RNA polymerase III subunit architecture and implications for open promoter complex formation

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 47, 2012, Pages 19232-19237

  Wu, Chih Chien ^a,b   Herzog, Franz ^c   Jennebach, Stefan ^d   Lin, Yu Chun ^a   Pai, Chih Yu ^a   Aebersold, Ruedi ^c,e   Cramer, Patrick ^d   Chen, Hung Ta ^a  

^a INSTITUTE OF MOLECULAR BIOLOGY   (Taiwan)

^b NATIONAL YANG MING UNIVERSITY   (Taiwan)

^c ETH ZURICH   (Switzerland)

^d UNIVERSITY OF MUNICH   (Germany)

^e UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; DNA DIRECTED RNA POLYMERASE III; HYDROXYL RADICAL;

ARTICLE; COMPLEX FORMATION; CROSS LINKING; DNA BINDING; ENZYME SUBUNIT; GENETIC TRANSCRIPTION; HUMAN; MASS SPECTROMETRY; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; TRANSCRIPTION INITIATION;

CATALYTIC DOMAIN; CROSS-LINKING REAGENTS; LIGHT; LYSINE; MODELS, MOLECULAR; NUCLEIC ACID CONFORMATION; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; PROTEIN INTERACTION MAPS; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS; PROTEIN TRANSPORT; RNA POLYMERASE III; SACCHAROMYCES CEREVISIAE; STRUCTURE-ACTIVITY RELATIONSHIP;

ARCHAEA; EUKARYOTA;

EID: 84869830300     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1211665109     Document Type: Article

References (43)

