RNA polymerase III-specific general transcription factor IIIC contains a heterodimer resembling TFIIF Rap30/Rap74

Nucleic Acids Research

Volumn 41, Issue 19, 2013, Pages 9183-9196

  Taylor, Nicholas M I ^a   Baudin, Florence ^a,b   Von Scheven, Gudrun ^a   Müller, Christoph W ^a  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

DNA DIRECTED RNA POLYMERASE III; DOUBLE STRANDED DNA; SINGLE STRANDED DNA; TRANSCRIPTION FACTOR II; TRANSCRIPTION FACTOR IIF; TRANSCRIPTION FACTOR III; TRANSCRIPTION FACTOR IIIC; UNCLASSIFIED DRUG;

AFFINITY CHROMATOGRAPHY; AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DIMERIZATION; DNA BINDING; EXPRESSION VECTOR; FUNGAL STRAIN; ISOTHERMAL TITRATION CALORIMETRY; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SACCHAROMYCES CEREVISIAE; SCHIZOSACCHAROMYCES POMBE; SEQUENCE HOMOLOGY; TRANSCRIPTION INITIATION SITE;

AMINO ACID SEQUENCE; DNA; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; SCHIZOSACCHAROMYCES POMBE PROTEINS; TRANSCRIPTION FACTORS; TRANSCRIPTION FACTORS, TFII; TRANSCRIPTION FACTORS, TFIII;

EID: 84885990149     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt664     Document Type: Article

References (59)

