Structure of the τ60/Δτ91 Subcomplex of Yeast Transcription Factor IIIC: Insights into Preinitiation Complex Assembly

Molecular Cell

Volumn 24, Issue 2, 2006, Pages 221-232

  Mylona, Anastasia ^a   Fernández Tornero, Carlos ^a   Legrand, Pierre ^a   Haupt, Melina ^a   Sentenac, André ^b   Acker, Joël ^b   Müller, Christoph W ^a  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY   (France)

^b CEA SACLAY   (France)

Author keywords

DNA

Indexed keywords

TATA BINDING PROTEIN; RECOMBINANT PROTEIN; TRANSCRIPTION FACTOR III; TRANSCRIPTION FACTOR TFIIIC;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CRYSTAL STRUCTURE; GENE STRUCTURE; GENETIC TRANSCRIPTION; NONHUMAN; PROMOTER REGION; SEQUENCE HOMOLOGY; YEAST; AMINO ACID SEQUENCE; CHEMICAL STRUCTURE; CHEMISTRY; DIMERIZATION; HUMAN; MOLECULAR GENETICS; PHYSIOLOGY; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; X RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; CRYSTALLOGRAPHY, X-RAY; DIMERIZATION; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; TRANSCRIPTION FACTORS, TFIII; TRANSCRIPTION, GENETIC;

EID: 33750087881     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2006.08.013     Document Type: Article

References (57)

