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Annual Review of Cell and Developmental Biology

Volume 36, 2020

Structural Biology of RNA Polymerase II Transcription: 20 Years On

Abstract

Gene transcription by RNA polymerase II (Pol II) is the first step in the expression of the eukaryotic genome and a focal point for cellular regulation during development, differentiation, and responses to the environment. Two decades after the determination of the structure of Pol II, the mechanisms of transcription have been elucidated with studies of Pol II complexes with nucleic acids and associated proteins. Here we provide an overview of the nearly 200 available Pol II complex structures and summarize how these structures have elucidated promoter-dependent transcription initiation, promoter-proximal pausing and release of Pol II into active elongation, and the mechanisms that Pol II uses to navigate obstacles such as nucleosomes and DNA lesions. We predict that future studies will focus on how Pol II transcription is interconnected with chromatin transitions, RNA processing, and DNA repair.

Keyword(s): cryo-electron microscopy, gene transcription, RNA polymerase, structural biology, transcriptional regulation, X-ray crystallography
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2020-10-06
2024-04-18
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Literature Cited

  1. Abascal-Palacios G, Ramsay EP, Beuron F, Morris E, Vannini A 2018. Structural basis of RNA polymerase III transcription initiation. Nature 553:301–6
     [Google Scholar]
  2. Adelman K, Lis JT. 2012. Promoter-proximal pausing of RNA polymerase II: emerging roles in metazoans. Nat. Rev. Genet. 13:720–31
     [Google Scholar]
  3. Alic N, Ayoub N, Landrieux E, Favry E, Baudouin-Cornu P et al. 2007. Selectivity and proofreading both contribute significantly to the fidelity of RNA polymerase III transcription. PNAS 104:10400–5
     [Google Scholar]
  4. Allen BL, Taatjes DJ. 2015. The Mediator complex: a central integrator of transcription. Nat. Rev. Mol. Cell Biol. 16:155–66
     [Google Scholar]
  5. Armache K-J, Kettenberger H, Cramer P 2003. Architecture of initiation-competent 12-subunit RNA polymerase II. PNAS 100:6964–68
     [Google Scholar]
  6. Armache K-J, Mitterweger S, Meinhart A, Cramer P 2005. Structures of complete RNA polymerase II and its subcomplex, Rpb4/7. J. Biol. Chem. 280:7131–34
     [Google Scholar]
  7. Artsimovitch I, Vassylyeva MN, Svetlov D, Svetlov V, Perederina A et al. 2005. Allosteric modulation of the RNA polymerase catalytic reaction is an essential component of transcription control by rifamycins. Cell 122:351–63
     [Google Scholar]
  8. Asturias FJ, Jiang YW, Myers LC, Gustafsson CM, Kornberg RD 1999. Conserved structures of Mediator and RNA polymerase II holoenzyme. Science 283:985–87
     [Google Scholar]
  9. Bar-Nahum G, Epshtein V, Ruckenstein AE, Rafikov R, Mustaev A, Nudler E 2005. A ratchet mechanism of transcription elongation and its control. Cell 120:183–93
     [Google Scholar]
  10. Barnes CO, Calero M, Malik I, Graham BW, Spahr H et al. 2015. Crystal structure of a transcribing RNA polymerase II complex reveals a complete transcription bubble. Mol. Cell 59:258–69
     [Google Scholar]
  11. Bernecky C, Grob P, Ebmeier CC, Nogales E, Taatjes DJ 2011. Molecular architecture of the human Mediator-RNA polymerase II-TFIIF assembly. PLOS Biol 9:e1000603
     [Google Scholar]
  12. Bernecky C, Herzog F, Baumeister W, Plitzko JM, Cramer P 2016. Structure of transcribing mammalian RNA polymerase II. Nature 529:551–54
     [Google Scholar]
  13. Bernecky C, Plitzko JM, Cramer P 2017. Structure of a transcribing RNA polymerase II-DSIF complex reveals a multidentate DNA-RNA clamp. Nat. Struct. Mol. Biol. 24:809–15
     [Google Scholar]
  14. Bieniossek C, Papai G, Schaffitzel C, Garzoni F, Chaillet M et al. 2013. The architecture of human general transcription factor TFIID core complex. Nature 493:699–702
     [Google Scholar]
  15. Blombach F, Matelska D, Fouqueau T, Cackett G, Werner F 2019. Key concepts and challenges in archaeal transcription. J. Mol. Biol. 431:4184–201
     [Google Scholar]
  16. Bondarenko VA, Steele LM, Újvári A, Gaykalova DA, Kulaeva OI et al. 2006. Nucleosomes can form a polar barrier to transcript elongation by RNA polymerase II. Mol. Cell 24:469–79
     [Google Scholar]
  17. Brueckner F, Armache K-J, Cheung A, Damsma GE, Kettenberger H et al. 2009a. Structure–function studies of the RNA polymerase II elongation complex. Acta Crystallogr. Sect. D 65:112–20
     [Google Scholar]
  18. Brueckner F, Cramer P. 2008. Structural basis of transcription inhibition by α-amanitin and implications for RNA polymerase II translocation. Nat. Struct. Mol. Biol. 15:811–18
     [Google Scholar]
  19. Brueckner F, Hennecke U, Carell T, Cramer P 2007. CPD damage recognition by transcribing RNA polymerase II. Science 315:859–62
     [Google Scholar]
  20. Brueckner F, Ortiz J, Cramer P 2009b. A movie of the RNA polymerase nucleotide addition cycle. Curr. Opin. Struct. Biol. 19:294–99
     [Google Scholar]
  21. Buratowski S. 2009. Progression through the RNA polymerase II CTD cycle. Mol. Cell 36:541–46
     [Google Scholar]
  22. Buratowski S, Hahn S, Guarente L, Sharp PA 1989. Five intermediate complexes in transcription initiation by RNA polymerase II. Cell 56:549–61
