RNA polymerase II structure, and organization of the preinitiation complex

Current Opinion in Structural Biology

Volumn 14, Issue 2, 2004, Pages 121-129

  Asturias, Francisco J ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

Cryo electron microscopy; Cryo EM; Double stranded DNA; dsDNA; General transcription factor; GTF; PIC; Preinitiation complex; RNA polymerase II; RNAPII; TATA binding protein; TBP; TFIIA, IIB, IID, IIE, IIF, IIH; Transcription factors

Indexed keywords

RNA POLYMERASE II;

COMPLEX FORMATION; CRYOELECTRON MICROSCOPY; DNA RNA HYBRIDIZATION; ENZYME STRUCTURE; EUKARYOTE EVOLUTION; HUMAN; MOLECULAR INTERACTION; MOLECULAR MODEL; NONHUMAN; PRIORITY JOURNAL; REVIEW; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; X RAY MICROANALYSIS;

ANIMALS; DNA-BINDING PROTEINS; HUMANS; MACROMOLECULAR SUBSTANCES; MODELS, MOLECULAR; RNA POLYMERASE II; SACCHAROMYCES CEREVISIAE; TRANSCRIPTION FACTORS, TFII; TRANSCRIPTION, GENETIC;

EUKARYOTA;

EID: 1842839787     PISSN: 0959440X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.sbi.2004.03.007     Document Type: Review

References (49)

