Archaeal TFEα/β is a hybrid of TFIIE and the RNA polymerase III subcomplex hRPC62/39

eLife

Volumn 4, Issue JUNE2015, 2015, Pages

  Blombach, Fabian ^a   Salvadori, Enrico ^a   Fouqueau, Thomas ^a   Yan, Jun ^a   Reimann, Julia ^b   Sheppard, Carol ^a   Smollett, Katherine L ^a   Albers, Sonja V ^b,c   Kay, Christopher W M ^a   Thalassinos, Konstantinos ^a   Werner, Finn ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b MAX PLANCK INSTITUTE FOR TERRESTRIAL MICROBIOLOGY   (Germany)

^c UNIVERSITY OF FREIBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DNA DIRECTED RNA POLYMERASE III; RECOMBINANT PROTEIN; TRANSCRIPTION FACTOR II; TRANSCRIPTION FACTOR TFIIE;

ARTICLE; CELL VIABILITY; DNA DENATURATION; ELECTRON SPIN RESONANCE; EVOLUTIONARY ADAPTATION; EVOLUTIONARY HOMOLOGY; GENETIC TRANSCRIPTION; MICROBIAL COMMUNITY; NONHUMAN; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; ENZYMOLOGY; GENETICS; METABOLISM; PROTEIN MULTIMERIZATION; SEQUENCE HOMOLOGY; SULFOLOBUS SOLFATARICUS;

ARCHAEA; EUKARYOTA;

PROTEIN MULTIMERIZATION; RECOMBINANT PROTEINS; RNA POLYMERASE III; SEQUENCE HOMOLOGY, AMINO ACID; SULFOLOBUS SOLFATARICUS; TRANSCRIPTION FACTORS, TFII;

EID: 84937057428     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.08378     Document Type: Article

References (58)