     [Google Scholar]
  23. Bushnell DA, Cramer P, Kornberg RD 2001. Selenomethionine incorporation in Saccharomyces cerevisiae RNA polymerase II. Structure 9:R11–14
     [Google Scholar]
  24. Bushnell DA, Cramer P, Kornberg RD 2002. Structural basis of transcription: α-amanitin–RNA polymerase II cocrystal at 2.8 Å resolution. PNAS 99:1218–22
     [Google Scholar]
  25. Bushnell DA, Kornberg RD. 2003. Complete, 12-subunit RNA polymerase II at 4.1-Å resolution: implications for the initiation of transcription. PNAS 100:6969–73
     [Google Scholar]
  26. Bushnell DA, Westover KD, Davis RE, Kornberg RD 2004. Structural basis of transcription: an RNA polymerase II-TFIIB cocrystal at 4.5 angstroms. Science 303:983–88
     [Google Scholar]
  27. Čabart P, Újvári A, Pal M, Luse DS 2011. Transcription factor TFIIF is not required for initiation by RNA polymerase II, but it is essential to stabilize transcription factor TFIIB in early elongation complexes. PNAS 108:15786–91
     [Google Scholar]
  28. Cai G, Chaban YL, Imasaki T, Kovacs JA, Calero G et al. 2012. Interaction of the mediator head module with RNA polymerase II. Structure 20:899–910
     [Google Scholar]
  29. Campos EI, Reinberg D. 2009. Histones: annotating chromatin. Annu. Rev. Genet. 43:559–99
     [Google Scholar]
  30. Chakraborty A, Wang D, Ebright YW, Korlann Y, Kortkhonjia E et al. 2012. Opening and closing of the bacterial RNA polymerase clamp. Science 337:591–95
     [Google Scholar]
  31. Chédin S, Riva M, Schultz P, Sentenac A, Carles C 1998. The RNA cleavage activity of RNA polymerase III is mediated by an essential TFIIS-like subunit and is important for transcription termination. Genes Dev 12:3857–71
     [Google Scholar]
  32. Chen H-T, Hahn S. 2003. Binding of TFIIB to RNA polymerase II: mapping the binding site for the TFIIB zinc ribbon domain within the preinitiation complex. Mol. Cell 12:437–47
     [Google Scholar]
  33. Chen H-T, Hahn S. 2004. Mapping the location of TFIIB within the RNA polymerase II transcription preinitiation complex: a model for the structure of the PIC. Cell 119:169–80
     [Google Scholar]
  34. Chen H-T, Warfield L, Hahn S 2007. The positions of TFIIF and TFIIE in the RNA polymerase II transcription preinitiation complex. Nat. Struct. Mol. Biol. 14:696–703
     [Google Scholar]
  35. Chen ZA, Jawhari A, Fischer L, Buchen C, Tahir S et al. 2010. Architecture of the RNA polymerase II–TFIIF complex revealed by cross‐linking and mass spectrometry. EMBO J 29:717–26
     [Google Scholar]
  36. Cheung AC, Cramer P. 2011. Structural basis of RNA polymerase II backtracking, arrest and reactivation. Nature 471:249–53
     [Google Scholar]
  37. Cheung AC, Sainsbury S, Cramer P 2011. Structural basis of initial RNA polymerase II transcription. EMBO J 30:4755–63
     [Google Scholar]
  38. Cho E-J, Kobor MS, Kim M, Greenblatt J, Buratowski S 2001. Opposing effects of Ctk1 kinase and Fcp1 phosphatase at Ser 2 of the RNA polymerase II C-terminal domain. Genes Dev 15:3319–29
     [Google Scholar]
  39. Cho E-J, Takagi T, Moore CR, Buratowski S 1997. mRNA capping enzyme is recruited to the transcription complex by phosphorylation of the RNA polymerase II carboxy-terminal domain. Genes Dev 11:3319–26
     [Google Scholar]
  40. Cianfrocco MA, Kassavetis GA, Grob P, Fang J, Juven-Gershon T et al. 2013. Human TFIID binds to core promoter DNA in a reorganized structural state. Cell 152:120–31
     [Google Scholar]
  41. Compe E, Egly J-M. 2012. TFIIH: when transcription met DNA repair. Nat. Rev. Mol. Cell Biol. 13:343–54
     [Google Scholar]
  42. Conaway RC, Conaway JW. 1993. General initiation factors for RNA polymerase II. Annu. Rev. Biochem. 62:161–90
     [Google Scholar]
  43. Conaway RC, Conaway JW. 2019. The hunt for RNA polymerase II elongation factors: a historical perspective. Nat. Struct. Mol. Biol. 26:771–76
     [Google Scholar]
  44. Cramer P. 2002. Multisubunit RNA polymerases. Curr. Opin. Struct. Biol. 12:89–97
     [Google Scholar]
  45. Cramer P. 2007. Extending the message. Nature 448:142–43
     [Google Scholar]
  46. Cramer P, Bushnell DA, Fu J, Gnatt AL, Maier-Davis B et al. 2000. Architecture of RNA polymerase II and implications for the transcription mechanism. Science 288:640–49
     [Google Scholar]
  47. Cramer P, Bushnell DA, Kornberg RD 2001. Structural basis of transcription: RNA polymerase II at 2.8 Ångstrom resolution. Science 292:1863–76
     [Google Scholar]
  48. Damsma GE, Alt A, Brueckner F, Carell T, Cramer P 2007. Mechanism of transcriptional stalling at cisplatin-damaged DNA. Nat. Struct. Mol. Biol 14:1127–33
     [Google Scholar]
  49. Damsma GE, Cramer P. 2009. Molecular basis of transcriptional mutagenesis at 8-oxoguanine. J. Biol. Chem. 284:31658–63
     [Google Scholar]
  50. Darst SA, Edwards AM, Kubalek EW, Kornberg RD 1991. Three-dimensional structure of yeast RNA polymerase II at 16 Å resolution. Cell 66:121–28
     [Google Scholar]
  51. Davis JA, Takagi Y, Kornberg RD, Asturias FJ 2002. Structure of the yeast RNA polymerase II holoenzyme: mediator conformation and polymerase interaction. Mol. Cell 10:409–15
     [Google Scholar]
  52. Dengl S, Cramer P. 2009. Torpedo nuclease Rat1 is insufficient to terminate RNA polymerase II in vitro. J. Biol. Chem. 284:21270–9
     [Google Scholar]