1. Andrade M.A., Perez-Iratxeta C., and Ponting C.P. Protein repeats: structures, functions, and evolution. J. Struct. Biol. 134 (2001) 117-131
2. Arrebola R., Manaud N., Rozenfeld S., Marsolier M.C., Lefebvre O., Carles C., Thuriaux P., Conesa C., and Sentenac A. Tau91, an essential subunit of yeast transcription factor IIIC, cooperates with tau138 in DNA binding. Mol. Cell. Biol. 18 (1998) 1-9
3. Bartholomew B., Kassavetis G.A., Braun B.R., and Geiduschek E.P. The subunit structure of Saccharomyces cerevisiae transcription factor IIIC probed with a novel photocrosslinking reagent. EMBO J. 9 (1990) 2197-2205
4. Bartholomew B., Kassavetis G.A., and Geiduschek E.P. Two components of Saccharomyces cerevisiae transcription factor IIIB (TFIIIB) are stereospecifically located upstream of a tRNA gene and interact with the second-largest subunit of TFIIIC. Mol. Cell. Biol. 11 (1991) 5181-5189
5. Bateman A., Coin L., Durbin R., Finn R.D., Hollich V., Griffiths-Jones S., Khanna A., Marshall M., Moxon S., Sonnhammer E.L., et al. The Pfam protein families database. Nucleic Acids Res. 32 (2004) D138-D141
6. Braun B.R., Bartholomew B., Kassavetis G.A., and Geiduschek E.P. Topography of transcription factor complexes on the Saccharomyces cerevisiae 5 S RNA gene. J. Mol. Biol. 228 (1992) 1063-1077
7. Brünger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., Jiang J.S., Kuszewski J., Nilges M., Pannu N.S., et al. Crystallography and NMR system: a new software for macromolecular structure determination. Acta Crystallogr. C 54 (1998) 905-921
8. Burnol A.F., Margottin F., Huet J., Almouzni G., Prioleau M.N., Mechali M., and Sentenac A. TFIIIC relieves repression of U6 snRNA transcription by chromatin. Nature 362 (1993) 475-477
9. CCP4 (Collaborative Computational Project, Number 4). The CCP4 suite: programs for protein crystallography. Acta. Crystallogr. D. Biol. Crystallogr. 50 (1994) 760-776
10. Chaussivert N., Conesa C., Shaaban S., and Sentenac A. Complex interactions between yeast TFIIIB and TFIIIC. J. Biol. Chem. 270 (1995) 15353-15358
11. Chedin S., Ferri M.L., Peyroche G., Andrau J.C., Jourdain S., Lefebvre O., Werner M., Carles C., and Sentenac A. The yeast RNA polymerase III transcription machinery: a paradigm for eukaryotic gene activation. Cold Spring Harb. Symp. Quant. Biol. 63 (1998) 381-389
12. Conesa C., Swanson R.N., Schultz P., Oudet P., and Sentenac A. On the subunit composition, stoichiometry, and phosphorylation of the yeast transcription factor TFIIIC/tau. J. Biol. Chem. 268 (1993) 18047-18052
13. Cozzarelli N.R., Gerrard S.P., Schlissel M., Brown D.D., and Bogenhagen D.F. Purified RNA polymerase III accurately and efficiently terminates transcription of 5S RNA genes. Cell 34 (1983) 829-835
14. DeLano W.L. The PyMOL molecular graphics system (2002). http://www.pymol.org
15. Deprez E., Arrebola R., Conesa C., and Sentenac A. A subunit of yeast TFIIIC participates in the recruitment of TATA-binding protein. Mol. Cell. Biol. 19 (1999) 8042-8051
16. Dieci G., Percudani R., Giuliodori S., Bottarelli L., and Ottonello S. TFIIIC-independent in vitro transcription of yeast tRNA genes. J. Mol. Biol. 299 (2000) 601-613
17. Ducrot C., Lefebvre O., Landrieux E., Guirouilh-Barbat J., Sentenac A., and Acker J. Reconstitution of the yeast RNA polymerase III transcription system with all recombinant factors. J. Biol. Chem. 281 (2006) 11685-11692
18. de la Fortelle E., and Bricogne G. Maximum-likelihood heavy-atom parameter refinement for the multiple isomorphous replacement and multiwavelength anomalous diffraction methods. Methods Enzymol. 276 (1997) 472-494
19. Gabrielsen O.S., and Oyen T.B. The requirement for the A block promoter element in tRNA gene transcription in vitro depends on the ionic environment. Nucleic Acids Res. 15 (1987) 5699-5713
20. Gabrielsen O.S., Marzouki N., Ruet A., Sentenac A., and Fromageot P. Two polypeptide chains in yeast transcription factor tau interact with DNA. J. Biol. Chem. 264 (1989) 7505-7511
21. Geiduschek E.P., and Kassavetis G.A. The RNA polymerase III transcription apparatus. J. Mol. Biol. 310 (2001) 1-26
22. Grant P.A., Duggan L., Cote J., Roberts S.M., Brownell J.E., Candau R., Ohba R., Owen-Hughes T., Allis C.D., Winston F., et al. Yeast Gcn5 functions in two multisubunit complexes to acetylate nucleosomal histones: characterization of an Ada complex and the SAGA (Spt/Ada) complex. Genes Dev. 11 (1997) 1640-1650
23. Holm L., and Sander C. Dali: a network tool for protein structure comparison. Trends Biochem. Sci. 20 (1995) 478-480
24. Hsieh Y.J., Kundu T.K., Wang Z., Kovelman R., and Roeder R.G. The TFIIIC90 subunit of TFIIIC interacts with multiple components of the RNA polymerase III machinery and contains a histone-specific acetyltransferase activity. Mol. Cell. Biol. 19 (1999) 7697-7704
25. Huang Y., and Maraia R.J. Comparison of the RNA polymerase III transcription machinery in Schizosaccharomyces pombe, Saccharomyces cerevisiae and human. Nucleic Acids Res. 29 (2001) 2675-2690
26. Huang Y., Hamada M., and Maraia R.J. Isolation and cloning of four subunits of a fission yeast TFIIIC complex that includes an ortholog of the human regulatory protein TFIIICbeta. J. Biol. Chem. 275 (2000) 31480-31487
27. Jawad Z., and Paoli M. Novel sequences propel familiar folds. Structure 10 (2002) 447-454
28. Joazeiro C.A., Kassavetis G.A., and Geiduschek E.P. Alternative outcomes in assembly of promoter complexes: the roles of TBP and a flexible linker in placing TFIIIB on tRNA genes. Genes Dev. 10 (1996) 725-739
29. Jones T.A., Zhou J.Y., Cowan S.W., and Kjeldgaard M. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A47 (1991) 110-119