1. Albers SV, Jonuscheit M, Dinkelaker S, Urich T, Kletzin A, Tampe R, Driessen AJ, Schleper C. 2006. Production of recombinant and tagged proteins in the hyperthermophilic archaeon Sulfolobus solfataricus. Applied and Environmental Microbiology 72:102-111. doi: 10.1128/AEM.72.1.102-111.2006.
2. Aravind L, Anantharaman V, Balaji S, Babu MM, Iyer LM. 2005. The many faces of the helix-turn-helix domain: transcription regulation and beyond. FEMS Microbiology Reviews 29:231-262. doi: 10.1016/j.femsre.2004.12.008.
3. Beinert H, Kennedy MC, Stout CD. 1996. Aconitase as iron-sulfur protein, enzyme, and iron-regulatory protein. Chemical Reviews 96:2335-2374. doi: 10.1021/cr950040z.
4. Bell SD, Brinkman AB, van der Oost J, Jackson SP. 2001. The archaeal TFIIEalpha homologue facilitates transcription initiation by enhancing TATA-box recognition. EMBO Reports 2:133-138. doi: 10.1093/emboreports/kve021.
5. Blombach F, Launay H, Snijders AP, Zorraquino V, Wu H, de Koning B, Brouns SJ, Ettema TJ, Camilloni C, Cavalli A, Vendruscolo M, Dickman MJ, Cabrita LD, La Teana A, Benelli D, Londei P, Christodoulou J, van der Oost J. 2014. Archaeal MBF1 binds to 30S and 70S ribosomes via its helix-turn-helix domain. The Biochemical Journal 462: 373-384. doi: 10.1042/BJ20131474.
6. Blombach F, Makarova KS, Marrero J, Siebers B, Koonin EV, van der Oost J. 2009. Identification of an ortholog of the eukaryotic RNA polymerase III subunit RPC34 in Crenarchaeota and Thaumarchaeota suggests specialization of RNA polymerases for coding and non-coding RNAs in Archaea. Biology Direct 4:39. doi: 10.1186/1745-6150-4-39.
7. Bushnell DA, Kornberg RD. 2003. Complete, 12-subunit RNA polymerase II at 4.1-A resolution: implications for the initiation of transcription. Proceedings of the National Academy of Sciences of USA 100:6969-6973. doi: 10.1073/pnas.1130601100.
8. 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. Molecular Biology and Evolution 27:1035-1043. doi: 10.1093/molbev/msp316.
9. Duttke SH, Doolittle RF, Wang YL, Kadonaga JT. 2014. TRF2 and the evolution of the bilateria. Genes & Development 28:2071-2076. doi: 10.1101/gad.250563.114.
10. Facciotti MT, Reiss DJ, Pan M, Kaur A, Vuthoori M, Bonneau R, Shannon P, Srivastava A, Donohoe SM, Hood LE, Baliga NS. 2007. General transcription factor specified global gene regulation in archaea. Proceedings of the National Academy of Sciences of USA 104:4630-4635. doi: 10.1073/pnas.0611663104.
11. Feaver WJ, Henry NL, Bushnell DA, Sayre MH, Brickner JH, Gileadi O, Kornberg RD. 1994. Yeast TFIIE. Cloning, expression, and homology to vertebrate proteins. Journal of Biological Chemistry 269:27549-27553.
12. Fishburn J, Tomko E, Galburt E, Hahn S. 2015. Double-stranded DNA translocase activity of transcription factor TFIIH and the mechanism of RNA polymerase II open complex formation. Proceedings of the National Academy of Sciences of USA 112:3961-3966. doi: 10.1073/pnas.1417709112.
13. Gietl A, Holzmeister P, Blombach F, Schulz S, von Voithenberg LV, Lamb DC, Werner F, Tinnefeld P, Grohmann D. 2014. Eukaryotic and archaeal TBP and TFB/TF(II)B follow different promoter DNA bending pathways. Nucleic Acids Research 42:6219-6231. doi: 10.1093/nar/gku273.
14. Goodrich JA, Tjian R. 2010. Unexpected roles for core promoter recognition factors in cell-type-specific transcription and gene regulation. Nature Reviews Genetics 11:549-558. doi: 10.1038/nrg2847.
15. Grogan DW. 2003. Cytosine methylation by the SuaI restriction-modification system: implications for genetic fidelity in a hyperthermophilic archaeon. Journal of Bacteriology 185:4657-4661. doi: 10.1128/JB.185.15.4657-4661.2003.
16. Grohmann D, Nagy J, Chakraborty A, Klose D, Fielden D, Ebright RH, Michaelis J, Werner F. 2011. The initiation factor TFE and the elongation factor Spt4/5 compete for the RNAP clamp during transcription initiation and elongation. Molecular Cell 43:263-274. doi: 10.1016/j.molcel.2011.05.030.
17. Grünberg S, Warfield L, Hahn S. 2012. Architecture of the RNA polymerase II preinitiation complex and mechanism of ATP-dependent promoter opening. Nature Structural & Molecular Biology 19:788-796. doi: 10.1038/nsmb.2334.
18. Guy L, Ettema TJ. 2011. The archaeal ’TACK’ superphylum and the origin of eukaryotes. Trends in Microbiology 19:580-587. doi: 10.1016/j.tim.2011.09.002.
19. Guzman E, Lis JT. 1999. Transcription factor TFIIH is required for promoter melting in vivo. Molecular and Cellular Biology 19:5652-5658.
