The structure of an Iws1/Spt6 complex reveals an interaction domain conserved in TFIIS, Elongin A and Med26

EMBO Journal

Volumn 29, Issue 23, 2010, Pages 3979-3991

  Diebold, Marie Laure ^a   Koch, Michael ^b   Loeliger, Erin ^c   Cura, Vincent ^a   Winston, Fred ^c   Cavarelli, Jean ^a   Romier, Christophe ^a  

^a INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^b UNIVERSITY OF COLOGNE   (Germany)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

crystallography; mRNA export; RNA polymerase II; transcription elongation; yeast genetics

Indexed keywords

ELONGATION FACTOR; ELONGATION FACTOR SPT6; ELONGIN A; FUNGAL PROTEIN; PROTEIN IWS1; PROTEIN MED13; PROTEIN MED26; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR IIS; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; COMPLEX FORMATION; CRYSTAL STRUCTURE; ENCEPHALITOZOON CUNICULI; FUNGUS MUTATION; MESSENGER RNA SYNTHESIS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; SACCHAROMYCES CEREVISIAE; YEAST;

ENCEPHALITOZOON CUNICULI; EUKARYOTA;

EID: 78649717707     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2010.272     Document Type: Article

References (41)

1. Adkins MW, Tyler JK (2006) Transcriptional activators are dispensable for transcription in the absence of Spt6-mediated chromatin reassembly of promoter regions. Mol Cell 21: 405-416
2. Andrade MA, Petosa C, O'Donoghue SI, Muller CW, Bork P (2001) Comparison of ARM and HEAT protein repeats. J Mol Biol 309: 1-18
3. Ardehali MB, Yao J, Adelman K, Fuda NJ, Petesch SJ, Webb WW, Lis JT (2009) Spt6 enhances the elongation rate of RNA polymerase II in vivo. EMBO J 28: 1067-1077
4. 0-phosphate decarboxylase activity in yeast: 5-fluoro-orotic acid resistance. Mol Gen Genet 197: 345-346
5. Bond CS, Schuttelkopf AW (2009) ALINE: a WYSIWYG protein-sequence alignment editor for publication-quality alignments. Acta Crystallogr D Biol Crystallogr 65(Part 5): 510-512
6. Booth V, Koth CM, Edwards AM, Arrowsmith CH (2000) Structure of a conserved domain common to the transcription factors TFIIS, elongin A, and CRSP70. J Biol Chem 275: 31266-31268
7. Bortvin A, Winston F (1996) Evidence that Spt6p controls chromatin structure by a direct interaction with histones. Science 272: 1473-1476
8. CCP4 (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 50(Part 5): 760-763
9. Diebold ML, Loeliger E, Koch M, Winston F, Cavarelli J, Romier C (2010) A non-canonical tandem SH2 enables interaction of elongation factor SPT6 with RNA polymerase II. J Biol Chem (doi:10.1074/jbc.M110.146696)
10. Emsley P, Cowtan K (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60 (Part 12 Part 1): 2126-2132
11. Endoh M, Zhu W, Hasegawa J, Watanabe H, Kim DK, Aida M, Inukai N, Narita T, Yamada T, Furuya A, Sato H, Yamaguchi Y, Mandal SS, Reinberg D, Wada T, Handa H (2004) Human Spt6 stimulates transcription elongation by RNA polymerase II in vitro. Mol Cell Biol 24: 3324-3336
12. Fischbeck JA, Kraemer SM, Stargell LA (2002) SPN1, a conserved gene identified by suppression of a postrecruitment-defective yeast TATA-binding protein mutant. Genetics 162: 1605-1616
13. Guglielmi B, Soutourina J, Esnault C, Werner M (2007) TFIIS elongation factor and Mediator act in conjunction during transcription initiation in vivo. Proc Natl Acad Sci USA 104: 16062-16067
14. Johnson SJ, Close D, Robinson H, Vallet-Gely I, Dove SL, Hill CP (2008) Crystal structure and RNA binding of the Tex protein from Pseudomonas aeruginosa. J Mol Biol 377: 1460-1473
15. Kaplan CD, Laprade L, Winston F (2003) Transcription elongation factors repress transcription initiation from cryptic sites. Science 301: 1096-1099
16. Katinka MD, Duprat S, Cornillot E, Metenier G, Thomarat F, Prensier G, Barbe V, Peyretaillade E, Brottier P, Wincker P, Delbac F, El Alaoui H, Peyret P, Saurin W, Gouy M, Weissenbach J, Vivares CP (2001) Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi. Nature 414: 450-453
17. Kim B, Nesvizhskii AI, Rani PG, Hahn S, Aebersold R, Ranish JA (2007) The transcription elongation factor TFIIS is a component of RNA polymerase II preinitiation complexes. Proc Natl Acad Sci USA 104: 16068-16073
18. Koch M, Diebold ML, Cavarelli J, Romier C (2010) Crystallization and preliminary crystallographic analysis of eukaryotic transcription and mRNA export factor Iws1 from Encephalitozoon cuni-culi. Acta Crystallogr Sect F Struct Biol Cryst Commun 66(Part 2): 207-210
