6f42 Citations

Molecular mechanism of promoter opening by RNA polymerase III.

OpenAccess logo Nature 553 295-300 (2018)
Related entries: 6f40, 6f41, 6f44

Cited: 69 times
EuropePMC logo PMID: 29345638

Abstract

RNA polymerase III (Pol III) and transcription factor IIIB (TFIIIB) assemble together on different promoter types to initiate the transcription of small, structured RNAs. Here we present structures of Pol III preinitiation complexes, comprising the 17-subunit Pol III and the heterotrimeric transcription factor TFIIIB, bound to a natural promoter in different functional states. Electron cryo-microscopy reconstructions, varying from 3.7 Å to 5.5 Å resolution, include two early intermediates in which the DNA duplex is closed, an open DNA complex, and an initially transcribing complex with RNA in the active site. Our structures reveal an extremely tight, multivalent interaction between TFIIIB and promoter DNA, and explain how TFIIIB recruits Pol III. Together, TFIIIB and Pol III subunit C37 activate the intrinsic transcription factor-like activity of the Pol III-specific heterotrimer to initiate the melting of double-stranded DNA, in a mechanism similar to that of the Pol II system.

Articles - 6f42 mentioned but not cited (5)

  1. Molecular mechanism of promoter opening by RNA polymerase III. Vorländer MK, Khatter H, Wetzel R, Hagen WJH, Müller CW. Nature 553 295-300 (2018)
  2. Cryo-EM structures of human RNA polymerase III in its unbound and transcribing states. Girbig M, Misiaszek AD, Vorländer MK, Lafita A, Grötsch H, Baudin F, Bateman A, Müller CW. Nat Struct Mol Biol 28 210-219 (2021)
  3. A Tool for Segmentation of Secondary Structures in 3D Cryo-EM Density Map Components Using Deep Convolutional Neural Networks. Mu Y, Sazzed S, Alshammari M, Sun J, He J. Front Bioinform 1 710119 (2021)
  4. Mechanism of RNA polymerase I selection by transcription factor UAF. Baudin F, Murciano B, Fung HKH, Fromm SA, Mattei S, Mahamid J, Müller CW. Sci Adv 8 eabn5725 (2022)
  5. Benchmark dataset for the Voronoi diagram of 3D spherical balls. Song C, Lee M, Choi S, Kim DS. Data Brief 45 108605 (2022)


Reviews citing this publication (17)

  1. Organization and regulation of gene transcription. Cramer P. Nature 573 45-54 (2019)
  2. tRNA Metabolism and Neurodevelopmental Disorders. Schaffer AE, Pinkard O, Coller JM. Annu Rev Genomics Hum Genet 20 359-387 (2019)
  3. Distinct Mechanisms of Transcription Initiation by RNA Polymerases I and II. Engel C, Neyer S, Cramer P. Annu Rev Biophys 47 425-446 (2018)
  4. Mechanisms of σ54-Dependent Transcription Initiation and Regulation. Danson AE, Jovanovic M, Buck M, Zhang X. J Mol Biol 431 3960-3974 (2019)
  5. Transfer RNAs: diversity in form and function. Berg MD, Brandl CJ. RNA Biol 18 316-339 (2021)
  6. Structural insights into nuclear transcription by eukaryotic DNA-dependent RNA polymerases. Girbig M, Misiaszek AD, Müller CW. Nat Rev Mol Cell Biol 23 603-622 (2022)
  7. RNA Polymerase III Subunit Mutations in Genetic Diseases. Lata E, Choquet K, Sagliocco F, Brais B, Bernard G, Teichmann M. Front Mol Biosci 8 696438 (2021)
  8. Regulation of ribosomal RNA gene copy number, transcription and nucleolus organization in eukaryotes. Hori Y, Engel C, Kobayashi T. Nat Rev Mol Cell Biol 24 414-429 (2023)
  9. The cryo-EM resolution revolution and transcription complexes. Hanske J, Sadian Y, Müller CW. Curr Opin Struct Biol 52 8-15 (2018)
  10. Cell Cycle-Dependent Transcription: The Cyclin Dependent Kinase Cdk1 Is a Direct Regulator of Basal Transcription Machineries. Enserink JM, Chymkowitch P. Int J Mol Sci 23 1293 (2022)
  11. The Structures of Eukaryotic Transcription Pre-initiation Complexes and Their Functional Implications. Greber BJ, Nogales E. Subcell Biochem 93 143-192 (2019)
  12. Light and shadow on the mechanisms of integration site selection in yeast Ty retrotransposon families. Bonnet A, Lesage P. Curr Genet 67 347-357 (2021)
  13. Retrotransposon targeting to RNA polymerase III-transcribed genes. Cheung S, Manhas S, Measday V. Mob DNA 9 14 (2018)
  14. Dynamics of the RNA polymerase I TFIIF/TFIIE-like subcomplex: a mini-review. Knutson BA, McNamar R, Rothblum LI. Biochem Soc Trans 48 1917-1927 (2020)
  15. Collaboration through chromatin: motors of transcription and chromatin structure. Gamarra N, Narlikar GJ. J Mol Biol 433 166876 (2021)
  16. The RNA polymerase III-RIG-I axis in antiviral immunity and inflammation. Naesens L, Haerynck F, Gack MU. Trends Immunol 44 435-449 (2023)
  17. Structural Studies of Eukaryotic RNA Polymerase I Using Cryo-Electron Microscopy. Pilsl M, Engel C. Methods Mol Biol 2533 71-80 (2022)