  53. Descostes N, Heidemann M, Spinelli L, Schüller R, Maqbool MA et al. 2014. Tyrosine phosphorylation of RNA polymerase II CTD is associated with antisense promoter transcription and active enhancers in mammalian cells. eLife 3:e02105
     [Google Scholar]
  54. Díaz-Santín LM, Lukoyanova N, Aciyan E, Cheung ACM 2017. Cryo-EM structure of the SAGA and NuA4 coactivator subunit Tra1 at 3.7 angstrom resolution. eLife 6:e28384
     [Google Scholar]
  55. 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]
  56. Ebright RH. 2000. RNA polymerase: structural similarities between bacterial RNA polymerase and eukaryotic RNA polymerase II. J. Mol. Biol. 304:687–98
     [Google Scholar]
  57. Edwards AM, Kane C, Young R, Kornberg RD 1991. Two dissociable subunits of yeast RNA polymerase II stimulate the initiation of transcription at a promoter in vitro. J. Biol. Chem. 266:71–75
     [Google Scholar]
  58. Ehara H, Kujirai T, Fujino Y, Shirouzu M, Kurumizaka H, Sekine SI 2019. Structural insight into nucleosome transcription by RNA polymerase II with elongation factors. Science 363:744–47
     [Google Scholar]
  59. Ehara H, Umehara T, Sekine SI, Yokoyama S 2017a. Crystal structure of RNA polymerase II from Komagataella pastoris.Biochem.Biophys.Res. . Commun 487:230–35
     [Google Scholar]
  60. Ehara H, Yokoyama T, Shigematsu H, Yokoyama S, Shirouzu M, Sekine S 2017b. Structure of the complete elongation complex of RNA polymerase II with basal factors. Science 357:921–24
     [Google Scholar]
  61. Eichner J, Chen HT, Warfield L, Hahn S 2010. Position of the general transcription factor TFIIF within the RNA polymerase II transcription preinitiation complex. EMBO J 29:706–16
     [Google Scholar]
  62. Eick D, Geyer M. 2013. The RNA polymerase II carboxy-terminal domain (CTD) code. Chem. Rev. 113:8456–90
     [Google Scholar]
  63. El Khattabi L, Zhao H, Kalchschmidt J, Young N, Jung S et al. 2019. A pliable mediator acts as a functional rather than an architectural bridge between promoters and enhancers. Cell 178:1145–58.e20
     [Google Scholar]
  64. Engel C, Neyer S, Cramer P 2018. Distinct mechanisms of transcription initiation by RNA polymerases I and II. Annu. Rev. Biophys. 47:425–46
     [Google Scholar]
  65. Epshtein V, Mustaev A, Markovtsov V, Bereshchenko O, Nikiforov V, Goldfarb A 2002. Swing-gate model of nucleotide entry into the RNA polymerase active center. Mol. Cell 10:623–34
     [Google Scholar]
  66. Farnung L, Vos SM, Cramer P 2018. Structure of transcribing RNA polymerase II-nucleosome complex. Nat. Commun. 9:5432
     [Google Scholar]
  67. Farnung L, Vos SM, Wigge C, Cramer P 2017. Nucleosome–Chd1 structure and implications for chromatin remodelling. Nature 550:539–42
     [Google Scholar]
  68. Fishburn J, Hahn S. 2012. Architecture of the yeast RNA polymerase II open complex and regulation of activity by TFIIF. Mol. Cell. Biol. 32:12–25
     [Google Scholar]
  69. 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. PNAS 112:3961–66
     [Google Scholar]
  70. Fu J, Gnatt AL, Bushnell DA, Jensen GJ, Thompson NE et al. 1999. Yeast RNA polymerase II at 5 Å resolution. Cell 98:799–810
     [Google Scholar]
  71. García-Muse T, Aguilera A. 2016. Transcription–replication conflicts: how they occur and how they are resolved. Nat. Rev. Mol. Cell Biol. 17:553
     [Google Scholar]
  72. Geiger JH, Hahn S, Lee S, Sigler PB 1996. Crystal structure of the yeast TFIIA/TBP/DNA complex. Science 272:830–36
     [Google Scholar]
  73. Gelles J, Landick R. 1998. RNA polymerase as a molecular motor. Cell 93:13–16
     [Google Scholar]
  74. Gnatt AL, Cramer P, Fu J, Bushnell DA, Kornberg RD 2001. Structural basis of transcription: an RNA polymerase II elongation complex at 3.3 Å resolution. Science 292:1876–82
     [Google Scholar]
  75. Gnatt AL, Fu J, Kornberg RD 1997. Formation and crystallization of yeast RNA polymerase II elongation complexes. J. Biol. Chem. 272:30799–805
     [Google Scholar]
  76. Gonzalez MN, Sato S, Tomomori-Sato C, Conaway JW, Conaway RC 2018. CTD-dependent and -independent mechanisms govern co-transcriptional capping of Pol II transcripts. Nat. Commun. 9:3392
     [Google Scholar]
  77. Greber BJ, Nguyen THD, Fang J, Afonine PV, Adams PD, Nogales E 2017. The cryo-electron microscopy structure of human transcription factor IIH. Nature 549:414–17
     [Google Scholar]
  78. Greber BJ, Toso DB, Fang J, Nogales E 2019. The complete structure of the human TFIIH core complex. eLife 8:e44771
     [Google Scholar]
  79. Grimm C, Hillen HS, Bedenk K, Bartuli J, Neyer S et al. 2019. Structural basis of Poxvirus transcription: Vaccinia RNA polymerase complexes. Cell 179:1537–50.e19
     [Google Scholar]
  80. Grohmann D, Nagy J, Chakraborty A, Klose D, Fielden D et al. 2011. The initiation factor TFE and the elongation factor Spt4/5 compete for the RNAP clamp during transcription initiation and elongation. Mol. Cell 43:263–74
     [Google Scholar]
  81. 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
     [Google Scholar]
  82. Guzder SN, Sung P, Bailly V, Prakash L, Prakash S 1994. RAD25 is a DMA helicase required for DNA repair and RNA polymerase II transcription. Nature 369:578–81
     [Google Scholar]
  83. Hahn S, Young ET. 2011. Transcriptional regulation in Saccharomyces cerevisiae: transcription factor regulation and function, mechanisms of initiation, and roles of activators and coactivators. Genetics 189:705–36
