Coupling σ Factor Conformation to RNA Polymerase Reorganisation for DNA Melting

Journal of Molecular Biology

Volumn 387, Issue 2, 2009, Pages 306-319

  Burrows, Patricia C ^a   Joly, Nicolas ^a   Cannon, Wendy V ^a   Cámara, Beatriz P ^b   Rappas, Mathieu ^a   Zhang, Xiaodong ^a   Dawes, Kathleen ^a   Nixon, B Tracy ^c   Wigneshweraraj, Siva R ^b   Buck, Martin ^a  

^a Faculty of Natural Sciences   (United Kingdom)

^b Faculty of Medicine   (United Kingdom)

^c PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

ATPase; DNA melting; protein DNA cross linking; RNA polymerase; transcription regulation

Indexed keywords

ADENOSINE TRIPHOSPHATE; DNA; RNA; RNA POLYMERASE;

ARTICLE; CATALYSIS; CONTROLLED STUDY; COUPLING FACTOR; DNA DENATURATION; GENE EXPRESSION; HYDROLYSIS; NONHUMAN; PRIORITY JOURNAL;

BACTERIA (MICROORGANISMS);

EID: 61849128326     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2009.01.052     Document Type: Article

References (39)

1. Cramer P. Multisubunit RNA polymerases. Curr. Opin. Struct. Biol. 12 (2002) 89-97
2. Rappas M., Bose D., and Zhang X. Bacterial enhancer-binding proteins: unlocking sigma54-dependent gene transcription. Curr. Opin. Struct. Biol. 17 (2007) 110-116
3. + enhancer binding proteins in transcriptional activation. J. Struct. Biol. 156 (2006) 190-199
4. Kim T.K., Ebright R.H., and Reinberg D. Mechanism of ATP-dependent promoter melting by transcription factor IIH. Science 288 (2000) 1418-1422
5. Lin Y.C., Choi W.S., and Gralla J.D. TFIIH XPB mutants suggest a unified bacterial-like mechanism for promoter opening but not escape. Nat. Struct. Mol. Biol. 12 (2005) 603-607
6. Cannon W.V., Gallegos M.T., and Buck M. Isomerization of a binary sigma-promoter DNA complex by transcription activators. Nat. Struct. Biol. 7 (2000) 594-601
7. Guo Y., Lew C.M., and Gralla J.D. Promoter opening by sigma(54) and sigma(70) RNA polymerases: sigma factor-directed alterations in the mechanism and tightness of control. Genes Dev. 14 (2000) 2242-2255
8. Wigneshweraraj S., Bose D., Burrows P.C., Joly N., Schumacher J., Rappas M., et al. Modus operandi of the bacterial RNA polymerase containing the sigma54 promoter-specificity factor. Mol. Microbiol. 68 (2008) 538-546
9. Chaney M., Grande R., Wigneshweraraj S.R., Cannon W., Casaz P., Gallegos M.T., et al. Binding of transcriptional activators to sigma 54 in the presence of the transition state analog ADP-aluminum fluoride: insights into activator mechanochemical action. Genes Dev. 15 (2001) 2282-2294
10. + ATPases support complex formation with their target protein, sigma54. Structure 15 (2007) 429-440
11. + ATPase domains. Genes Dev. 17 (2003) 2552-2563
12. Rappas M., Schumacher J., Beuron F., Niwa H., Bordes P., Wigneshweraraj S., et al. Structural insights into the activity of enhancer-binding proteins. Science 307 (2005) 1972-1975
13. Joly N., Rappas M., Buck M., and Zhang X. Trapping of a transcription complex using a new nucleotide analogue: AMP aluminium fluoride. J. Mol. Biol. 375 (2008) 1206-1211
14. Burrows P.C., Severinov K., Buck M., and Wigneshweraraj S.R. Reorganisation of an RNA polymerase-promoter DNA complex for DNA melting. EMBO J. 23 (2004) 4253-4263
15. + activator-dependent bacterial transcription initiation. J. Mol. Biol. 375 (2008) 43-58
16. Mayer A.N., and Barany F. Photoaffinity cross-linking of TaqI restriction endonuclease using an aryl azide linked to the phosphate backbone. Gene 153 (1995) 1-8
17. Wedel A., and Kustu S. The bacterial enhancer-binding protein NTRC is a molecular machine: ATP hydrolysis is coupled to transcriptional activation. Genes Dev. 9 (1995) 2042-2052