1. Cramer P., Bushnell D.A., Kornberg R.D. Structural basis of transcription: RNA polymerase II at 2.8 angstrom resolution. Science. 292:2001;1863-1876.
2. Zhang G., Campbell E.A., Minakhin L., Richter C., Severinov K., Darst S.A. Crystal structure of Thermus aquaticus core RNA polymerase at 3.3 Å resolution. Cell. 98:1999;811-824.
3. Fu J., Gnatt A.L., Bushnell D.A., Jensen G.J., Thompson N.E., Burgess R.R., David P.R., Kornberg R.D. Yeast RNA polymerase II at 5 Å resolution. Cell. 98:1999;799-810.
4. Cramer P., Bushnell D.A., Fu J., Gnatt A.L., Maier-Davis B., Thompson N.E., Burgess R.R., Edwards A.M., David P.R., Kornberg R.D. Architecture of RNA polymerase II and implications for the transcription mechanism. Science. 288:2000;640-649.
5. Gnatt A.L., Cramer P., Fu J., Bushnell D.A., Kornberg R.D. Structural basis of transcription: an RNA polymerase II elongation complex at 3.3 Å resolution. Science. 292:2001;1876-1882.
6. Dvir A., Conaway J.W., Conaway R.C. Mechanism of transcription initiation and promoter escape by RNA polymerase II. Curr Opin Genet Dev. 11:2001;209-214.
7. Woychik N.A., Hampsey M. The RNA polymerase II machinery: structure illuminates function. Cell. 108:2002;453-463.
8. Bushnell D.A., Cramer P., Kornberg R.D. Structural basis of transcription: alpha -Amanitin-RNA polymerase II cocrystal at 2.8 Å resolution. Proc Natl Acad Sci USA. 99:2002;1218-1222.
9. Craighead J., Chang W., Asturias F. Structure of yeast RNA polymerase II in solution. Implications for enzyme regulation and interaction with promoter DNA. Structure (Camb). 10:2002;1117-1125 This paper describes the structure of the complete (12-subunit) RNAPII, showing the polymerase clamp in its functional conformation. The structure led to the proposition that promoter melting would be required for the DNA template strand to reach the polymerase active site.
10. Armache K.J., Kettenberger H., Cramer P. Architecture of initiation-competent 12-subunit RNA polymerase II. Proc Natl Acad Sci USA. 100:2003;6964-6968 Here, the X-ray structure of the complete (12-subunit) RNAPII is described, and the exact mode of interaction between the core enzyme and the Rpb4-Rpb7 complex is determined.
11. •].
12. 3.2 loop in abortive initiation.
13. Vassylyev D.G., Sekine S., Laptenko O., Lee J., Vassylyeva M.N., Borukhov S., Yokoyama S. Crystal structure of a bacterial RNA polymerase holoenzyme at 2.6 Å resolution. Nature. 417:2002;712-719 This paper describes the X-ray structure of the T. thermophilus RNA polymerase holoenzyme.
14. Conaway J.W., Conaway R.C. An RNA polymerase II transcription factor shares functional properties with Escherichia coli sigma 70. Science. 248:1990;1550-1553.
15. Killeen M.T., Greenblatt J.F. The general transcription factor RAP30 binds to RNA polymerase II and prevents it from binding nonspecifically to DNA. Mol Cell Biol. 12:1992;30-37.
16. Tan S., Conaway R.C., Conaway J.W. Dissection of transcription factor TFIIF functional domains required for initiation and elongation. Proc Natl Acad Sci USA. 92:1995;6042-6046.
17. Henry N.L., Campbell A.M., Feaver W.J., Poon D., Weil P.A., Kornberg R.D. TFIIF-TAF-RNA polymerase II connection. Genes Dev. 8:1994;2868-2878.
18. Sopta M., Burton Z.F., Greenblatt J. Structure and associated DNA-helicase activity of a general transcription initiation factor that binds to RNA polymerase II. Nature. 341:1989;410-414.
19. Chung W.H., Craighead J.L., Chang W.H., Ezeokonkwo C., Bareket-Samish A., Kornberg R.D., Asturias F.J. RNA polymerase II/TFIIF structure and conserved organization of the initiation complex. Mol Cell. 12:2003;1003-1013 Here, the low-resolution structure of the yeast RNAPII-IIF complex is described. The middle IIF subunit, Tfg2, was identified as the structural homolog of the bacterial σ factor, leading to the proposition of a conserved mode of interaction between RNA polymerase and promoter DNA. These ideas were used to propose a model for the organization of the catalytic core of the transcription machinery.
20. ••].
21. Nikolov D.B., Chen H., Halay E.D., Usheva A.A., Hisatake K., Lee D.K., Roeder R.G., Burley S.K. Crystal structure of a TFIIB-TBP-TATA-element ternary complex. Nature. 377:1995;119-128.
22. Tsai F.T., Sigler P.B. Structural basis of preinitiation complex assembly on human pol II promoters. EMBO J. 19:2000;25-36.
23. Tyree C.M., George C.P., Lira-DeVito L.M., Wampler S.L., Dahmus M.E., Zawel L., Kadonaga J.T. Identification of a minimal set of proteins that is sufficient for accurate initiation of transcription by RNA polymerase II. Genes Dev. 7:1993;1254-1265.
24. Parvin J.D., Sharp P.A. DNA topology and a minimal set of basal factors for transcription by RNA polymerase II. Cell. 73:1993;533-540.
25. Parvin J.D., Shykind B.M., Meyers R.E., Kim J., Sharp P.A. Multiple sets of basal factors initiate transcription by RNA polymerase II. J Biol Chem. 269:1994;18414-18421.