30. Kassavetis G.A., Braun B.R., Nguyen L.H., and Geiduschek E.P. S. cerevisiae TFIIIB is the transcription initiation factor proper of RNA polymerase III, while TFIIIA and TFIIIC are assembly factors. Cell 60 (1990) 235-245
31. Kassavetis G.A., Joazeiro C.A., Pisano M., Geiduschek E.P., Colbert T., Hahn S., and Blanco J.A. The role of the TATA-binding protein in the assembly and function of the multisubunit yeast RNA polymerase III transcription factor, TFIIIB. Cell 71 (1992) 1055-1064
32. Kundu T.K., Wang Z., and Roeder R.G. Human TFIIIC relieves chromatin-mediated repression of RNA polymerase III transcription and contains an intrinsic histone acetyltransferase activity. Mol. Cell. Biol. 19 (1999) 1605-1615
33. Lefebvre O., Ruth J., and Sentenac A. A mutation in the largest subunit of yeast TFIIIC affects tRNA and 5 S RNA synthesis. Identification of two classes of suppressors. J. Biol. Chem. 269 (1994) 23374-23381
34. Manaud N., Arrebola R., Buffin-Meyer B., Lefebvre O., Voss H., Riva M., Conesa C., and Sentenac A. A chimeric subunit of yeast transcription factor IIIC forms a subcomplex with tau95. Mol. Cell. Biol. 18 (1998) 3191-3200
35. Marck C., Lefebvre O., Carles C., Riva M., Chaussivert N., Ruet A., and Sentenac A. The TFIIIB-assembling subunit of yeast transcription factor TFIIIC has both tetratricopeptide repeats and basic helix-loop-helix motifs. Proc. Natl. Acad. Sci. USA 90 (1993) 4027-4031
36. Margottin F., Dujardin G., Gerard M., Egly J.M., Huet J., and Sentenac A. Participation of the TATA factor in transcription of the yeast U6 gene by RNA polymerase C. Science 251 (1991) 424-426
37. Marzouki N., Camier S., Ruet A., Moenne A., and Sentenac A. Selective proteolysis defines two DNA binding domains in yeast transcription factor tau. Nature 323 (1986) 176-178
38. Miller T., Krogan N.J., Dover J., Erdjument-Bromage H., Tempst P., Johnston M., Greenblatt J.F., and Shilatifard A. COMPASS: a complex of proteins associated with a trithorax-related SET domain protein. Proc. Natl. Acad. Sci. USA 98 (2001) 12902-12907
39. Mylona A., Acker J., Fernandez-Tornero C., Sentenac A., and Muller C.W. Expression, proteolytic analysis, reconstitution, and crystallization of the tau60/tau91 subcomplex of yeast TFIIIC. Protein Expr. Purif. 45 (2006) 255-261
40. Nekrasov M., Wild B., and Muller J. Nucleosome binding and histone methyltransferase activity of Drosophila PRC2. EMBO Rep. 6 (2005) 348-353
41. Nicholls A., Bharadwaj R., and Honig B. GRASP - graphical representation and analysis of surface properties. Biophys. J. 64 (1993) A166
42. Noma K., Cam H.P., Maraia R.J., and Grewal S.I. A role for TFIIIC transcription factor complex in genome organization. Cell 125 (2006) 859-872
43. Rameau G., Puglia K., Crowe A., Sethy I., and Willis I. A mutation in the second largest subunit of TFIIIC increases a rate-limiting step in transcription by RNA polymerase III. Mol. Cell. Biol. 14 (1994) 822-830
44. Robinson R.C., Turbedsky K., Kaiser D.A., Marchand J.B., Higgs H.N., Choe S., and Pollard T.D. Crystal structure of Arp2/3 complex. Science 294 (2001) 1679-1684
45. Roussel A., and Cambillau C.T.-F. TURBO-Frodo. Silicon Graphics Geometry Partners Directory (1989), Silicon Graphics, Mountain View, CA 77-79
46. Rozenfeld S., and Thuriaux P. Genetic interactions within TFIIIC, the promoter-binding factor of yeast RNA polymerase III. Mol. Genet. Genomics 265 (2001) 705-710
47. Rudenko G., Henry L., Henderson K., Ichtchenko K., Brown M.S., Goldstein J.L., and Deisenhofer J. Structure of the LDL receptor extracellular domain at endosomal pH. Science 298 (2002) 2353-2358
48. Schneider T.R., and Sheldrick G.M. Substructure solution with SHELXD. Acta Crystallogr. D Biol. Crystallogr. 58 (2002) 1772-1779
49. Schramm L., and Hernandez N. Recruitment of RNA polymerase III to its target promoters. Genes Dev. 16 (2002) 2593-2620
50. Schultz J., Milpetz F., Bork P., and Ponting C.P. SMART, a simple modular architecture research tool: identification of signaling domains. Proc. Natl. Acad. Sci. USA 95 (1998) 5857-5864
51. Schultz P., Marzouki N., Marck C., Ruet A., Oudet P., and Sentenac A. The two DNA-binding domains of yeast transcription factor tau as observed by scanning transmission electron microscopy. EMBO J. 8 (1989) 3815-3824
52. Shindyalov I.N., and Bourne P.E. Protein structure alignment by incremental combinatorial extension (CE) of the optimal path. Protein Eng. 11 (1998) 739-747
53. Shivaswamy S., Kassavetis G.A., and Bhargava P. High-level activation of transcription of the yeast U6 snRNA gene in chromatin by the basal RNA polymerase III transcription factor TFIIIC. Mol. Cell. Biol. 24 (2004) 3596-3606
54. Sinn E., Wang Z., Kovelman R., and Roeder R.G. Cloning and characterization of a TFIIIC2 subunit (TFIIIC beta) whose presence correlates with activation of RNA polymerase III-mediated transcription by adenovirus E1A expression and serum factors. Genes Dev. 9 (1995) 675-685
55. Sprague E.R., Redd M.J., Johnson A.D., and Wolberger C. Structure of the C-terminal domain of Tup1, a corepressor of transcription in yeast. EMBO J. 19 (2000) 3016-3027
56. Weirich C.S., Erzberger J.P., Berger J.M., and Weis K. The N-terminal domain of Nup159 forms a beta-propeller that functions in mRNA export by tethering the helicase Dbp5 to the nuclear pore. Mol. Cell 16 (2004) 749-760
57. Wysocka J., Swigut T., Milne T.A., Dou Y., Zhang X., Burlingame A.L., Roeder R.G., Brivanlou A.H., and Allis C.D. WDR5 associates with histone H3 methylated at K4 and is essential for H3 K4 methylation and vertebrate development. Cell 121 (2005) 859-872