     [Google Scholar]
  84. Hantsche M, Cramer P. 2017. Conserved RNA polymerase II initiation complex structure. Curr. Opin. Struct. Biol. 47:17–22
     [Google Scholar]
  85. He Y, Fang J, Taatjes DJ, Nogales E 2013. Structural visualization of key steps in human transcription initiation. Nature 495:481–86
     [Google Scholar]
  86. He Y, Yan C, Fang J, Inouye C, Tjian R et al. 2016. Near-atomic resolution visualization of human transcription promoter opening. Nature 533:359–65
     [Google Scholar]
  87. Helmlinger D, Tora L. 2017. Sharing the SAGA. Trends Biochem. Sci. 42:850–61
     [Google Scholar]
  88. Hillen HS, Bartuli J, Grimm C, Dienemann C, Bedenk K et al. 2019. Structural basis of Poxvirus transcription: transcribing and capping Vaccinia complexes. Cell 179:1525–36.e12
     [Google Scholar]
  89. Hirtreiter A, Damsma GE, Cheung AC, Klose D, Grohmann D et al. 2010. Spt4/5 stimulates transcription elongation through the RNA polymerase clamp coiled-coil motif. Nucleic Acids Res 38:4040–51
     [Google Scholar]
  90. Ho CK, Shuman S. 1999. Distinct roles for CTD Ser-2 and Ser-5 phosphorylation in the recruitment and allosteric activation of mammalian mRNA capping enzyme. Mol. Cell 3:405–11
     [Google Scholar]
  91. Jeronimo C, Robert F. 2014. Kin28 regulates the transient association of Mediator with core promoters. Nat. Struct. Mol. Biol. 21:449
     [Google Scholar]
  92. Jeronimo C, Robert F. 2017. The mediator complex: at the nexus of RNA polymerase II transcription. Trends Cell Biol 27:765–83
     [Google Scholar]
  93. Jishage M, Yu X, Shi Y, Ganesan SJ, Chen WY et al. 2018. Architecture of Pol II(G) and molecular mechanism of transcription regulation by Gdown1. Nat. Struct. Mol. Biol. 25:859–67
     [Google Scholar]
  94. Juven-Gershon T, Hsu J-Y, Theisen JW, Kadonaga JT 2008. The RNA polymerase II core promoter—the gateway to transcription. Curr. Opin. Cell Biol. 20:253–59
     [Google Scholar]
  95. Kadonaga JT. 2012. Perspectives on the RNA polymerase II core promoter. Dev. Biol. 1:40–51
     [Google Scholar]
  96. Kang JY, Mishanina TV, Landick R, Darst SA 2019. Mechanisms of transcriptional pausing in bacteria. J. Mol. Biol. 431:4007–29
     [Google Scholar]
  97. Kaplan CD, Larsson KM, Kornberg RD 2008. The RNA polymerase II trigger loop functions in substrate selection and is directly targeted by α-amanitin. Mol. Cell 30:547–56
     [Google Scholar]
  98. Kettenberger H, Armache K-J, Cramer P 2003. Architecture of the RNA polymerase II-TFIIS complex and implications for mRNA cleavage. Cell 114:347–57
     [Google Scholar]
  99. Kettenberger H, Armache K-J, Cramer P 2004. Complete RNA polymerase II elongation complex structure and its interactions with NTP and TFIIS. Mol. Cell 16:955–65
     [Google Scholar]
  100. Kettenberger H, Eisenführ A, Brueckner F, Theis M, Famulok M, Cramer P 2006. Structure of an RNA polymerase II–RNA inhibitor complex elucidates transcription regulation by noncoding RNAs. Nat. Struct. Mol. Biol. 13:44–48
     [Google Scholar]
  101. Khatter H, Vorlaender MK, Mueller CW 2017. RNA polymerase I and III: similar yet unique. Curr. Opin. Struct. Biol. 47:88–94
     [Google Scholar]
  102. Kim T-K, Ebright RH, Reinberg D 2000. Mechanism of ATP-dependent promoter melting by transcription factor IIH. Science 288:1418–21
     [Google Scholar]
  103. Kinkelin K, Wozniak GG, Rothbart SB, Lidschreiber M, Strahl BD, Cramer P 2013. Structures of RNA polymerase II complexes with Bye1, a chromatin-binding PHF3/DIDO homologue. PNAS 110:15277–82
     [Google Scholar]
  104. Kireeva ML, Hancock B, Cremona GH, Walter W, Studitsky VM, Kashlev M 2005. Nature of the nucleosomal barrier to RNA polymerase II. Mol. Cell 18:97–108
     [Google Scholar]
  105. Kireeva ML, Kashlev M, Burton ZF 2010. Translocation by multi-subunit RNA polymerases. Biochim. Biophys. Acta Gene Regul. Mech. 1799:389–401
     [Google Scholar]
  106. Kireeva ML, Komissarova N, Waugh DS, Kashlev M 2000. The 8-nucleotide-long RNA:DNA hybrid is a primary stability determinant of the RNA polymerase II elongation complex. J. Biol. Chem. 275:6530–36
     [Google Scholar]
  107. Kireeva ML, Nedialkov YA, Cremona GH, Purtov YA, Lubkowska L et al. 2008. Transient reversal of RNA polymerase II active site closing controls fidelity of transcription elongation. Mol. Cell 30:557–66
     [Google Scholar]
  108. Klein BJ, Bose D, Baker KJ, Yusoff ZM, Zhang X, Murakami KS 2011. RNA polymerase and transcription elongation factor Spt4/5 complex structure. PNAS 108:546–50
     [Google Scholar]
  109. Kokic G, Chernev A, Tegunov D, Dienemann C, Urlaub H, Cramer P 2019. Structural basis of TFIIH activation for nucleotide excision repair. Nat. Commun. 10:2885
     [Google Scholar]
  110. Komarnitsky P, Cho E-J, Buratowski S 2000. Different phosphorylated forms of RNA polymerase II and associated mRNA processing factors during transcription. Genes Dev 14:2452–60
     [Google Scholar]
  111. Kosa PF, Ghosh G, DeDecker BS, Sigler PB 1997. The 2.1-Å crystal structure of an archaeal preinitiation complex: TATA-box-binding protein/transcription factor (II)B core/TATA-box. PNAS 94:6042–47
     [Google Scholar]
  112. Kostrewa D, Zeller ME, Armache KJ, Seizl M, Leike K et al. 2009. RNA polymerase II-TFIIB structure and mechanism of transcription initiation. Nature 462:323–30
