription initiation by yeast RNA polymerase I. EMBO J 36(18):2698–2709

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sadowski CL, Henry RW, Lobo SM, Hernandez N (1993) Targeting TBP to a non-TATA box cis-regulatory element: a TBP-containing complex activates transcription from snRNA promoters through the PSE. Genes Dev 7:1535–1548

    Article  CAS  PubMed  Google Scholar 

  • Sainsbury S, Niesser J, Cramer P (2013) Structure and function of the initially transcribing RNA polymerase II-TFIIB complex. Nature 493:437–440

    Article  CAS  PubMed  Google Scholar 

  • Sainsbury S, Bernecky C, Cramer P (2015) Structural basis of transcription initiation by RNA polymerase II. Nat Rev Mol Cell Biol 16:129–143

    Article  CAS  PubMed  Google Scholar 

  • Sandelin A, Carninci P, Lenhard B, Ponjavic J, Hayashizaki Y, Hume DA (2007) Mammalian RNA polymerase II core promoters: insights from genome-wide studies. Nat Rev Genet 8:424–436

    Article  CAS  PubMed  Google Scholar 

  • Sanders SL, Garbett KA, Weil PA (2002) Molecular characterization of Saccharomyces cerevisiae TFIID. Mol Cell Biol 22:6000–6013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sandrock B, Egly JM (2001) A yeast four-hybrid system identifies Cdk-activating kinase as a regulator of the XPD helicase, a subunit of transcription factor IIH. J Biol Chem 276:35328–35333

    Article  CAS  PubMed  Google Scholar 

  • Schilbach S, Hantsche M, Tegunov D, Dienemann C, Wigge C, Urlaub H, Cramer P (2017) Structures of transcription pre-initiation complex with TFIIH and Mediator. Nature 551:204–209

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schneider DA (2012) RNA polymerase I activity is regulated at multiple steps in the transcription cycle: recent insights into factors that influence transcription elongation. Gene 493:176–184

    Article  CAS  PubMed  Google Scholar 

  • Schneider EV, Böttcher J, Blaesse M, Neumann L, Huber R, Maskos K (2011) The structure of CDK8/CycC implicates specificity in the CDK/cyclin family and reveals interaction with a deep pocket binder. J Mol Biol 412:251–266

    Article  CAS  PubMed  Google Scholar 

  • Schramm L, Hernandez N (2002) Recruitment of RNA polymerase III to its target promoters. Genes Dev 16:2593–2620

    Article  CAS  PubMed  Google Scholar 

  • Schramm L, Pendergrast PS, Sun Y, Hernandez N (2000) Different human TFIIIB activities direct RNA polymerase III transcription from TATA-containing and TATA-less promoters. Genes Dev 14:2650–2663

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schultz P, Fribourg S, Poterszman A, Mallouh V, Moras D, Egly JM (2000) Molecular structure of human TFIIH. Cell 102:599–607

    Article  CAS  PubMed  Google Scholar 

  • Shah SM, Kumar A, Geiduschek EP, Kassavetis GA (1999) Alignment of the B″ subunit of RNA polymerase III transcription factor IIIB in its promoter complex. J Biol Chem 274:28736–28744

    Article  CAS  PubMed  Google Scholar 

  • Shiekhattar R et al (1995) Cdk-activating kinase complex is a component of human transcription factor TFIIH. Nature 374:283–287

    Article  CAS  PubMed  Google Scholar 

  • Sklar VE, Schwartz LB, Roeder RG (1975) Distinct molecular structures of nuclear class I, II, and III DNA-dependent RNA polymerases. Proc Natl Acad Sci USA 72:348–352

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith DJ, Whitehouse I (2012) Intrinsic coupling of lagging-strand synthesis to chromatin assembly. Nature 483:434–438

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Soutourina J (2018) Transcription regulation by the Mediator complex. Nat Rev Mol Cell Biol 19:262–274

    Article  CAS  PubMed  Google Scholar 

  • Steffan JS, Keys DA, Vu L, Nomura M (1998) Interaction of TATA-binding protein with upstream activation factor is required for activated transcription of ribosomal DNA by RNA polymerase I in Saccharomyces cerevisiae in vivo. Mol Cell Biol 18:3752–3761

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stillman DJ, Geiduschek EP (1984) Differential binding of a S. cerevisiae RNA polymerase III transcription factor to two promoter segments of a tRNA gene. EMBO J 3:847–853

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stringer KF, Ingles CJ, Greenblatt J (1990) Direct and selective binding of an acidic transcriptional activation domain to the TATA-box factor TFIID. Nature 345:783–786

    Article  CAS  PubMed  Google Scholar 

  • Sugasawa K, Akagi J-i, Nishi R, Iwai S, Hanaoka F (2009) Two-step recognition of DNA damage for mammalian nucleotide excision repair: Directional binding of the XPC complex and DNA strand scanning. Mol Cell 36:642–653

