A common feature from different subunits of a homomeric AAA+ protein contacts three spatially distinct transcription elements

Nucleic Acids Research

Volumn 40, Issue 18, 2012, Pages 9139-9152

  Zhang, Nan ^a   Joly, Nicolas ^a,b   Buck, Martin ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b INSTITUT JACQUES MONOD   (France)

Author keywords

[No Author keywords available]

Indexed keywords

4 BENZOYL LEVO PHENYLALANINE; ALANINE; AMINO ACID; AMINO ACID TRANSFER RNA LIGASE; NUCLEOTIDE; RNA POLYMERASE; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; DNA STRAND; ISOMERIZATION; MOLECULAR INTERACTION; PRIORITY JOURNAL; PROTEIN CROSS LINKING; PROTEIN DNA INTERACTION; PROTEIN NUCLEIC ACID INTERACTION; PROTEIN TARGETING; SEQUENCE ANALYSIS; STRUCTURE ACTIVITY RELATION;

ADENOSINE TRIPHOSPHATASES; AMINO ACID SEQUENCE; BINDING SITES; DNA; DNA-DIRECTED RNA POLYMERASES; ESCHERICHIA COLI PROTEINS; MOLECULAR SEQUENCE DATA; PROMOTER REGIONS, GENETIC; PROTEIN SUBUNITS; RNA POLYMERASE SIGMA 54; TRANS-ACTIVATORS; TRANSCRIPTIONAL ACTIVATION;

EID: 84867508943     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gks661     Document Type: Article

References (64)