     [Google Scholar]
  113. Kuhn C-D, Geiger SR, Baumli S, Gartmann M, Gerber J et al. 2007. Functional architecture of RNA polymerase I. Cell 131:1260–72
     [Google Scholar]
  114. Kujirai T, Ehara H, Fujino Y, Shirouzu M, Sekine S, Kurumizaka H 2018. Structural basis of the nucleosome transition during RNA polymerase II passage. Science 362:595–98
     [Google Scholar]
  115. Lahiri I, Xu J, Han BG, Oh J, Wang D et al. 2019. 3.1 Å structure of yeast RNA polymerase II elongation complex stalled at a cyclobutane pyrimidine dimer lesion solved using streptavidin affinity grids. J. Struct. Biol. 207:270–78
     [Google Scholar]
  116. Landick R. 2009. Transcriptional pausing without backtracking. PNAS 106:8797–98
     [Google Scholar]
  117. Lans H, Hoeijmakers JHJ, Vermeulen W, Marteijn JA 2019. The DNA damage response to transcription stress. Nat. Rev. Mol. Cell Biol. 20:766–84
     [Google Scholar]
  118. Larivière L, Plaschka C, Seizl M, Wenzeck L, Kurth F, Cramer P 2012a. Structure of the Mediator head module. Nature 492:448–51
     [Google Scholar]
  119. Larivière L, Seizl M, Cramer P 2012b. A structural perspective on Mediator function. Curr. Opin. Cell Biol. 24:305–13
     [Google Scholar]
  120. Lehmann E, Brueckner F, Cramer P 2007. Molecular basis of RNA-dependent RNA polymerase II activity. Nature 450:445–49
     [Google Scholar]
  121. LeRoy G, Oksuz O, Descostes N, Aoi Y, Ganai RA et al. 2019. LEDGF and HDGF2 relieve the nucleosome-induced barrier to transcription in differentiated cells. Sci. Adv. 5:eaay3068
     [Google Scholar]
  122. Lidschreiber M, Leike K, Cramer P 2013. Cap completion and C-terminal repeat domain kinase recruitment underlie the initiation-elongation transition of RNA polymerase II. Mol. Cell. Biol. 33:3805–16
     [Google Scholar]
  123. Liu X, Bushnell DA, Silva DA, Huang X, Kornberg RD 2011. Initiation complex structure and promoter proofreading. Science 333:633–7
     [Google Scholar]
  124. 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 327:206–9
     [Google Scholar]
  125. Liu X, Farnung L, Wigge C, Cramer P 2018. Cryo-EM structure of a mammalian RNA polymerase II elongation complex inhibited by α-amanitin. J. Biol. Chem. 293:7189–94
     [Google Scholar]
  126. Liu Y, Zhou K, Zhang N, Wei H, Tan YZ et al. 2020. FACT caught in the act of manipulating the nucleosome. Nature 577:426–31
     [Google Scholar]
  127. 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 531:604–9
     [Google Scholar]
  128. Malagon F, Kireeva ML, Shafer BK, Lubkowska L, Kashlev M, Strathern JN 2006. Mutations in the Saccharomyces cerevisiae RPB1 gene conferring hypersensitivity to 6-azauracil. Genetics 172:2201–9
     [Google Scholar]
  129. Malik S, Roeder RG. 2010. The metazoan Mediator co-activator complex as an integrative hub for transcriptional regulation. Nat. Rev. Genet. 11:761–72
     [Google Scholar]
  130. Malvezzi S, Farnung L, Aloisi CMN, Angelov T, Cramer P, Sturla SJ 2017. Mechanism of RNA polymerase II stalling by DNA alkylation. PNAS 114:12172–77
     [Google Scholar]
  131. Marshall NF, Price DH. 1992. Control of formation of two distinct classes of RNA polymerase II elongation complexes. Mol. Cell. Biol. 12:2078–90
     [Google Scholar]
  132. Martinez-Rucobo FW, Cramer P. 2013. Structural basis of transcription elongation. Biochim. Biophys. Acta Gene Regul. Mech. 1829:9–19
     [Google Scholar]
  133. Martinez-Rucobo FW, Kohler R, van de Waterbeemd M, Heck AJ, Hemann M et al. 2015. Molecular basis of transcription-coupled pre-mRNA capping. Mol. Cell 58:1079–89
     [Google Scholar]
  134. Martinez‐Rucobo FW, Sainsbury S, Cheung AC, Cramer P 2011. Architecture of the RNA polymerase–Spt4/5 complex and basis of universal transcription processivity. EMBO J 30:1302–10
     [Google Scholar]
  135. 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 8:515–24
     [Google Scholar]
  136. Mayer A, Heidemann M, Lidschreiber M, Schreieck A, Sun M et al. 2012. CTD tyrosine phosphorylation impairs termination factor recruitment to RNA polymerase II. Science 336:1723–25
     [Google Scholar]
  137. McCracken S, Fong N, Rosonina E, Yankulov K, Brothers G et al. 1997a. 5′-Capping enzymes are targeted to pre-mRNA by binding to the phosphorylated carboxy-terminal domain of RNA polymerase II. Genes Dev 11:3306–18
     [Google Scholar]
  138. McCracken S, Fong N, Yankulov K, Ballantyne S, Pan G et al. 1997b. The C-terminal domain of RNA polymerase II couples mRNA processing to transcription. Nature 385:357–61
     [Google Scholar]
  139. Meinhart A, Kamenski T, Hoeppner S, Baumli S, Cramer P 2005. A structural perspective of CTD function. Genes Dev 19:1401–15
     [Google Scholar]
  140. Meredith GD, Chang W-H, Li Y, Bushnell DA, Darst SA, Kornberg RD 1996. The C-terminal domain revealed in the structure of RNA polymerase II. J. Mol. Biol. 258:413–19
     [Google Scholar]
  141. Meyer PA, Ye P, Suh MH, Zhang M, Fu J 2009. Structure of the 12-subunit RNA polymerase II refined with the aid of anomalous diffraction data. J. Biol. Chem. 284:12933–39
     [Google Scholar]
  142. Meyer PA, Ye P, Zhang M, Suh MH, Fu J 2006. Phasing RNA polymerase II using intrinsically bound Zn atoms: an updated structural model. Structure 14:973–82
     [Google Scholar]
  143. Monté D, Clantin B, Dewitte F, Lens Z, Rucktooa P et al. 2018. Crystal structure of human Mediator subunit MED23. Nat. Commun. 9:3389
