Conformational flexibility of RNA polymerase III during transcriptional elongation

EMBO Journal

Volumn 29, Issue 22, 2010, Pages 3762-3772

  Fernández Tornero, Carlos ^a,b   Böttcher, Bettina ^a,c   Rashid, Umar Jan ^a   Steuerwald, Ulrich ^a   Flörchinger, Beate ^a   Devos, Damien P ^a   Lindner, Doris ^a   Müller, Christoph W ^a  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^b CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

electron cryomicroscopy; elongation complex; RNA polymerase III; transcription elongation; transcription initiation

Indexed keywords

DOUBLE STRANDED DNA; RNA POLYMERASE II;

ARTICLE; CONFORMATIONAL TRANSITION; CRYOELECTRON MICROSCOPY; DNA BINDING; DNA STRUCTURE; ENZYME STRUCTURE; MOLECULAR MODEL; PARTICLE SIZE; PRIORITY JOURNAL; RNA CONFORMATION; RNA TRANSCRIPTION; STRUCTURAL HOMOLOGY; TRANSCRIPTION INITIATION;

CRYOELECTRON MICROSCOPY; MODELS, MOLECULAR; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; RNA POLYMERASE III; SACCHAROMYCES CEREVISIAE; STRUCTURAL HOMOLOGY, PROTEIN; TRANSCRIPTION, GENETIC;

EID: 78449300336     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2010.266     Document Type: Article

References (54)