19. Krogan NJ, Kim M, Ahn SH, Zhong G, Kobor MS, Cagney G, Emili A, Shilatifard A, Buratowski S, Greenblatt JF (2002) RNA poly-merase II elongation factors of Saccharomyces cerevisiae: a targeted proteomics approach. Mol Cell Biol 22: 6979-6992
20. La Fortelle E, Bricogne G (1997) Maximum-likelihood heavy-atom parameter refinement for multiple isomorphous replacement and multiwavelength anomalous diffraction methods. In: Methods in Enzymology, Carter JCW, Sweet RM (eds), Vol. 276, pp 472-494. New-York: Academic Press
21. Li B, Carey M, Workman JL (2007) The role of chromatin during transcription. Cell 128: 707-719
22. Lindstrom DL, Squazzo SL, Muster N, Burckin TA, Wachter KC, Emigh CA, McCleery JA, Yates III JR, Hartzog GA (2003) Dual roles for Spt5 in pre-mRNA processing and transcription elongation revealed by identification of Spt5-associated proteins. Mol Cell Biol 23: 1368-1378
23. Ling Y, Smith AJ, Morgan GT (2006) A sequence motif conserved in diverse nuclear proteins identifies a protein interaction domain utilised for nuclear targeting by human TFIIS. Nucleic Acids Res 34: 2219-2229
24. Mayer A, Lidschreiber M, Siebert M, Leike K, Soding J, Cramer P (2010) Uniform transitions of the general RNA polymerase II transcription complex. Nat Struct Mol Biol 17: 1272-1278
25. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ (2007) Phaser crystallographic software. J Appl Crystallogr 40(Part 4): 658-674
26. Nicholls A, Sharp KA, Honig B (1991) Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins 11 : 281-296
27. Otwinowski Z, Minor W (1997) Processing X-ray diffraction data collected in oscillation mode. In Methods in Enzymology, Carter JCW, Sweet RM (eds), Vol. 276, pp 307-326. New-York: Academic Press
28. Pan G, Aso T, Greenblatt J (1997) Interaction of elongation factors TFIIS and elongin A with a human RNA polymerase II holoenzyme capable of promoter-specific initiation and responsive to transcriptional activators. J Biol Chem 272: 24563-24571
29. Perales R, Bentley D (2009) 'Cotranscriptionality': the transcription elongation complex as a nexus for nuclear transactions. Mol Cell 36: 178-191
30. Prather DM, Larschan E, Winston F (2005) Evidence that the elongation factor TFIIS plays a role in transcription initiation at GAL1 in Saccharomyces cerevisiae. Mol Cell Biol 25: 2650-2659
31. Pujari V, Radebaugh CA, Chodaparambil JV, Muthurajan UM, Almeida AR, Fischbeck JA, Luger K, Stargell LA (2010) The transcription factor Spn1 regulates gene expression via a highly conserved novel structural motif. J Mol Biol (doi:10.1016/j.jmb. 2010.09.040)
32. 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 prokaryotic and eukaryotic hosts: experimental procedures, database tracking and case studies. Acta Crystallogr D Biol Crystallogr 62(Part 10): 1232-1242
33. Romier C, James N, Birck C, Cavarelli J, Vivares C, Collart MA, Moras D (2007) Crystal structure, biochemical and genetic characterization of yeast and E. cuniculi TAF(II)5 N-terminal domain: implications for TFIID assembly. J Mol Biol 368: 1292-1306
34. Rose MD, Winston F, Hieter P (1990) Laboratory Course Manual for Methods in Yeast Genetics. New York: Cold Spring Harbor
35. Saunders A, Core LJ, Lis JT (2006) Breaking barriers to transcription elongation. Nat Rev Mol Cell Biol 7: 557-567
36. Sun M, Lariviere L, Dengl S, Mayer A, Cramer P (2010) A tandem SH2 domain in transcription elongation factor Spt6 binds the phosphorylated RNA polymerase II CTD. J Biol Chem (doi:10.1074/jbc.M110.144568)
37. Wery M, Shematorova E, Van Driessche B, Vandenhaute J, Thuriaux P, Van Mullem V (2004) Members of the SAGA and Mediator complexes are partners of the transcription elongation factor TFIIS. EMBO J 23: 4232-4242
38. Winkler M, aus Dem Siepen T, Stamminger T (2000) Functional interaction between pleiotropic transactivator pUL69 of human cytomegalovirus and the human homolog of yeast chromatin regulatory protein SPT6. J Virol 74: 8053-8064
39. Yoh SM, Cho H, Pickle L, Evans RM, Jones KA (2007) The Spt6 SH2 domain binds Ser2-P RNAPII to direct Iws1-dependent mRNA splicing and export. Genes Dev 21: 160-174
40. Yoh SM, Lucas JS, Jones KA (2008) The Iws1:Spt6:CTD complex controls cotranscriptional mRNA biosynthesis and HYPB/Setd2-mediated histone H3K36 methylation. Genes Dev 22: 3422-3434
41. Zhang L, Fletcher AG, Cheung V, Winston F, Stargell LA (2008) Spn1 regulates the recruitment of Spt6 and the Swi/Snf complex during transcriptional activation by RNA polymerase II. Mol Cell Biol 28: 1393-1403