     [Google Scholar]
  144. Morgan MT, Haj-Yahya M, Ringel AE, Bandi P, Brik A, Wolberger C 2016. Structural basis for histone H2B deubiquitination by the SAGA DUB module. Science 351:725–28
     [Google Scholar]
  145. Moteki S, Price D. 2002. Functional coupling of capping and transcription of mRNA. Mol. Cell 10:599–609
     [Google Scholar]
  146. Mühlbacher W, Sainsbury S, Hemann M, Hantsche M, Neyer S et al. 2014. Conserved architecture of the core RNA polymerase II initiation complex. Nat. Commun. 5:4310
     [Google Scholar]
  147. Mullen Davis MA, Guo J, Price DH, Luse DS 2014. Functional interactions of the RNA polymerase II-interacting proteins Gdown1 and TFIIF. J. Biol. Chem. 289:11143–52
     [Google Scholar]
  148. Murakami K, Elmlund H, Kalisman N, Bushnell DA, Adams CM et al. 2013. Architecture of an RNA polymerase II transcription pre-initiation complex. Science 342:1238724
     [Google Scholar]
  149. Murakami K, Tsai KL, Kalisman N, Bushnell DA, Asturias FJ, Kornberg RD 2015. Structure of an RNA polymerase II preinitiation complex. PNAS 112:13543–48
     [Google Scholar]
  150. Murakami KS, Darst SA. 2003. Bacterial RNA polymerases: the wholo story. Curr. Opin. Struct. Biol. 13:31–39
     [Google Scholar]
  151. NandyMazumdar M, Artsimovitch I. 2015. Ubiquitous transcription factors display structural plasticity and diverse functions: NusG proteins–shifting shapes and paradigms. Bioessays 37:324–34
     [Google Scholar]
  152. Nikolov DB, Chen H, Halay ED, Usheva AA, Hisatake K et al. 1995. Crystal structure of a TFIIB–TBP–TATA-element ternary complex. Nature 377:119–28
     [Google Scholar]
  153. Nogales E, Louder RK, He Y 2017. Structural insights into the eukaryotic transcription initiation machinery. Annu. Rev. Biophys. 46:59–83
     [Google Scholar]
  154. Nozawa K, Schneider TR, Cramer P 2017. Core Mediator structure at 3.4 Å extends model of transcription initiation complex. Nature 545:248–51
     [Google Scholar]
  155. Oberthuer D, Knoška J, Wiedorn MO, Beyerlein KR, Bushnell DA et al. 2017. Double-flow focused liquid injector for efficient serial femtosecond crystallography. Sci. Rep. 7:44628
     [Google Scholar]
  156. O'Reilly FJ, Xue L, Graziadei A, Sinn L, Lenz S et al. 2020. In-cell architecture of an actively transcribing-translating expressome. bioRxiv 970111. https://doi.org/10.1101/2020.02.28.970111
    [Crossref]
  157. Palangat M, Renner DB, Price DH, Landick R 2005. A negative elongation factor for human RNA polymerase II inhibits the anti-arrest transcript-cleavage factor TFIIS. PNAS 102:15036–41
     [Google Scholar]
  158. Papai G, Frechard A, Kolesnikova O, Crucifix C, Schultz P, Ben-Shem A 2020. Structure of SAGA and mechanism of TBP deposition on gene promoters. Nature 577:711–16
     [Google Scholar]
  159. Patel AB, Louder RK, Greber BJ, Grünberg S, Luo J et al. 2018. Structure of human TFIID and mechanism of TBP loading onto promoter DNA. Science 362:eaau8872
     [Google Scholar]
  160. Petrenko N, Jin Y, Wong KH, Struhl K 2016. Mediator undergoes a compositional change during transcriptional activation. Mol. Cell 64:443–54
     [Google Scholar]
  161. Plaschka C, Hantsche M, Dienemann C, Burzinski C, Plitzko J, Cramer P 2016a. Transcription initiation complex structures elucidate DNA opening. Nature 533:353–58
     [Google Scholar]
  162. Plaschka C, Larivière L, Wenzeck L, Seizl M, Hemann M et al. 2015. Architecture of the RNA polymerase II-Mediator core initiation complex. Nature 518:376–80
     [Google Scholar]
  163. Plaschka C, Nozawa K, Cramer P 2016b. Mediator architecture and RNA polymerase II interaction. J. Mol. Biol. 428:2569–74
     [Google Scholar]
  164. Poglitsch CL, Meredith GD, Gnatt AL, Jensen GJ, Chang W-H et al. 1999. Electron crystal structure of an RNA polymerase II transcription elongation complex. Cell 98:791–98
     [Google Scholar]
  165. Ramanathan A, Robb GB, Chan S-H 2016. mRNA capping: biological functions and applications. Nucleic Acids Res 44:7511–26
     [Google Scholar]
  166. Reinberg D, Orphanides G, Ebright R, Akoulitchev S, Carcamo J et al. 1998. The RNA polymerase II general transcription factors: past, present, and future. Cold Spring Harbor Symposia on Quantitative Biology, Vol. 63 Stillman 83–105 Cold Spring Harbor, NY: Cold Spring Harb. Lab. Press
     [Google Scholar]
  167. Robinson PJ, 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. PNAS 109:17931–35
     [Google Scholar]
  168. Robinson PJ, Trnka MJ, Bushnell DA, Davis RE, Mattei PJ et al. 2016. Structure of a complete Mediator-RNA polymerase II pre-initiation complex. Cell 166:1411–22.e16
     [Google Scholar]
  169. Roeder RG. 2019. 50+ years of eukaryotic transcription: an expanding universe of factors and mechanisms. Nat. Struct. Mol. Biol. 26:783–91
     [Google Scholar]
  170. Ruan W, Lehmann E, Thomm M, Kostrewa D, Cramer P 2011. Evolution of two modes of intrinsic RNA polymerase transcript cleavage. J. Biol. Chem. 286:18701–7
     [Google Scholar]
  171. Sainsbury S, Bernecky C, Cramer P 2015. Structural basis of transcription initiation by RNA polymerase II. Nat. Rev. Mol. Cell Biol. 16:129–43
     [Google Scholar]
  172. Sainsbury S, Niesser J, Cramer P 2013. Structure and function of the initially transcribing RNA polymerase II-TFIIB complex. Nature 493:437–40
     [Google Scholar]