20. Hanzelka BL, Darcy TJ, Reeve JN. 2001. TFE, an archaeal transcription factor in Methanobacterium thermoautotrophicum related to eucaryal transcription factor TFIIEalpha. Journal of Bacteriology 183:1813-1818. doi: 10.1128/JB.183.5.1813-1818.2001.
21. Hausner W, Wettach J, Hethke C, Thomm M. 1996. Two transcription factors related with the eucaryal transcription factors TATA-binding protein and transcription factor IIB direct promoter recognition by an archaeal RNA polymerase. The Journal of Biological Chemistry 271:30144-30148. doi: 10.1074/jbc.271.47.30144.
22. He Y, Fang J, Taatjes DJ, Nogales E. 2013. Structural visualization of key steps in human transcription initiation. Nature 495:481-486. doi: 10.1038/nature11991.
23. Hirata A, Klein BJ, Murakami KS. 2008. The X-ray crystal structure of RNA polymerase from Archaea. Nature 451: 851-854. doi: 10.1038/nature06530.
24. Holstege FC, Tantin D, Carey M, van der Vliet PC, Timmers HT. 1995. The requirement for the basal transcription factor IIE is determined by the helical stability of promoter DNA. EMBO Journal 14:810-819.
25. Holstege FC, van der Vliet PC, Timmers H. 1996. Opening of an RNA polymerase II promoter occurs in two distinct steps and requires the basal transcription factors IIE and IIH. EMBO Journal 15:1666-1677.
26. Jonuscheit M, Martusewitsch E, Stedman KM, Schleper C. 2003. A reporter gene system for the hyperthermophilic archaeon Sulfolobus solfataricus based on a selectable and integrative shuttle vector. Molecular Microbiology 48: 1241-1252. doi: 10.1046/j.1365-2958.2003.03509.x.
27. Jun SH, Hirata A, Kanai T, Santangelo TJ, Imanaka T, Murakami KS. 2014. The X-ray crystal structure of the euryarchaeal RNA polymerase in an open-clamp configuration. Nature Communications 5:5132. doi: 10.1038/ncomms6132.
28. Kim TK, Ebright RH, Reinberg D. 2000. Mechanism of ATP-dependent promoter melting by transcription factor IIH. Science 288:1418-1422. doi: 10.1126/science.288.5470.1418.
29. Korkhin Y, Unligil UM, Littlefield O, Nelson PJ, Stuart DI, Sigler PB, Bell SD, Abrescia NG. 2009. Evolution of complex RNA polymerases: the complete archaeal RNA polymerase structure. PLOS Biology 7:e102. doi: 10.1371/journal.pbio.1000102.
30. Kostrewa D, Zeller M, Armache K, Seizl M, Leike K, Thomm M, Cramer P. 2009. RNA polymerase II-TFIIB structure and mechanism of transcription initiation. Nature 462:323-330. doi: 10.1038/nature08548.
31. Kuldell NH, Buratowski S. 1997. Genetic analysis of the large subunit of yeast transcription factor IIE reveals two regions with distinct functions. Molecular and Cellular Biology 17:5288-5298.
32. Lefèvre S, Dumay-Odelot H, El-Ayoubi L, Budd A, Legrand P, Pinaud N, Teichmann M, Fribourg S. 2011. Structurefunction analysis of hRPC62 provides insights into RNA polymerase III transcription initiation. Nature Structural & Molecular Biology 18:352-358. doi: 10.1038/nsmb.1996.
33. Martinez-Rucobo FW, Sainsbury S, Cheung AC, Cramer P. 2011. Architecture of the RNA polymerase-Spt4/5 complex and basis of universal transcription processivity. The EMBO Journal 30:1302-1310. doi: 10.1038/emboj.2011.64.
34. Meinhart A, Blobel J, Cramer P. 2003. An extended winged helix domain in general transcription factor E/IIE alpha. The Journal of Biological Chemistry 278:48267-48274. doi: 10.1074/jbc.M307874200.
35. Meyer BH, Albers SV. 2014. AglB, catalyzing the oligosaccharyl transferase step of the archaeal N-glycosylation process, is essential in the thermoacidophilic crenarchaeon Sulfolobus acidocaldarius. Microbiologyopen 3: 531-543. doi: 10.1002/mbo3.185.
36. Nagy J, Grohmann D, Cheung AC, Schulz S, Smollett K, Werner F, Michaelis J. 2015. Complete architecture of the archaeal RNA polymerase open complex from single-molecule FRET and NPS. Nature Communications 6:6161. doi: 10.1038/ncomms7161.
37. Naji S, Grünberg S, Thomm M. 2007. The RPB7 orthologue E’ is required for transcriptional activity of a reconstituted archaeal core enzyme at low temperatures and stimulates open complex formation. The Journal of Biological Chemistry 282:11047-11057. doi: 10.1074/jbc.M611674200.
38. Netz DJ, Stith CM, Stumpfig M, Kopf G, Vogel D, Genau HM, Stodola JL, Lill R, Burgers PM, Pierik AJ. 2012. Eukaryotic DNA polymerases require an iron-sulfur cluster for the formation of active complexes. Nature Chemical Biology 8:125-132. doi: 10.1038/nchembio.721.