18. Popham D.L., Szeto D., Keener J., and Kustu S. Function of a bacterial activator protein that binds to transcriptional enhancers. Science 243 (1989) 629-635
19. + protease is dependent on ATP-hydrolysis rates and substrate energy landscapes. Nat. Struct. Mol. Biol. 15 (2008) 139-145
20. Sauna Z.E., Kim I.W., Nandigama K., Kopp S., Chiba P., and Ambudkar S.V. Catalytic cycle of ATP hydrolysis by P-glycoprotein: evidence for formation of the ES reaction intermediate with ATP-gamma-S, a nonhydrolyzable analogue of ATP. Biochemistry 46 (2007) 13787-13799
21. Bordes P., Wigneshweraraj S.R., Schumacher J., Zhang X., Chaney M., and Buck M. The ATP hydrolyzing transcription activator phage shock protein F of Escherichia coli: identifying a surface that binds sigma 54. Proc. Natl Acad. Sci. USA 100 (2003) 2278-2283
22. + domain of transcription activator PspF. J. Mol. Biol. 357 (2006) 481-492
23. Joly N., Rappas M., Wigneshweraraj S.R., Zhang X., and Buck M. Coupling nucleotide hydrolysis to transcription activation performance in a bacterial enhancer binding protein. Mol. Microbiol. 66 (2007) 583-595
24. + protein. J. Mol. Biol. 338 (2004) 863-875
25. + transcriptional activator. J. Biol. Chem. 281 (2006) 34997-35007
26. + ring ATPase. J. Mol. Biol. 381 (2008) 1-12
27. Wigneshweraraj S.R., Burrows P.C., Severinov K., and Buck M. Stable DNA opening within open promoter complexes is mediated by the RNA polymerase beta′-jaw domain. J. Biol. Chem. 280 (2005) 36176-36184
28. Wigneshweraraj S.R., Nechaev S., Bordes P., Jones S., Cannon W., Severinov K., and Buck M. Enhancer-dependent transcription by bacterial RNA polymerase: the beta subunit downstream lobe is used by sigma 54 during open promoter complex formation. Methods Enzymol. 370 (2003) 646-657
29. Cannon W., Gallegos M.T., Casaz P., and Buck M. Amino-terminal sequences of sigmaN (sigma54) inhibit RNA polymerase isomerization. Genes Dev. 13 (1999) 357-370
30. Wigneshweraraj S.R., Burrows P.C., Nechaev S., Zenkin N., Severinov K., and Buck M. Regulated communication between the upstream face of RNA polymerase and the beta′ subunit jaw domain. EMBO J. 23 (2004) 4264-4274
31. Ederth J., Artsimovitch I., Isaksson L.A., and Landick R. The downstream DNA jaw of bacterial RNA polymerase facilitates both transcriptional initiation and pausing. J. Biol. Chem. 277 (2002) 37456-37463
32. Wigneshweraraj S.R., Savalia D., Severinov K., and Buck M. Interplay between the beta′ clamp and the beta′ jaw domains during DNA opening by the bacterial RNA polymerase at sigma54-dependent promoters. J. Mol. Biol. 359 (2006) 1182-1195
33. + proteins for transcription activation. J. Biol. Chem 283 (2008) 13725-13735
34. Cannon W., Gallegos M.T., and Buck M. DNA melting within a binary sigma(54)-promoter DNA complex. J. Biol. Chem. 276 (2001) 386-394
35. Young B.A., Gruber T.M., and Gross C.A. Minimal machinery of RNA polymerase holoenzyme sufficient for promoter melting. Science 303 (2004) 1382-1384
36. Bose D., Pape T., Burrows P.C., Rappas M., Wigneshweraraj S.R., Buck M., and Zhang X. Organization of an activator-bound RNA polymerase holoenzyme. Mol. Cell 32 (2008) 337-346
37. Wang J.T., Syed A., and Gralla J.D. Multiple pathways to bypass the enhancer requirement of sigma 54 RNA polymerase: roles for DNA and protein determinants. Proc. Natl Acad. Sci. USA 94 (1997) 9538-9543
38. 2-terminal leucine patch in sigma 54. Science 270 (1995) 992-994
39. Lim H.M., Lee H.J., Roy S., and Adhya S. A "master" in base unpairing during isomerization of a promoter upon RNA polymerase binding. Proc. Natl Acad. Sci. USA 98 (2001) 14849-14852