  173. Samara NL, Wolberger C. 2011. A new chapter in the transcription SAGA. Curr. Opin. Struct. Biol. 21:767–74
     [Google Scholar]
  174. Sayre MH, Tschochner H, Kornberg RD 1992. Reconstitution of transcription with five purified initiation factors and RNA polymerase II from Saccharomyces cerevisiae. J. Biol. Chem 267:23376–82
     [Google Scholar]
  175. Schilbach S, Hantsche M, Tegunov D, Dienemann C, Wigge C et al. 2017. Structures of transcription pre-initiation complex with TFIIH and Mediator. Nature 551:204–9
     [Google Scholar]
  176. Schulz S, Gietl A, Smollett K, Tinnefeld P, Werner F, Grohmann D 2016. TFE and Spt4/5 open and close the RNA polymerase clamp during the transcription cycle. PNAS 113:E1816–25
     [Google Scholar]
  177. Seizl M, Hartmann H, Hoeg F, Kurth F, Martin DE et al. 2011. A conserved GA element in TATA-less RNA polymerase II promoters. PLOS ONE 6:e27595
     [Google Scholar]
  178. Shetty A, Kallgren SP, Demel C, Maier KC, Spatt D et al. 2017. Spt5 plays vital roles in the control of sense and antisense transcription elongation. Mol. Cell 66:77–88.e5
     [Google Scholar]
  179. Shilatifard A, Conaway RC, Conaway JW 2003. The RNA polymerase II elongation complex. Annu. Rev. Biochem. 72:693–715
     [Google Scholar]
  180. Sosunov V, Sosunova E, Mustaev A, Bass I, Nikiforov V, Goldfarb A 2003. Unified two‐metal mechanism of RNA synthesis and degradation by RNA polymerase. EMBO J 22:2234–44
     [Google Scholar]
  181. Spåhr H, Calero G, Bushnell DA, Kornberg RD 2009. Schizosaccharomyces pombe RNA polymerase II at 3.6-Å resolution. PNAS 106:9185–90
     [Google Scholar]
  182. Steitz T, Smerdon S, Jager J, Joyce C, Pelletier H 1994. A unified polymerase mechanism for nonhomologous DNA and RNA polymerases–comment/reply. Science 266:2022
     [Google Scholar]
  183. Svejstrup JQ, Vichi P, Egly J-M 1996. The multiple roles of transcription/repair factor TFIIH. Trends Biochem. Sci. 21:346–50
     [Google Scholar]
  184. Svejstrup JQ, Wang Z, Feave WJ, Wu X, Bushnell DA et al. 1995. Different forms of TFIIH for transcription and DNA repair: holo-TFIIH and a nucleotide excision repairosome. Cell 80:21–28
     [Google Scholar]
  185. Svetlov V, Vassylyev DG, Artsimovitch I 2004. Discrimination against deoxyribonucleotide substrates by bacterial RNA polymerase. J. Biol. Chem. 279:38087–90
     [Google Scholar]
  186. Sydow JF, Brueckner F, Cheung AC, Damsma GE, Dengl S et al. 2009. Structural basis of transcription: mismatch-specific fidelity mechanisms and paused RNA polymerase II with frayed RNA. Mol. Cell 34:710–21
     [Google Scholar]
  187. Sydow JF, Cramer P. 2009. RNA polymerase fidelity and transcriptional proofreading. Curr. Opin. Struct. Biol. 19:732–39
     [Google Scholar]
  188. Takagi Y, Kornberg RD. 2006. Mediator as a general transcription factor. J. Biol. Chem. 281:80–89
     [Google Scholar]
  189. Tan S, Hunziker Y, Sargent DF, Richmond TJ 1996. Crystal structure of a yeast TFIIA/TBP/DNA complex. Nature 381:127–34
     [Google Scholar]
  190. Thomas MJ, Platas AA, Hawley DK 1998. Transcriptional fidelity and proofreading by RNA polymerase II. Cell 93:627–37
     [Google Scholar]
  191. Thompson N, Aronson D, Burgess R 1990. Purification of eukaryotic RNA polymerase II by immunoaffinity chromatography. Elution of active enzyme with protein stabilizing agents from a polyol-responsive monoclonal antibody. J. Biol. Chem. 265:7069–77
     [Google Scholar]
  192. Tirode F, Busso D, Coin F, Egly J-M 1999. Reconstitution of the transcription factor TFIIH: assignment of functions for the three enzymatic subunits, XPB, XPD, and cdk7. Mol. Cell 3:87–95
     [Google Scholar]
  193. 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
     [Google Scholar]
  194. Tsai K-L, Yu X, Gopalan S, Chao TC, Zhang Y et al. 2017. Mediator structure and rearrangements required for holoenzyme formation. Nature 544:196–201
     [Google Scholar]
  195. Tuske S, Sarafianos SG, Wang X, Hudson B, Sineva E et al. 2005. Inhibition of bacterial RNA polymerase by streptolydigin: stabilization of a straight-bridge-helix active-center conformation. Cell 122:541–52
     [Google Scholar]
  196. Van Oss SB, Cucinotta CE, Arndt KM 2017. Emerging insights into the roles of the Paf1 complex in gene regulation. Trends Biochem. Sci. 42:788–98
     [Google Scholar]
  197. Vassylyev DG, Vassylyeva MN, Zhang J, Palangat M, Artsimovitch I, Landick R 2007. Structural basis for substrate loading in bacterial RNA polymerase. Nature 448:163–68
     [Google Scholar]
  198. Vos SM, Farnung L, Boehning M, Wigge C, Linden A et al. 2018a. Structure of activated transcription complex Pol II-DSIF-PAF-SPT6. Nature 560:607–12
     [Google Scholar]
  199. Vos SM, Farnung L, Linden A, Urlaub H, Cramer P 2020. Structure of complete Pol II-DSIF-PAF-SPT6 transcription complex reveals RTF1 allosteric activation. Nat. Struct. Mol. Biol. 27:668–77
     [Google Scholar]
  200. Vos SM, Farnung L, Urlaub H, Cramer P 2018b. Structure of paused transcription complex Pol II-DSIF-NELF. Nature 560:601–6
     [Google Scholar]
  201. Walmacq C, Cheung AC, Kireeva ML, Lubkowska L, Ye C et al. 2012. Mechanism of translesion transcription by RNA polymerase II and its role in cellular resistance to DNA damage. Mol. Cell 46:18–29
     [Google Scholar]