1. Schramm, L. and Hernandez, N. (2002) Recruitment of RNA polymerase III to its target promoters. Genes Dev., 16, 2593-2620.
2. Marck, C., Kachouri-Lafond, R., Lafontaine, I., Westhof, E., Dujon, B. and Grosjean, H. (2006) The RNA polymerase III-dependent family of genes in hemiascomycetes: comparative RNomics, decoding strategies, transcription and evolutionary implications. Nucleic Acids Res., 34, 1816-1835.
3. Stillman, D.J. and Geiduschek, E.P. (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.
4. Iwasaki, O. and Noma, K.I. (2012) Global genome organization mediated by RNA polymerase III-transcribed genes in fission yeast. Gene, 493, 195-200.
5. Schultz, P., Marzouki, N., Marck, C., Ruet, A., Oudet, P. and Sentenac, A. (1989) The two DNA-binding domains of yeast transcription factor tau as observed by scanning transmission electron microscopy. EMBO J., 8, 3815-3824.
6. Huang, Y. and Maraia, R.J. (2001) Comparison of the RNA polymerase III transcription machinery in Schizosaccharomyces pombe, Saccharomyces cerevisiae and human. Nucleic Acids Res., 29, 2675-2690.
7. Ducrot, C., Lefebvre, O., Landrieux, E., Guirouilh-Barbat, J., Sentenac, A. and Acker, J. (2006) Reconstitution of the yeast RNA polymerase III transcription system with all recombinant factors. J. Biol. Chem., 281, 11685-11692.
8. Bartholomew, B., Kassavetis, G.A., Braun, B.R. and Geiduschek, E.P. (1990) The subunit structure of Saccharomyces cerevisiae transcription factor IIIC probed with a novel photocrosslinking reagent. EMBO J., 9, 2197-2205.
9. Manaud, N., Arrebola, R., Buffin-Meyer, B., Lefebvre, O., Voss, H., Riva, M., Conesa, C. and Sentenac, A. (1998) A chimeric subunit of yeast transcription factor IIIC forms a subcomplex with tau95. Mol. Cell. Biol., 18, 3191-3200.
10. Dumay-Odelot, H., Marck, C., Durrieu-Gaillard, S., Lefebvre, O., Jourdain, S., Prochazkova, M., Pflieger, A. and Teichmann, M. (2007) Identification, molecular cloning, and characterization of the sixth subunit of human transcription factor TFIIIC. J. Biol. Chem., 282, 17179-17189.
11. Taylor, N.M., Glatt, S., Hennrich, M.L., von Scheven, G., Grotsch, H., Fernandez-Tornero, C., Rybin, V., Gavin, A.C., Kolb, P. and Muller, C.W. (2013) Structural and functional characterization of a phosphatase domain within yeast general transcription factor IIIC. J. Biol. Chem., 288, 15110-15120.
12. Mylona, A., Fernández-Tornero, C., Legrand, P., Haupt, M., Sentenac, A., Acker, J. and Müller, C.W. (2006) Structure of the tau60/Delta tau91 subcomplex of yeast transcription factor IIIC: insights into preinitiation complex assembly. Mol. Cell, 24, 221-232.
13. Hubbard, S.J. (1998) The structural aspects of limited proteolysis of native proteins. Biochim. Biophys. Acta, 1382, 191-206.
14. Kabsch, W. (2010) XDS. Acta Crystallogr. D, 66, 125-132.
15. Evans, P. (2006) Scaling and assessment of data quality. Acta Crystallogr. D, 62, 72-82.
16. Sheldrick, G.M. (2008) A short history of SHELX. Acta Crystallogr. A, 64, 112-122.
17. Pape, T. and Schneider, T. (2004) HKL2MAP: a graphical user interface for macromolecular phasing with SHELX programs. J. Appl. Crystallogr., 37, 843-844.
18. Vonrhein, C., Blanc, E., Roversi, P. and Bricogne, G. (2007) Automated structure solution with autoSHARP. Methods Mol. Biol., 364, 215-230.
19. Abrahams, J.P. and Leslie, A.G.W. (1996) Methods used in the structure determination of bovine mitochondrial F1 ATPase. Acta Crystallogr. D, 52, 30-42.
20. Perrakis, A., Harkiolaki, M., Wilson, K.S. and Lamzin, V.S. (2001) ARP/wARP and molecular replacement. Acta Crystallogr. D, 57, 1445-1450.
21. Emsley, P., Lohkamp, B., Scott, W.G. and Cowtan, K. (2010) Features and development of Coot. Acta Crystallogr. D, 66, 486-501.
22. Adams, P.D., Afonine, P.V., Bunkóczi, G., Chen, V.B., Davis, I.W., Echols, N., Headd, J.J., Hung, L.W., Kapral, G.J., Grosse-Kunstleve, R.W. et al. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D, 66, 213-221.
23. Chen, V.B., Arendall, W.B., Headd, J.J., Keedy, D.A., Immormino, R.M., Kapral, G.J., Murray, L.W., Richardson, J.S. and Richardson, D.C. (2010) MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D, 66, 12-21.
24. Doublie, S. (2007) Production of selenomethionyl proteins in prokaryotic and eukaryotic expression systems. Methods Mol. Biol., 363, 91-108.
25. Baudin, F., Bach, C., Cusack, S. and Ruigrok, R.W. (1994) Structure of influenza virus RNP.I. Influenza virus nucleoprotein melts secondary structure in panhandle RNA and exposes the bases to the solvent. EMBO J., 13, 3158-3165.
26. Goldschmidt, L., Cooper, D.R., Derewenda, Z.S. and Eisenberg, D. (2007) Toward rational protein crystallization: A Web server for the design of crystallizable protein variants. Protein Sci., 16, 1569-1576.
27. Holm, L. and Rosenström, P. (2010) Dali server: conservation mapping in 3D. Nucleic Acids Res., 38, W545-549.
28. Gaiser, F., Tan, S. and Richmond, T.J. (2000) Novel dimerization fold of RAP30/RAP74 in human TFIIF at 1.7 A resolution. J. Mol. Biol., 302, 1119-1127.
29. Groft, C.M., Uljon, S.N., Wang, R. and Werner, M.H. (1998) Structural homology between the Rap30 DNA-binding domain and linker histone H5: implications for preinitiation complex assembly. Proc. Natl Acad. Sci. USA, 95, 9117-9122.
30. Baker, R.E., Gabrielsen, O. and Hall, B.D. (1986) Effects of tRNATyr point mutations on the binding of yeast RNA polymerase III transcription factor C. J. Biol. Chem., 261, 5275-5282.