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  1. SPHIRE-crYOLO is a fast and accurate fully automated particle picker for cryo-EM. Wagner T, Merino F, Stabrin M, Moriya T, Antoni C, Apelbaum A, Hagel P, Sitsel O, Raisch T, Prumbaum D, Quentin D, Roderer D, Tacke S, Siebolds B, Schubert E, Shaikh TR, Lill P, Gatsogiannis C, Raunser S. Commun Biol 2 218 (2019)
  2. Stepwise Promoter Melting by Bacterial RNA Polymerase. Chen J, Chiu C, Gopalkrishnan S, Chen AY, Olinares PDB, Saecker RM, Winkelman JT, Maloney MF, Chait BT, Ross W, Gourse RL, Campbell EA, Darst SA. Mol Cell 78 275-288.e6 (2020)
  3. Structural visualization of RNA polymerase III transcription machineries. Han Y, Yan C, Fishbain S, Ivanov I, He Y. Cell Discov 4 40 (2018)
  4. Structure of human RNA polymerase III. Ramsay EP, Abascal-Palacios G, Daiß JL, King H, Gouge J, Pilsl M, Beuron F, Morris E, Gunkel P, Engel C, Vannini A. Nat Commun 11 6409 (2020)
  5. Structures of Bacterial RNA Polymerase Complexes Reveal the Mechanism of DNA Loading and Transcription Initiation. Glyde R, Ye F, Jovanovic M, Kotta-Loizou I, Buck M, Zhang X. Mol Cell 70 1111-1120.e3 (2018)
  6. Structural basis for RNA polymerase III transcription repression by Maf1. Vorländer MK, Baudin F, Moir RD, Wetzel R, Hagen WJH, Willis IM, Müller CW. Nat Struct Mol Biol 27 229-232 (2020)
  7. Structural insights into transcriptional regulation of human RNA polymerase III. Wang Q, Li S, Wan F, Xu Y, Wu Z, Cao M, Lan P, Lei M, Wu J. Nat Struct Mol Biol 28 220-227 (2021)
  8. Structural basis of ECF-σ-factor-dependent transcription initiation. Lin W, Mandal S, Degen D, Cho MS, Feng Y, Das K, Ebright RH. Nat Commun 10 710 (2019)
  9. Molecular insight into RNA polymerase I promoter recognition and promoter melting. Sadian Y, Baudin F, Tafur L, Murciano B, Wetzel R, Weis F, Müller CW. Nat Commun 10 5543 (2019)
  10. Inhibition of RNA polymerase III transcription by Triptolide attenuates colorectal tumorigenesis. Liang X, Xie R, Su J, Ye B, Wei S, Liang Z, Bai R, Chen Z, Li Z, Gao X. J Exp Clin Cancer Res 38 217 (2019)
  11. Structural basis of RNA polymerase I pre-initiation complex formation and promoter melting. Pilsl M, Engel C. Nat Commun 11 1206 (2020)
  12. Structures and mechanism of transcription initiation by bacterial ECF factors. Fang C, Li L, Shen L, Shi J, Wang S, Feng Y, Zhang Y. Nucleic Acids Res 47 7094-7104 (2019)
  13. RNA extension drives a stepwise displacement of an initiation-factor structural module in initial transcription. Li L, Molodtsov V, Lin W, Ebright RH, Zhang Y. Proc Natl Acad Sci U S A 117 5801-5809 (2020)
  14. DNA origami-based single-molecule force spectroscopy elucidates RNA Polymerase III pre-initiation complex stability. Kramm K, Schröder T, Gouge J, Vera AM, Gupta K, Heiss FB, Liedl T, Engel C, Berger I, Vannini A, Tinnefeld P, Grohmann D. Nat Commun 11 2828 (2020)
  15. Structure of human RNA polymerase III elongation complex. Li L, Yu Z, Zhao D, Ren Y, Hou H, Xu Y. Cell Res 31 791-800 (2021)
  16. The nuclear and cytoplasmic activities of RNA polymerase III, and an evolving transcriptome for surveillance. Kessler AC, Maraia RJ. Nucleic Acids Res 49 12017-12034 (2021)