    Article  CAS  PubMed  Google Scholar 

  • Sung P, Bailly V, Weber C, Thompson LH, Prakash L, Prakash S (1993) Human xeroderma pigmentosum group D gene encodes a DNA helicase. Nature 365:852–855

    Article  CAS  PubMed  Google Scholar 

  • Svejstrup JQ et al (1995) Different forms of TFIIH for transcription and DNA repair: holo-TFIIH and a nucleotide excision repairosome. Cell 80:21–28

    Article  CAS  PubMed  Google Scholar 

  • Svetlov V, Nudler E (2013) Basic mechanism of transcription by RNA polymerase II. Biochim Biophys Acta 1829:20–28

    Article  CAS  PubMed  Google Scholar 

  • Tafur L et al (2016) Molecular structures of transcribing RNA polymerase I. Mol Cell 64:1135–1143

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tan S, Hunziker Y, Sargent DF, Richmond TJ (1996) Crystal structure of a yeast TFIIA/TBP/DNA complex. Nature 381:127–151

    Article  CAS  PubMed  Google Scholar 

  • Teichmann M, Wang Z, Roeder RG (2000) A stable complex of a novel transcription factor IIB-related factor, human TFIIIB50, and associated proteins mediate selective transcription by RNA polymerase III of genes with upstream promoter elements. Proc Natl Acad Sci USA 97:14200–14205

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Theron T et al (2005) Transcription-associated breaks in xeroderma pigmentosum group D cells from patients with combined features of xeroderma pigmentosum and Cockayne syndrome. Mol Cell Biol 25:8368–8378

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Torreira E et al (2017) The dynamic assembly of distinct RNA polymerase I complexes modulates rDNA transcription. Elife 6:e20832

    Article  PubMed  PubMed Central  Google Scholar 

  • Tsai K-L et al (2017) Mediator structure and rearrangements required for holoenzyme formation. Nature 544:196–201

    Google Scholar 

  • Tsai FT, Sigler PB (2000) Structural basis of preinitiation complex assembly on human pol II promoters. EMBO J 19:25–36

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsai K-L, Sato S, Tomomori-Sato C, Conaway RC, Conaway JW, Asturias FJ (2013) A conserved Mediator-CDK8 kinase module association regulates Mediator-RNA polymerase II interaction. Nat Struct Mol Biol 20:611–619

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsai K-L, Tomomori-Sato C, Sato S, Conaway RC, Conaway JW, Asturias FJ (2014) Subunit architecture and functional modular rearrangements of the transcriptional mediator complex. Cell 157:1430–1444

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vannini A, Cramer P (2012) Conservation between the RNA polymerase I, II, and III transcription initiation machineries. Mol Cell 45:439–446

    Article  CAS  PubMed  Google Scholar 

  • Vassylyev DG, Vassylyeva MN, Perederina A, Tahirov TH, Artsimovitch I (2007) Structural basis for transcription elongation by bacterial RNA polymerase. Nature 448:157–162

    Article  CAS  PubMed  Google Scholar 

  • Verger A, Monté D, Villeret V (2019) Twenty years of Mediator complex structural studies. Biochem Soc Trans 47:399–410

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vermeulen M et al (2007) Selective anchoring of TFIID to nucleosomes by trimethylation of histone H3 lysine 4. Cell 131:58–69

    Article  CAS  PubMed  Google Scholar 

  • Verrijzer CP, Chen JL, Yokomori K, Tjian R (1995) Binding of TAFs to core elements directs promoter selectivity by RNA polymerase II. Cell 81:1115–1125

    Article  CAS  PubMed  Google Scholar 

  • Vojnic E et al (2011) Structure and VP16 binding of the Mediator Med25 activator interaction domain. Nat Struct Mol Biol 18:404–409

    Article  CAS  PubMed  Google Scholar 

  • Vorländer MK, Khatter H, Wetzel R, Hagen WJH, Müller CW (2018) Molecular mechanism of promoter opening by RNA polymerase III. Nature 553:295–300

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang D, Hawley DK (1993) Identification of a 3′–5′ exonuclease activity associated with human RNA polymerase II. Proc Natl Acad Sci USA 90:843–847

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Z, Roeder RG (1995) Structure and function of a human transcription factor TFIIIB subunit that is evolutionarily conserved and contains both TFIIB- and high-mobility-group protein 2-related domains. Proc Natl Acad Sci USA 92:7026–7030

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang D, Bushnell DA, Westover KD, Kaplan CD, Kornberg RD (2006) Structural basis of transcription: role of the trigger loop in substrate specificity and catalysis. Cell 127:941–954