1. Andrau JC, Sentenac A, Werner M (1999) Mutagenesis of yeast TFIIIB70 reveals C-terminal residues critical for interaction with TBP and C34. J Mol Biol 288: 511-520
2. Andrecka J, Lewis R, Brückner F, Lehmann E, Cramer P, Michaelis J (2008) Single-molecule tracking of mRNA exiting from RNA polymerase II. Proc Natl Acad Sci USA 105: 135-140
3. Armache KJ, Mitterweger S, Meinhart A, Cramer P (2005) Structures of complete RNA polymerase II and its subcomplex, Rpb4/7. J Biol Chem 280: 7131-7134
4. Bartholomew B, Durkovich D, Kassavetis GA, Geiduschek EP (1993) Orientation and topography of RNA polymerase III in transcription complexes. Mol Cell Biol 13: 942-952
5. Bottcher B, Wynne SA, Crowther RA (1997) Determination of the fold of the core protein of hepatitis B virus by electron cryomicro-scopy. Nature 386: 88-91
6. 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
7. Carter R, Drouin G (2010) The increase in the number of subunits in eukaryotic RNA polymerase III relative to RNA polymerase II is due to the permanent recruitment of general transcription factors. Mol Biol Evol 27: 1035-1043
8. Chedin 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: 3857-3871
9. Chen HT, 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
10. Chen ZA, Jawhari A, Fischer L, Buchen C, Tahir S, Kamenski T, Rasmussen M, Lariviere L, Bukowski-Wills JC, Nilges M, Cramer P, Rappsilber J (2010) Architecture of the RNA polymerase II-TFIIF complex revealed by cross-linking and mass spectrometry. EMBO J 29: 717-726
11. Craighead JL, Chang WH, Asturias FJ (2002) Structure of yeast RNA polymerase II in solution: implications for enzyme regulation and interaction with promoter DNA. Structure 10 : 1117-1125
12. Cramer P, Armache KJ, Baumli S, Benkert S, Brueckner F, Buchen C, Damsma GE, Dengl S, Geiger SR, Jasiak AJ, Jawhari A, Jennebach S, Kamenski T, Kettenberger H, Kuhn CD, Lehmann E, Leike K, Sydow JF, Vannini A (2008) Structure of eukaryotic RNA poly-merases. Annu Rev Biophys 37: 337-352
13. Cramer P, Bushnell DA, Kornberg RD (2001) Structural basis of transcription: RNA polymerase II at 2.8 angstrom resolution. Science 292: 1863-1876
14. De Carlo S, Carles C, Riva M, Schultz P (2003) Cryo-negative staining reveals conformational flexibility within yeast RNA polymerase I. J Mol Biol 329: 891-902
15. Dieci G, Fiorino G, Castelnuovo M, Teichmann M, Pagano A (2007) The expanding RNA polymerase III transcriptome. Trends Genet 23: 614-622
16. Dieci G, Sentenac A (1996) Facilitated recycling pathway for RNA polymerase III. Cell 84: 245-252
17. 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: 706-716
18. Fernandez-Tornero C, Bottcher B, Riva M, Carles C, Steuerwald U, Ruigrok RW, Sentenac A, Muller CW, Schoehn G (2007) Insights into transcription initiation and termination from the electron microscopy structure of yeast RNA polymerase III. Mol Cell 25: 813-823
19. Ferri ML, Peyroche G, Siaut M, Lefebvre O, Carles C, Conesa C, Sentenac A (2000) A novel subunit of yeast RNA polymerase III interacts with the TFIIB-related domain of TFIIIB70. Mol Cell Biol 20: 488-495
20. Gaiser F, Tan S, Richmond TJ (2000) Novel dimerization fold of RAP30/RAP74 in human TFIIF at 1.7 A resolution. J Mol Biol 302: 1119-1127
21. Harpaz Y, Gerstein M, Chothia C (1994) Volume changes on protein folding. Structure 2: 641-649
22. Huet J, Manaud N, Dieci G, Peyroche G, Conesa C, Lefebvre O, Ruet A, Riva M, Sentenac A (1996) RNA polymerase III and class III transcription factors from Saccharomyces cerevisiae. Methods Enzymol 273: 249-267
23. Jasiak AJ, Armache KJ, Martens B, Jansen RP, Cramer P (2006) Structural biology of RNA polymerase III: subcomplex C17/25 X-ray structure and 11 subunit enzyme model. Mol Cell 23: 71-81
24. Jones DT (1999) Protein secondary structure prediction based on position-specific scoring matrices. J Mol Biol 292: 195-202
25. 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
26. Kassavetis GA, Blanco JA, Johnson TE, Geiduschek EP (1992) Formation of open and elongating transcription complexes by RNA polymerase III. J Mol Biol 226: 47-58
27. 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
28. Kettenberger H, Armache KJ, Cramer P (2004) Complete RNA polymerase II elongation complex structure and its interactions with NTP and TFIIS. Mol Cell 16: 955-965
29. Khoo B, Brophy B, Jackson SP (1994) Conserved functional domains of the RNA polymerase III general transcription factor BRF. Genes Dev 8: 2879-2890
30. Kitano K, Kim SY, Hakoshima T (2010) Structural basis for DNA strand separation by the unconventional winged-helix domain of RecQ helicase WRN. Structure 18: 177-187
31. Korkhin Y, Unligil UM, Littlefield O, Nelson PJ, Stuart DI, Sigler PB, Bell SD, Abrescia NG (2009) Evolution of complex RNA poly-merases: the complete archaeal RNA polymerase structure. PLoS Biol 7: e102
32. Kostrewa D, Zeller ME, Armache KJ, Seizl M, Leike K, Thomm M, Cramer P (2009) RNA polymerase II-TFIIB structure and mechanism of transcription initiation. Nature 462: 323-330
33. Kuhn CD, Geiger SR, Baumli S, Gartmann M, Gerber J, Jennebach S, Mielke T, Tschochner H, Beckmann R, Cramer P (2007) Functional architecture of RNA polymerase I. Cell 131: 1260-1272
34. 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
35. 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
36. Ludtke SJ, Baldwin PR, Chiu W (1999) EMAN: semiautomated software for high-resolution single-particle reconstructions. J Struct Biol 128: 82-97
37. Mindell JA, Grigorieff N (2003) Accurate determination of local defocus and specimen tilt in electron microscopy. J Struct Biol 142: 334-347
38. Mus E, Hof PR, Tiedge H (2007) Dendritic BC200 RNA in aging and in Alzheimer's disease. Proc Natl Acad Sci USA 104: 10679-10684
39. Nikolov DB, Chen H, Halay ED, Usheva AA, Hisatake K, Lee DK, Roeder RG, Burley SK (1995) Crystal structure of a TFIIB-TBP-TATA-element ternary complex. Nature 377: 119-128
40. 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
41. Pruzan R, Flint SJ (1995) Transcription of adenovirus RNA polymerase III genes. Curr Top Microbiol Immunol 199 (Pt 1): 201-226
42. Romier C, Ben Jelloul M, Albeck S, Buchwald G, Busso D, Celie PH, Christodoulou E, De Marco V, van Gerwen S, Knipscheer P, Lebbink JH, Notenboom V, Poterszman A, Rochel N, Cohen SX, Unger T, Sussman JL, Moras D, Sixma TK, Perrakis A (2006) Co-expression of protein complexes in prokar-yotic and eukaryotic hosts: experimental procedures, database tracking and case studies. Acta Crystallogr D Biol Crystallogr 62: 1232-1242
43. Rosenthal PB, Henderson R (2003) Optimal determination of particle orientation, absolute hand, and contrast loss in single-particle electron cryomicroscopy. J Mol Biol 333: 721-745
44. Sali A, Blundell TL (1993) Comparative protein modelling by satisfaction of spatial restraints. J Mol Biol 234: 779-815
45. Scheres SH, Nunez-Ramirez R, Sorzano CO, Carazo JM, Marabini R (2008) Image processing for electron microscopy single-particle analysis using XMIPP. Nat Protoc 3: 977-990
46. Shaikh TR, Gao H, Baxter WT, Asturias FJ, Boisset N, Leith A, Frank J (2008) SPIDER image processing for single-particle reconstruction of biological macromolecules from electron micrographs. Nat Protoc 3: 1941-1974
47. Soding J (2005) Protein homology detection by HMM-HMM comparison. Bioinformatics 21 : 951-960
48. Takada K (2001) Role of Epstein-Barr virus in Burkitt's lymphoma. Curr Top Microbiol Immunol 258: 141-151
49. Tate JJ, Persinger J, Bartholomew B (1998) Survey of four different photoreactive moieties for DNA photoaffinity labeling of yeast RNA polymerase III transcription complexes. Nucleic Acids Res 26: 1421-1426
50. Thuillier V, Stettler S, Sentenac A, Thuriaux P, Werner M (1995) A mutation in the C31 subunit of Saccharomyces cerevisiae RNA polymerase III affects transcription initiation. EMBO J 14: 351-359
51. Van Heel M, Harauz G, Orlova EV, Schmidt R, Schatz M (1996) A new generation of the IMAGIC image processing system. J Struct Biol 116: 17-24
52. Wang Z, Roeder RG (1997) Three human RNA polymerase III-specific subunits form a subcomplex with a selective function in specific transcription initiation. Genes Dev 11 : 1315-1326
53. Werner M, Hermann-Le Denmat S, Treich I, Sentenac A, Thuriaux P (1992) Effect of mutations in a zinc-binding domain of yeast RNA polymerase C (III) on enzyme function and subunit association. Mol Cell Biol 12: 1087-1095
54. Wriggers W (2010) Using Situs for the integration of multi-resolution structures. Biophys Rev 2: 21-27