  17. Function of TFIIIC, RNA polymerase III initiation factor, in activation and repression of tRNA gene transcription. Ciesla M, Skowronek E, Boguta M. Nucleic Acids Res 46 9444-9455 (2018)
  18. RNA polymerase III subunits C37/53 modulate rU:dA hybrid 3' end dynamics during transcription termination. Mishra S, Maraia RJ. Nucleic Acids Res 47 310-327 (2019)
  19. BRLF1 suppresses RNA Pol III-mediated RIG-I inflammasome activation in the early EBV lytic lifecycle. Long X, Yang J, Zhang X, Yang Z, Li Y, Wang F, Li X, Kuang E. EMBO Rep 22 e50714 (2021)
  20. De novo variants in POLR3B cause ataxia, spasticity, and demyelinating neuropathy. Djordjevic D, Pinard M, Gauthier MS, Smith-Hicks C, Hoffman TL, Wolf NI, Oegema R, van Binsbergen E, Baskin B, Bernard G, Fribourg S, Coulombe B, Yoon G. Am J Hum Genet 108 186-193 (2021)
  21. Structure of the TFIIIC subcomplex τA provides insights into RNA polymerase III pre-initiation complex formation. Vorländer MK, Jungblut A, Karius K, Baudin F, Grötsch H, Kosinski J, Müller CW. Nat Commun 11 4905 (2020)
  22. Truncated PARP1 mediates ADP-ribosylation of RNA polymerase III for apoptosis. Chen Q, Ma K, Liu X, Chen SH, Li P, Yu Y, Leung AKL, Yu X. Cell Discov 8 3 (2022)
  23. Molecular determinants underlying functional innovations of TBP and their impact on transcription initiation. Ravarani CNJ, Flock T, Chavali S, Anandapadamanaban M, Babu MM, Balaji S. Nat Commun 11 2384 (2020)
  24. Structural insights into RNA polymerase III-mediated transcription termination through trapping poly-deoxythymidine. Hou H, Li Y, Wang M, Liu A, Yu Z, Chen K, Zhao D, Xu Y. Nat Commun 12 6135 (2021)
  25. Brf1 loss and not overexpression disrupts tissues homeostasis in the intestine, liver and pancreas. Liko D, Mitchell L, Campbell KJ, Ridgway RA, Jones C, Dudek K, King A, Bryson S, Stevenson D, Blyth K, Strathdee D, Morton JP, Bird TG, Knight JRP, Willis AE, Sansom OJ. Cell Death Differ 26 2535-2550 (2019)
  26. Mechanism of RNA polymerase III termination-associated reinitiation-recycling conferred by the essential function of the N terminal-and-linker domain of the C11 subunit. Mishra S, Hasan SH, Sakhawala RM, Chaudhry S, Maraia RJ. Nat Commun 12 5900 (2021)
  27. An integrated model for termination of RNA polymerase III transcription. Xie J, Aiello U, Clement Y, Haidara N, Girbig M, Schmitzova J, Pena V, Müller CW, Libri D, Porrua O. Sci Adv 8 eabm9875 (2022)
  28. Functional characterization of Polr3a hypomyelinating leukodystrophy mutations in the S. cerevisiae homolog, RPC160. Moir RD, Lavados C, Lee J, Willis IM. Gene 768 145259 (2021)
  29. Bdp1 interacts with SNAPc bound to a U6, but not U1, snRNA gene promoter element to establish a stable protein-DNA complex. Verma N, Hurlburt AM, Wolfe A, Kim MK, Kang YS, Kang JJ, Stumph WE. FEBS Lett 592 2489-2498 (2018)
  30. Novel ribonucleotide discrimination in the RNA polymerase-like two-barrel catalytic core of Family D DNA polymerases. Zatopek KM, Alpaslan E, Evans TC, Sauguet L, Gardner AF. Nucleic Acids Res 48 12204-12218 (2020)
  31. Structural basis of Ty3 retrotransposon integration at RNA Polymerase III-transcribed genes. Abascal-Palacios G, Jochem L, Pla-Prats C, Beuron F, Vannini A. Nat Commun 12 6992 (2021)