26. Bushnell D.A., Westover K.D., Davis R., Kornberg R.D. Structural basis of transcription: an RNA polymerase II-transcription factor IIB cocrystal at 4.5-Å resolution, and architecture of the transcription initiation complex. Science. 303:2004;983-988.
27. Pokholok D.K., Hannett N.M., Young R.A. Exchange of RNA polymerase II initiation and elongation factors during gene expression in vivo. Mol Cell. 9:2002;799-809.
28. Murakami K.S., Darst S.A. Bacterial RNA polymerases: the wholo story. Curr Opin Struct Biol. 13:2003;31-39 A clear and informative review of structural studies of the bacterial holoenzyme and the bacterial initiation process.
29. Kelleher I.R.J., Flanagan P.M., Kornberg R.D. A novel mediator between activator proteins and the RNA polymerase II transcription apparatus. Cell. 61:1990;1209-1215.
30. Flanagan P.M., Kelleher R.J. III, Sayre M.H., Tschochner H., Kornberg R.D. A mediator required for activation of RNA polymerase II transcription in vitro. Nature. 350:1991;436-438.
31. Kim Y.J., Bjorklund S., Li Y., Sayre M.H., Kornberg R.D. A multiprotein mediator of transcriptional activation and its interaction with the C-terminal repeat domain of RNA polymerase II. Cell. 77:1994;599-608.
32. Myers L.C., Gustafsson C.M., Hayashibara K.C., Brown P.O., Kornberg R.D. Mediator protein mutations that selectively abolish activated transcription. Proc Natl Acad Sci USA. 96:1999;67-72.
33. Boube M., Joulia L., Cribbs D.L., Bourbon H.M. Evidence for a mediator of RNA polymerase II transcriptional regulation conserved from yeast to man. Cell. 110:2002;143-151.
34. Malik S., Roeder R.G. Transcriptional regulation through Mediator-like coactivators in yeast and metazoan cells. Trends Biochem Sci. 25:2000;277-283.
35. Baek H.J., Malik S., Qin J., Roeder R.G. Requirement of TRAP/mediator for both activator-independent and activator-dependent transcription in conjunction with TFIID-associated TAF(II)s. Mol Cell Biol. 22:2002;2842-2852.
36. Davis J.A., Takagi Y., Kornberg R.D., Asturias F.A. Structure of the yeast RNA polymerase II holoenzyme: Mediator conformation and polymerase interaction. Mol Cell. 10:2002;409-415 This paper describes the low-resolution structure of the yeast RNAPII-Mediator complex, and identifies the relative orientation of RNAPII and Mediator. It demonstrates the requirement for large conformational changes in Mediator for interaction with RNAPII.
37. Tan Q., Linask K.L., Ebright R.H., Woychik N.A. Activation mutants in yeast RNA polymerase II subunit RPB3 provide evidence for a structurally conserved surface required for activation in eukaryotes and bacteria. Genes Dev. 14:2000;339-348.
38. Busby S., Ebright R.H. Transcription activation by catabolite activator protein (CAP). J Mol Biol. 293:1999;199-213.
39. Niu W., Kim Y., Tau G., Heyduk T., Ebright R.H. Transcription activation at class II CAP-dependent promoters: two interactions between CAP and RNA polymerase. Cell. 87:1996;1123-1134.
40. Cosma M.P., Tanaka T., Nasmyth K. Ordered recruitment of transcription and chromatin remodeling factors to a cell cycle- and developmentally regulated promoter. Cell. 97:1999;299-311.
41. Park J.M., Werner J., Kim J.M., Lis J.T., Kim Y.J. Mediator, not holoenzyme, is directly recruited to the heat shock promoter by HSF upon heat shock. Mol Cell. 8:2001;9-19.
42. Shang Y., Hu X., DiRenzo J., Lazar M.A., Brown M. Cofactor dynamics and sufficiency in estrogen receptor-regulated transcription. Cell. 103:2000;843-852.
43. Yudkovsky N., Ranish J.A., Hahn S. A transcription reinitiation intermediate that is stabilized by activator. Nature. 408:2000;225-229.
44. Reeves W.M., Hahn S. Activator-independent functions of the yeast mediator sin4 complex in preinitiation complex formation and transcription reinitiation. Mol Cell Biol. 23:2003;349-358 The authors describe the role of a Mediator-based complex in transcription re-initiation, and provide information about the possible role of Mediator modules in the initiation and re-initiation processes.
45. Asturias F.J., Jiang Y.W., Myers L.C., Gustafsson C.M., Kornberg R.D. Conserved structures of mediator and RNA polymerase II holoenzyme. Science. 283:1999;985-987.
46. Lewis B.A., Reinberg D. The mediator coactivator complex: functional and physical roles in transcriptional regulation. J Cell Sci. 116:2003;3667-3675.
47. Samuelsen C.O., Baraznenok V., Khorosjutina O., Spahr H., Kieselbach T., Holmberg S., Gustafsson C.M. TRAP230/ARC240 and TRAP240/ARC250 Mediator subunits are functionally conserved through evolution. Proc Natl Acad Sci USA. 100:2003;6422-6427.
48. Malik S., Wallberg A.E., Kang Y.K., Roeder R.G. TRAP/SMCC/mediator- dependent transcriptional activation from DNA and chromatin templates by orphan nuclear receptor hepatocyte nuclear factor 4. Mol Cell Biol. 22:2002;5626-5637.
49. Taatjes D.J., Naar A.M., Andel F. III, Nogales E., Tjian R. Structure, function, and activator-induced conformations of the CRSP coactivator. Science. 295:2002;1058-1062.