39. Parvin JD, Sharp PA. 1993. DNA topology and a minimal set of basal factors for transcription by RNA polymerase II. Cell 73:533-540. doi: 10.1016/0092-8674(93)90140-L.
40. Peterson MG, Inostroza J, Maxon ME, Flores O, Admon A, Reinberg D, Tjian R. 1991. Structure and functional properties of human general transcription factor IIE. Nature 354:369-373. doi: 10.1038/354369a0.
41. Pringle SD, Giles K, Wildgoose JL, Williams JP, Slade SE, Thalassinos K, Bateman RH, Bowers MT, Scrivens JH. 2007. An investigation of the mobility separation of some peptide and protein ions using a new hybrid quadrupole/travelling wave IMS/oa-ToF instrument. Int. J. Mass Spectrom 261:1-12. doi: 10.1016/j.ijms.2006.07.021.
42. Proshkina GM, Shematorova EK, Proshkin SA, Zaros C, Thuriaux P, Shpakovski GV. 2006. Ancient origin, functional conservation and fast evolution of DNA-dependent RNA polymerase III. Nucleic Acids Research 34:3615-3624. doi: 10.1093/nar/gkl421.
43. Qureshi SA, Bell SD, Jackson SP. 1997. Factor requirements for transcription in the Archaeon Sulfolobus shibatae. The EMBO Journal 16:2927-2936. doi: 10.1093/emboj/16.10.2927.
44. Rouillon C, White MF. 2011. The evolution and mechanisms of nucleotide excision repair proteins. Research in Microbiology 162:19-26. doi: 10.1016/j.resmic.2010.09.003.
45. Sawadogo M, Roeder RG. 1985. Factors involved in specific transcription by human RNA polymerase II: analysis by a rapid and quantitative in vitro assay. Proceedings of the National Academy of Sciences of USA 82:4394-4398. doi: 10.1073/pnas.82.13.4394.
46. Stettler S, Mariotte S, Riva M, Sentenac A, Thuriaux P. 1992. An essential and specific subunit of RNA polymerase III (C) is encoded by gene RPC34 in Saccharomyces cerevisiae. The Journal of Biological Chemistry 267: 21390-21395.
47. Vannini A, Cramer P. 2012. Conservation between the RNA polymerase I, II, and III transcription initiation machineries. Molecular Cell 45:439-446. doi: 10.1016/j.molcel.2012.01.023.
48. Vannini A, Ringel R, Kusser AG, Berninghausen O, Kassavetis GA, Cramer P. 2010. Molecular basis of RNA polymerase III transcription repression by Maf1. Cell 143:59-70. doi: 10.1016/j.cell.2010.09.002.
49. Wagner M, van Wolferen M, Wagner A, Lassak K, Meyer BH, Reimann J, Albers SV. 2012. Versatile genetic Tool box for the Crenarchaeote Sulfolobus acidocaldarius. Frontiers in Microbiology 3:214. doi: 10.3389/fmicb.2012.00214.
50. Wang YL, Duttke SH, Chen K, Johnston J, Kassavetis GA, Zeitlinger J, Kadonaga JT. 2014. TRF2, but not TBP, mediates the transcription of ribosomal protein genes. Genes & Development 28:1550-1555. doi: 10.1101/gad.245662.114.
51. Werner F, Grohmann D. 2011. Evolution of multisubunit RNA polymerases in the three domains of life. Nature Reviews Microbiology 9:85-98. doi: 10.1038/nrmicro2507.
52. Werner F, Weinzierl RO. 2002. A recombinant RNA polymerase II-like enzyme capable of promoter-specific transcription. Molecular Cell 10:635-646. doi: 10.1016/S1097-2765(02)00629-9.
53. Werner F, Weinzierl RO. 2005. Direct modulation of RNA polymerase core functions by basal transcription factors. Molecular and Cellular Biology 25:8344-8355. doi: 10.1128/MCB.25.18.8344-8355.2005.
54. White MF, Dillingham MS. 2012. Iron-sulphur clusters in nucleic acid processing enzymes. Current Opinion in Structural Biology 22:94-100. doi: 10.1016/j.sbi.2011.11.004.
55. Williams TA, Foster PG, Cox CJ, Embley TM. 2013. An archaeal origin of eukaryotes supports only two primary domains of life. Nature 504:231-236. doi: 10.1038/nature12779.
56. Wu CC, Herzog F, Jennebach S, Lin YC, Pai CY, Aebersold R, Cramer P, Chen HT. 2012. RNA polymerase III subunit architecture and implications for open promoter complex formation. Proceedings of the National Academy of Sciences of USA 109:19232-19237. doi: 10.1073/pnas.1211665109.
57. Yutin N, Makarova KS, Mekhedov SL, Wolf YI, Koonin EV. 2008. The deep archaeal roots of eukaryotes. Molecular Biology and Evolution 25:1619-1630. doi: 10.1093/molbev/msn108.
58. Zaparty M, Esser D, Gertig S, Haferkamp P, Kouril T, Manica A, Pham TK, Reimann J, Schreiber K, Sierocinski P, Teichmann D, van Wolferen M, von Jan M, Wieloch P, Albers SV, Driessen AJ, Klenk HP, Schleper C, Schomburg D, van der Oost J, Wright PC, Siebers B. 2010. ‘Hot standards’ for the thermoacidophilic archaeon Sulfolobus solfataricus. Extremophiles 14:119-142. doi: 10.1007/s00792-009-0280-0.