  32. Structural basis of SNAPc-dependent snRNA transcription initiation by RNA polymerase II. Rengachari S, Schilbach S, Kaliyappan T, Gouge J, Zumer K, Schwarz J, Urlaub H, Dienemann C, Vannini A, Cramer P. Nat Struct Mol Biol 29 1159-1169 (2022)
  33. The hRPC62 subunit of human RNA polymerase III displays helicase activity. Ayoubi LE, Dumay-Odelot H, Chernev A, Boissier F, Minvielle-Sébastia L, Urlaub H, Fribourg S, Teichmann M. Nucleic Acids Res 47 10313-10326 (2019)
  34. Assembly of SNAPc, Bdp1, and TBP on the U6 snRNA Gene Promoter in Drosophila melanogaster. Kim MK, Tranvo A, Hurlburt AM, Verma N, Phan P, Luo J, Ranish J, Stumph WE. Mol Cell Biol 40 e00641-19 (2020)
  35. TFIIIB Subunit Bdp1 Participates in RNA Polymerase III Transcription in the Protozoan Parasite Leishmania major. Román-Carraro FC, Florencio-Martínez LE, Romero-Meza G, Nepomuceno-Mejía T, Carrero JC, Arroyo R, Ortega-López J, Manning-Cela RG, Martínez-Calvillo S. Biomed Res Int 2019 1425281 (2019)
  36. A structural perspective of human RNA polymerase III. Wang Q, Lei M, Wu J. RNA Biol 19 246-255 (2022)
  37. Modeling DNA Opening in the Eukaryotic Transcription Initiation Complexes via Coarse-Grained Models. Shino G, Takada S. Front Mol Biosci 8 772486 (2021)
  38. Participation of TFIIIB Subunit Brf1 in Transcription Regulation in the Human Pathogen Leishmania major. Florencio-Martínez LE, Cano-Santiago A, Mondragón-Rosas F, Gómez-García M, Flores-Pérez C, Román-Carraro FC, Barocio-Rodríguez LA, Manning-Cela RG, Nepomuceno-Mejía T, Martínez-Calvillo S. Genes (Basel) 12 280 (2021)
  39. Structural basis of TFIIIC-dependent RNA polymerase III transcription initiation. Talyzina A, Han Y, Banerjee C, Fishbain S, Reyes A, Vafabakhsh R, He Y. Mol Cell 83 2641-2652.e7 (2023)
  40. Structural basis of Ty1 integrase tethering to RNA polymerase III for targeted retrotransposon integration. Nguyen PQ, Huecas S, Asif-Laidin A, Plaza-Pegueroles A, Capuzzi B, Palmic N, Conesa C, Acker J, Reguera J, Lesage P, Fernández-Tornero C. Nat Commun 14 1729 (2023)
  41. The MAF1 Phosphoregulatory Region Controls MAF1 Interaction with the RNA Polymerase III C34 Subunit and Transcriptional Repression in Plants. Oliveira Andrade M, Sforça ML, Batista FAH, Figueira ACM, Benedetti CE. Plant Cell 32 3019-3035 (2020)
  42. Universal functions of the σ finger in alternative σ factors during transcription initiation by bacterial RNA polymerase. Oguienko A, Petushkov I, Pupov D, Esyunina D, Kulbachinskiy A. RNA Biol 18 2028-2037 (2021)
  43. DNA-dependent RNA polymerases in plants. Yang DL, Huang K, Deng D, Zeng Y, Wang Z, Zhang Y. Plant Cell 35 3641-3661 (2023)
  44. Evolution of the RNA Cleavage Subunit C11/RPC10, and Recycling by RNA Polymerase III. Mishra S, Maraia RJ. J Cell Immunol 4 65-71 (2022)
  45. Mutational and biophysical analyses reveal a TFIIIC binding region in the TFIIF-related Rpc53 subunit of RNA polymerase III. Shekhar AC, Wu WJ, Chen HT. J Biol Chem 299 104859 (2023)
  46. Site-directed biochemical analyses reveal that the switchable C-terminus of Rpc31 contributes to RNA polymerase III transcription initiation. Shekhar AC, Sun YE, Khoo SK, Lin YC, Malau EB, Chang WH, Chen HT. Nucleic Acids Res 51 4223-4236 (2023)
  47. Letter Structure of the SNAPc-bound RNA polymerase III preinitiation complex. Hou H, Jin Q, Ren Y, Chen Z, Wang Q, Xu Y. Cell Res 33 565-568 (2023)