1. Cramer P, et al. (2008) Structure of eukaryotic RNA polymerases. Annu Rev Biophys 37:337-352.
2. Dieci G, Fiorino G, Castelnuovo M, Teichmann M, Pagano A (2007) The expanding RNA polymerase III transcriptome. Trends Genet 23(12):614-622.
3. Schramm L, Hernandez N (2002) Recruitment of RNA polymerase III to its target promoters. Genes Dev 16(20):2593-2620.
4. Bernard G, et al. (2011) Mutations of POLR3A encoding a catalytic subunit of RNA polymerase Pol III cause a recessive hypomyelinating leukodystrophy. Am J Hum Genet 89(3):415-423.
5. Tétreault M, et al. (2011) Recessive mutations in POLR3B, encoding the second largest subunit of Pol III, cause a rare hypomyelinating leukodystrophy. Am J Hum Genet 89(5):652-655.
6. Saitsu H, et al. (2011) Mutations in POLR3A and POLR3B encoding RNA Polymerase III subunits cause an autosomal-recessive hypomyelinating leukoencephalopathy. Am J Hum Genet 89(5):644-651.
7. 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(4):2695-2706.
8. Wu CC, Lin YC, Chen HT (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(13):2715-2728.
9. Landrieux E, et al. (2006) A subcomplex of RNA polymerase III subunits involved in transcription termination and reinitiation. EMBO J 25(1):118-128.
10. Werner M, Chaussivert N, Willis IM, Sentenac A (1993) Interaction between a complex of RNA polymerase III subunits and the 70-kDa component of transcription factor IIIB. J Biol Chem 268(28):20721-20724.
11. 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(10):1315-1326.
12. Brun I, Sentenac A, Werner M (1997) Dual role of the C34 subunit of RNA polymerase III in transcription initiation. EMBO J 16(18):5730-5741.
13. Bartholomew B, Durkovich D, Kassavetis GA, Geiduschek EP (1993) Orientation and topography of RNA polymerase III in transcription complexes. Mol Cell Biol 13(2):942-952.
14. 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(5):1035-1043.
15. Knutson BA, Hahn S (2011) Yeast Rrn7 and human TAF1B are TFIIB-related RNA polymerase I general transcription factors. Science 333(6049):1637-1640.
16. Naidu S, Friedrich JK, Russell J, Zomerdijk JC (2011) TAF1B is a TFIIB-like component of the basal transcription machinery for RNA polymerase I. Science 333(6049):1640-1642.
17. Werner F, Grohmann D (2011) Evolution of multisubunit RNA polymerases in the three domains of life. Nat Rev Microbiol 9(2):85-98.
18. Geiger SR, et al. (2010) RNA polymerase I contains a TFIIF-related DNA-binding subcomplex. Mol Cell 39(4):583-594.
19. Vannini A, Cramer P (2012) Conservation between the RNA polymerase I, II, and III transcription initiation machineries. Mol Cell 45(4):439-446.
20. Lefèvre S, et al. (2011) Structure-function analysis of hRPC62 provides insights into RNA polymerase III transcription initiation. Nat Struct Mol Biol 18(3):352-358.
21. Luo J, Fishburn J, Hahn S, Ranish J (2012) An integrated chemical cross-linking and mass spectrometry approach to study protein complex architecture and function. Mol Cell Proteomics 11(2):M111.008318.
22. Meinhart A, Blobel J, Cramer P (2003) An extended winged helix domain in general transcription factor E/IIE alpha. J Biol Chem 278(48):48267-48274.
23. Jennebach S, Herzog F, Aebersold R, Cramer P (2012) Crosslinking-MS analysis reveals RNA polymerase I domain architecture and basis of rRNA cleavage. Nucleic Acids Res 40(12):5591-5601.
24. Vannini A, et al. (2010) Molecular basis of RNA polymerase III transcription repression by Maf1. Cell 143(1):59-70.
25. Fernández-Tornero C, et al. (2010) Conformational flexibility of RNA polymerase III during transcriptional elongation. EMBO J 29(22):3762-3772.
26. Fernández-Tornero C, Böttcher B, Rashid UJ, Müller CW (2011) Analyzing RNA polymerase III by electron cryomicroscopy. RNA Biol 8(5):760-765.
27. 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(1):71-81.
28. Lane LA, et al. (2011) Mass spectrometry reveals stable modules in holo and apo RNA polymerases I and III. Structure 19(1):90-100.
29. Jennebach S (2011) RNA polymerase I domain architecture and basis of rRNA cleavage. PhD dissertation (Ludwig-Maximilians-Universität München, Munich).
30. Feklistov A, Darst SA (2011) Structural basis for promoter-10 element recognition by the bacterial RNA polymerase σ subunit. Cell 147(6):1257-1269.
31. Naji S, Bertero MG, Spitalny P, Cramer P, Thomm M (2008) Structure-function analysis of the RNA polymerase cleft loops elucidates initial transcription, DNA unwinding and RNA displacement. Nucleic Acids Res 36(2):676-687.
32. Cheung AC, Sainsbury S, Cramer P (2011) Structural basis of initial RNA polymerase II transcription. EMBO J 30(23):4755-4763.
33. 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(11):2823-2834.
34. 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(8):696-703.
35. 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(8):788-796.
36. Grohmann 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(2):263-274.
37. Kostrewa D, et al. (2009) RNA polymerase II-TFIIB structure and mechanism of transcription initiation. Nature 462(7271):323-330.
38. Kassavetis GA, Han S, Naji S, Geiduschek EP (2003) The role of transcription initiation factor IIIB subunits in promoter opening probed by photochemical cross-linking. J Biol Chem 278(20):17912-17917.
39. 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(5962):206-209.
40. Khoo B, Brophy B, Jackson SP (1994) Conserved functional domains of the RNA polymerase III general transcription factor BRF. Genes Dev 8(23):2879-2890.
41. Artsimovitch I, et al. (2005) Allosteric modulation of the RNA polymerase catalytic reaction is an essential component of transcription control by rifamycins. Cell 122(3):351-363.
42. Eswar N, Eramian D, Webb B, Shen MY, Sali A (2008) Protein structure modeling with MODELLER. Methods Mol Biol 426:145-159.
43. Juo ZS, Kassavetis GA, Wang J, Geiduschek EP, Sigler PB (2003) Crystal structure of a transcription factor IIIB core interface ternary complex. Nature 422(6931):534-539.