31. Stillman, D.J., Caspers, P. and Geiduschek, E.P. (1985) Effects of temperature and single-stranded DNA on the interaction of an RNA polymerase III transcription factor with a tRNA gene. Cell, 40, 311-317.
32. Tan, S., Garrett, K.P., Conaway, R.C. and Conaway, J.W. (1994) Cryptic DNA-binding domain in the C terminus of RNA polymerase II general transcription factor RAP30. Proc. Natl Acad. Sci. USA, 91, 9808-9812.
33. Huet, J., Conesa, C., Carles, C. and Sentenac, A. (1997) A cryptic DNA binding domain at the COOH terminus of TFIIIB70 affects formation, stability, and function of preinitiation complexes. J. Biol. Chem., 272, 18341-18349.
34. Aye, M., Dildine, S.L., Claypool, J.A., Jourdain, S. and Sandmeyer, S.B. (2001) A truncation mutant of the 95-kilodalton subunit of transcription factor IIIC reveals asymmetry in Ty3 integration. Mol. Cell. Biol., 21, 7839-7851.
35. Jourdain, S., Acker, J., Ducrot, C., Sentenac, A. and Lefebvre, O. (2003) The tau95 subunit of yeast TFIIIC influences upstream and downstream functions of TFIIIC.DNA complexes. J. Biol. Chem., 278, 10450-10457.
36. Gajiwala, K.S. and Burley, S.K. (2000) Winged helix proteins. Curr. Opin. Struct. Biol., 10, 110-116.
37. Feklistov, A. and Darst, S.A. (2011) Structural basis for promoter- 10 element recognition by the bacterial RNA polymerase sigma subunit. Cell, 147, 1257-1269.
38. Henry, N.L., Campbell, A.M., Feaver, W.J., Poon, D., Weil, P.A. and Kornberg, R.D. (1994) TFIIF-TAF-RNA polymerase II connection. Genes Dev., 8, 2868-2878.
39. Tan, S., Conaway, R.C. and Conaway, J.W. (1995) Dissection of transcription factor TFIIF functional domains required for initiation and elongation. Proc. Natl Acad. Sci. USA, 92, 6042-6046.
40. Cabart, P., Ujvari, A., Pal, M. and Luse, D.S. (2012) 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. Proc. Natl Acad. Sci. USA, 108, 15786-15791.
41. Fishburn, J. and Hahn, S. (2012) Architecture of the yeast RNA polymerase II open complex and regulation of activity by TFIIF. Mol. Cell. Biol., 32, 12-25.
42. Wang, B.Q. and Burton, Z.F. (1995) Functional domains of human RAP74 including a masked polymerase binding domain. J. Biol. Chem., 270, 27035-27044.
43. Yan, Q., Moreland, R.J., Conaway, J.W. and Conaway, R.C. (1999) Dual roles for transcription factor IIF in promoter escape by RNA polymerase II. J. Biol. Chem., 274, 35668-35675.
44. Chen, H.T., Warfield, L. and Hahn, S. (2007) The positions of TFIIF and TFIIE in the RNA polymerase II transcription preinitiation complex. Nat. Struct. Mol. Biol., 14, 696-703.
45. Freire-Picos, M.A., Krishnamurthy, S., Sun, Z.W. and Hampsey, M. (2005) Evidence that the Tfg1/Tfg2 dimer interface of TFIIF lies near the active center of the RNA polymerase II initiation complex. Nucleic Acids Res., 33, 5045-5052.
46. Kamada, K., De Angelis, J., Roeder, R.G. and Burley, S.K. (2001) Crystal structure of the C-terminal domain of the RAP74 subunit of human transcription factor IIF. Proc. Natl Acad. Sci. USA, 98, 3115-3120.
47. Vannini, A. and Cramer, P. (2012) Conservation between the RNA polymerase I, II, and III transcription initiation machineries. Mol. Cell, 45, 439-446.
48. Carter, R. and 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.
49. Chen, Z.A., Jawhari, A., Fischer, L., Buchen, C., Tahir, S., Kamenski, T., Rasmussen, M., Lariviere, L., Bukowski-Wills, J.C., Nilges, M. et al. (2010) Architecture of the RNA polymerase IITFIIF complex revealed by cross-linking and mass spectrometry. EMBO J., 29, 717-726.
50. Eichner, J., Chen, H.T., Warfield, L. and Hahn, S. (2010) Position of the general transcription factor TFIIF within the RNA polymerase II transcription preinitiation complex. EMBO J., 29, 706-716.
51. Fernández-Tornero, C., Böttcher, B., Rashid, U.J., Steuerwald, U., Flörchinger, B., Devos, D.P., Lindner, D. and Müller, C.W. (2010) Conformational flexibility of RNA polymerase III during transcriptional elongation. EMBO J., 29, 3762-3772.
52. Kuhn, C., Geiger, S.R., Baumli, S., Gartmann, M., Gerber, J., Jennebach, S., Mielke, T., Tschochner, H., Beckmann, R. and Cramer, P. (2007) Functional architecture of RNA polymerase I. Cell, 131, 1260-1272.
53. Söding, J., Biegert, A. and Lupas, A.N. (2005) The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res., 33, W244-W248.
54. He, Y., Fang, J., Taatjes, D.J. and Nogales, E. (2013) Structural visualization of key steps in human transcription initiation. Nature, 495, 481-486.
55. Landrieux, E., Alic, N., Ducrot, C., Acker, J., Riva, M. and Carles, C. (2006) A subcomplex of RNA polymerase III subunits involved in transcription termination and reinitiation. EMBO J., 25, 118-128.
56. Kassavetis, G.A., Prakash, P. and 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.
57. Wu, C.C., Lin, Y.C. and 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.
58. Rosonina, E., Willis, I.M. and Manley, J.L. (2009) Sub1 functions in osmoregulation and in transcription by both RNA polymerases II and III. Mol. Cell. Biol., 29, 2308-2321.
59. Tavenet, A., Suleau, A., Dubreuil, G., Ferrari, R., Ducrot, C., Michaut, M., Aude, J.C., Dieci, G., Lefebvre, O., Conesa, C. et al. (2009) Genome-wide location analysis reveals a role for Sub1 in RNA polymerase III transcription. Proc. Natl Acad. Sci. USA, 106, 14265-14270.