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Warner JR (1999) The economics of ribosome biosynthesis in yeast. Trends Biochem Sci 24:437–440

    Article  CAS  PubMed  Google Scholar 

  • Weeda G, van Ham RC, Vermeulen W, Bootsma D, van der Eb AJ, Hoeijmakers JH (1990) A presumed DNA helicase encoded by ERCC-3 is involved in the human repair disorders xeroderma pigmentosum and Cockayne’s syndrome. Cell 62:777–791

    Article  CAS  PubMed  Google Scholar 

  • Weinmann R, Roeder RG (1974) Role of DNA-dependent RNA polymerase 3 in the transcription of the tRNA and 5S RNA genes. Proc Natl Acad Sci USA 71:1790–1794

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Westover KD, Bushnell DA, Kornberg RD (2004) Structural basis of transcription: nucleotide selection by rotation in the RNA polymerase II active center. Cell 119:481–489

    Article  CAS  PubMed  Google Scholar 

  • Wolski SC, Kuper J, Hänzelmann P, Truglio JJ, Croteau DL, Van Houten B, Kisker C (2008) Crystal structure of the FeS cluster-containing nucleotide excision repair helicase XPD. PLoS Biol 6:e149

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu SY, Chiang CM (2001) TATA-binding protein-associated factors enhance the recruitment of RNA polymerase II by transcriptional activators. J Biol Chem 276:34235–34243

    Article  CAS  PubMed  Google Scholar 

  • Wu C-C, Lin Y-C, Chen H-T (2011) 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu C-C et al (2012) RNA polymerase III subunit architecture and implications for open promoter complex formation. Proc Natl Acad Sci USA 109:19232–19237

    Article  PubMed  PubMed Central  Google Scholar 

  • Xie X et al (1996) Structural similarity between TAFs and the heterotetrameric core of the histone octamer. Nature 380:316–322

    Article  CAS  PubMed  Google Scholar 

  • Yan Q, Moreland RJ, Conaway JW, Conaway RC (1999) Dual roles for transcription factor IIF in promoter escape by RNA polymerase II. J Biol Chem 274:35668–35675

    Article  CAS  PubMed  Google Scholar 

  • Yudkovsky N, Ranish JA, Hahn S (2000) A transcription reinitiation intermediate that is stabilized by activator. Nature 408:225–229

    Article  CAS  PubMed  Google Scholar 

  • Zhang G, Campbell EA, Minakhin L, Richter C, Severinov K, Darst SA (1999) Crystal structure of Thermus aquaticus core RNA polymerase at 3.3 A resolution. Cell 98:811–824

    Article  CAS  PubMed  Google Scholar 

  • Zhang Z et al (2015) Chemical perturbation of an intrinsically disordered region of TFIID distinguishes two modes of transcription initiation. Elife 4:e07777

    Article  PubMed Central  Google Scholar 

Download references

Acknowledgements

Molecular depictions were created using UCSF Chimera (Pettersen et al. 2004) and PyMol (The PyMOL Molecular Graphics System, Version 1.8, Schrödinger, LLC.). This work was funded through NIGMS grant R35-GM127018 to E. N; B. J. G. was supported by the Swiss National Science Foundation (projects P300PA-160983 and P300PA-174355). E. N. is a Howard Hughes Medical Investigator.

Author information

Authors and Affiliations

  1. California Institute for Quantitative Biosciences (QB3), University of California, Berkeley, CA, 94720, USA

    Basil J. Greber & Eva Nogales

  2. Molecular Biophysics and Integrative Bio-Imaging Division, Lawrence Berkeley National Laboratory, Berkeley, CA, 94720, USA

    Basil J. Greber & Eva Nogales

  3. Howard Hughes Medical Institute, University of California, Berkeley, CA, 94720, USA

    Eva Nogales

  4. Department of Molecular and Cell Biology, University of California, Berkeley, CA, 94720, USA

    Eva Nogales

Authors
  1. Basil J. Greber
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Eva Nogales
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Basil J. Greber .

Editor information

Editors and Affiliations

  1. Institute of Zoology, University of Mainz, Mainz, Germany

    J. Robin Harris

  2. School of Natural and Environmental Sciences, Newcastle University, Newcastle upon Tyne, UK

    Jon Marles-Wright

Rights and permissions

Reprints and permissions

Copyright information

© 2019 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Greber, B.J., Nogales, E. (2019). The Structures of Eukaryotic Transcription Pre-initiation Complexes and Their Functional Implications. In: Harris, J., Marles-Wright, J. (eds) Macromolecular Protein Complexes II: Structure and Function . Subcellular Biochemistry, vol 93. Springer, Cham. https://doi.org/10.1007/978-3-030-28151-9_5

Download citation

Publish with us

Policies and ethics

Search

Navigation