  202. Walmacq C, Wang L, Chong J, Scibelli K, Lubkowska L et al. 2015. Mechanism of RNA polymerase II bypass of oxidative cyclopurine DNA lesions. PNAS 112:E410–19
     [Google Scholar]
  203. Wang D, Bushnell DA, Huang X, Westover KD, Levitt M, Kornberg RD 2009. Structural basis of transcription: backtracked RNA polymerase II at 3.4 angstrom resolution. Science 324:1203–6
     [Google Scholar]
  204. 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 127:941–54
     [Google Scholar]
  205. Wang D, Zhu G, Huang X, Lippard SJ 2010. X-ray structure and mechanism of RNA polymerase II stalled at an antineoplastic monofunctional platinum-DNA adduct. PNAS 107:9584–89
     [Google Scholar]
  206. Wang H, Dienemann C, Stützer A, Urlaub H, Cheung AC, Cramer P 2020. Structure of the transcription coactivator SAGA. Nature 577:717–20
     [Google Scholar]
  207. Wang L, Zhou Y, Xu L, Xiao R, Lu X et al. 2015. Molecular basis for 5-carboxycytosine recognition by RNA polymerase II elongation complex. Nature 523:621–25
     [Google Scholar]
  208. Wang W, Walmacq C, Chong J, Kashlev M, Wang D 2018. Structural basis of transcriptional stalling and bypass of abasic DNA lesion by RNA polymerase II. PNAS 115:E2538–45
     [Google Scholar]
  209. Wang W, Xu L, Hu L, Chong J, He C, Wang D 2017. Epigenetic DNA modification N(6)-methyladenine causes site-specific RNA polymerase II transcriptional pausing. J. Am. Chem. Soc. 139:14436–42
     [Google Scholar]
  210. Wang X, Wang J, Ding Z, Ji J, Sun Q, Cai G 2013. Structural flexibility and functional interaction of Mediator Cdk8 module. Protein Cell 4:911–20
     [Google Scholar]
  211. Weinzierl RO. 2012. The Bridge Helix of RNA polymerase acts as a central nanomechanical switchboard for coordinating catalysis and substrate movement. Archaea 2011:608385
     [Google Scholar]
  212. Weixlbaumer A, Leon K, Landick R, Darst SA 2013. Structural basis of transcriptional pausing in bacteria. Cell 152:431–41
     [Google Scholar]
  213. Wen Y, Shatkin AJ. 1999. Transcription elongation factor hSPT5 stimulates mRNA capping. Genes Dev 13:1774–79
     [Google Scholar]
  214. Werner F. 2007. Structure and function of archaeal RNA polymerases. Mol. Microbiol. 65:1395–404
     [Google Scholar]
  215. Werner F. 2012. A nexus for gene expression—molecular mechanisms of Spt5 and NusG in the three domains of life. J. Mol. Biol. 417:13–27
     [Google Scholar]
  216. Westover KD, Bushnell DA, Kornberg RD 2004a. Structural basis of transcription: nucleotide selection by rotation in the RNA polymerase II active center. Cell 119:481–89
     [Google Scholar]
  217. Westover KD, Bushnell DA, Kornberg RD 2004b. Structural basis of transcription: separation of RNA from DNA by RNA polymerase II. Science 303:1014–16
     [Google Scholar]
  218. Wigley DB, Bowman GD. 2017. A glimpse into chromatin remodeling. Nat. Struct. Mol. Biol. 24:498–500
     [Google Scholar]
  219. Wu C-H, Yamaguchi Y, Benjamin LR, Horvat-Gordon M, Washinsky J et al. 2003. NELF and DSIF cause promoter proximal pausing on the hsp70 promoter in Drosophila. . Genes Dev 17:1402–14
     [Google Scholar]
  220. Xu J, Lahiri I, Wang W, Wier A, Cianfrocco MA et al. 2017. Structural basis for the initiation of eukaryotic transcription-coupled DNA repair. Nature 551:653–57
     [Google Scholar]
  221. Xu L, Wang W, Chong J, Shin JH, Xu J, Wang D 2015. RNA polymerase II transcriptional fidelity control and its functional interplay with DNA modifications. Crit. Rev. Biochem. Mol. Biol. 50:503–19
     [Google Scholar]
  222. Xu Y, Bernecky C, Lee C-T, Maier KC, Schwalb B et al. 2017. Architecture of the RNA polymerase II-Paf1C-TFIIS transcription elongation complex. Nat. Commun. 8:15741
     [Google Scholar]
  223. Yamaguchi Y, Takagi T, Wada T, Yano K, Furuya A et al. 1999. NELF, a multisubunit complex containing RD, cooperates with DSIF to repress RNA polymerase II elongation. Cell 97:41–51
     [Google Scholar]
  224. Yan C, Dodd T, He Y, Tainer JA, Tsutakawa SE, Ivanov I 2019. Transcription preinitiation complex structure and dynamics provide insight into genetic diseases. Nat. Struct. Mol. Biol. 26:397–406
     [Google Scholar]
  225. Yu M, Yang W, Ni T, Tang Z, Nakadai T et al. 2015. RNA polymerase II–associated factor 1 regulates the release and phosphorylation of paused RNA polymerase II. Science 350:1383–86
     [Google Scholar]
  226. Zenkin N, Yuzenkova Y, Severinov K 2006. Transcript-assisted transcriptional proofreading. Science 313:518–20
     [Google Scholar]
  227. Zhang G, Campbell EA, Minakhin L, Richter C, Severinov K, Darst SA 1999. Crystal structure of Thermus aquaticus core RNA polymerase at 3.3 Å resolution. Cell 98:811–24
     [Google Scholar]
  228. Zhang J, Palangat M, Landick R 2010. Role of the RNA polymerase trigger loop in catalysis and pausing. Nat. Struct. Mol. Biol. 17:99–104
     [Google Scholar]
  229. Zhang S, Wang D. 2013. Understanding the molecular basis of RNA polymerase II transcription. Israel J. Chem. 53:442–49
     [Google Scholar]
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Structural Biology of RNA Polymerase II Transcription: 20 Years On
Annual Review of Cell and Developmental Biology 36, 1 (2020); https://doi.org/10.1146/annurev-cellbio-042020-021954
/content/journals/10.1146/annurev-cellbio-042020-021954
/content/journals/10.1146/annurev-cellbio-042020-021954
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