1. Browning, D. F. and Busby, S. J. (2004) The regulation of bacterial transcription initiation. Nat. Rev. Microbiol., 2, 57-65. (Pubitemid 39490048)
2. Morris, L., Cannon, W., Claverie-Martin, F., Austin, S. and Buck, M. (1994) DNA distortion and nucleation of local DNA unwinding within sigma-54 (sigma N) holoenzyme closed promoter complexes. J. Biol. Chem., 269, 11563-11571.
3. Burrows, P. C., Wigneshweraraj, S. R. and Buck, M. (2008) Protein-DNA interactions that govern AAA+activator-dependent bacterial transcription initiation. J. Mol. Biol., 375, 43-58. (Pubitemid 350160688)
4. Friedman, L. J. and Gelles, J. (2012) Mechanism of transcription initiation at an activator-dependent promoter defined by single-molecule observation. Cell, 148, 679-689.
5. Lin, Y. C., Choi, W. S. and Gralla, J. D. (2005) TFIIH XPB mutants suggest a unified bacterial-like mechanism for promoter opening but not escape. Nat. Struct. Mol. Biol., 12, 603-607. (Pubitemid 40980810)
6. Studholme, D. J. and Buck, M. (2000) The biology of enhancer-dependent transcriptional regulation in bacteria: insights from genome sequences. FEMS Microbiol. Lett., 186, 1-9. (Pubitemid 30211734)
7. Wolfe, A. J., Millikan, D. S., Campbell, J. M. and Visick, K. L. (2004) Vibrio fischeri sigma54 controls motility, biofilm formation, luminescence, and colonization. Appl. Environ. Microbiol., 70, 2520-2524. (Pubitemid 38500560)
8. Correa, N. E., Lauriano, C. M., McGee, R. and Klose, K. E. (2000) Phosphorylation of the flagellar regulatory protein FlrC is necessary for Vibrio cholerae motility and enhanced colonization. Mol. Microbiol., 35, 743-755. (Pubitemid 30107526)
9. Fisher, M. A., Grimm, D., Henion, A. K.,-elias, A. F., Stewart, P. E., Rosa, P. A. and Gherardini, F. C. (2005) Borrelia burgdorferi sigma54 is required for mammalian infection and vector transmission but not for tick colonization. Proc. Natl Acad. Sci. USA, 102, 5162-5167.
10. Villain-Guillot, P., Bastide, L., Gualtieri, M. and Leonetti, J. P. (2007) Progress in targeting bacterial transcription. Drug Discov. Today, 12, 200-208. (Pubitemid 46321530)
11. Bose, D., Pape, T., Burrows, P. C., Rappas, M., Wigneshweraraj, S. R., Buck, M. and Zhang, X. (2008) Organization of an activator-bound RNA polymerase holoenzyme. Mol. Cell, 32, 337-346.
12. Rappas, M., Schumacher, J., Beuron, F., Niwa, H., Bordes, P., Wigneshweraraj, S., Keetch, C. A., Robinson, C. V., Buck, M. and Zhang, X. (2005) Structural insights into the activity of enhancer-binding proteins. Science, 307, 1972-1975. (Pubitemid 40404708)
13. Doucleff, M., Malak, L. T., Pelton, J. G. and Wemmer, D. E. (2005) The C-terminal RpoN domain of sigma54 forms an unpredicted helix-turn-helix motif similar to domains of sigma70. J. Biol. Chem., 280, 41530-41536. (Pubitemid 41832214)
14. Doucleff, M., Pelton, J. G., Lee, P. S., Nixon, B. T. and Wemmer, D. E. (2007) Structural basis of DNA recognition by the alternative sigma-factor, sigma54. J. Mol. Biol., 369, 1070-1078. (Pubitemid 46759524)
15. Hong, E., Doucleff, M. and Wemmer, D. E. (2009) Structure of the RNA polymerase core-binding domain of sigma(54) reveals a likely conformational fracture point. J. Mol. Biol., 390, 70-82.
16. Svergun, D. I., Malfois, M., Koch, M. H., Wigneshweraraj, S. R. and Buck, M. (2000) Low resolution structure of the sigma54 transcription factor revealed by X-ray solution scattering. J. Biol. Chem., 275, 4210-4214. (Pubitemid 30094657)
17. Chen, B., Sysoeva, T. A., Chowdhury, S., Guo, L., De Carlo, S., Hanson, J. A., Yang, H. and Nixon, B. T. (2010) Engagement of arginine finger to ATP triggers large conformational changes in NtrC1 AAA+ATPase for remodeling bacterial RNA polymerase. Structure, 18, 1420-1430.
18. De Carlo, S., Chen, B., Hoover, T. R., Kondrashkina, E., Nogales, E. and Nixon, B. T. (2006) The structural basis for regulated assembly and function of the transcriptional activator Ntr C. Genes Dev., 20, 1485-1495. (Pubitemid 43830655)
19. Lee, S. Y., De La Torre, A., Yan, D., Kustu, S., Nixon, B. T. and Wemmer, D. E. (2003) Regulation of the transcriptional activator NtrC1: structural studies of the regulatory and AAA+ATPase domains. Genes Dev., 17, 2552-2563. (Pubitemid 37271425)
20. Rappas, M., Schumacher, J., Niwa, H., Buck, M. and Zhang, X. (2006) Structural basis of the nucleotide driven conformational changes in the AAA+domain of transcription activator Psp F. J. Mol. Biol., 357, 481-492. (Pubitemid 43290749)
21. Bordes, P., Wigneshweraraj, S. R., Schumacher, J., Zhang, X., Chaney, M. and Buck, M. (2003) 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, 2278-2283. (Pubitemid 36297490)
22. Buck, M., Gallegos, M. T., Studholme, D. J., Guo, Y. and Gralla, J. D. (2000) The bacterial enhancer-dependent sigma(54) (sigma(N)) transcription factor. J. Bacteriol., 182, 4129-4136. (Pubitemid 30463773)
23. Sasse-Dwight, S. and Gralla, J. D. (1988) Probing the Escherichia coli glnALG upstream activation mechanism in vivo. Proc. Natl Acad. Sci. USA, 85, 8934-8938. (Pubitemid 19001819)
24. Cannon, W., Gallegos, M. T. and Buck, M. (2001) DNA melting within a binary sigma(54)-promoter DNA complex. J. Biol. Chem., 276, 386-394. (Pubitemid 32050331)
25. Gallegos, M. T. and Buck, M. (1999) Sequences in sigmaN determining holoenzyme formation and properties. J. Mol. Biol., 288, 539-553. (Pubitemid 29240514)
26. Erzberger, J. P. and Berger, J. M. (2006) Evolutionary relationships and structural mechanisms of AAA+proteins. Annu. Rev. Biophys. Biomol. Struct., 35, 93-114. (Pubitemid 43877371)
27. Joly, N.,-engl, C., Jovanovic, G., Huvet, M., Toni, T., Sheng, X., Stumpf, M. P. and Buck, M. (2010) Managing membrane stress: the phage shock protein (Psp) response, from molecular mechanisms to physiology. FEMS Microbiol. Rev., 34, 797-827.
28. Zhang, N., Joly, N., Burrows, P. C., Jovanovic, M., Wigneshweraraj, S. R. and Buck, M. (2009) The role of the conserved phenylalanine in the sigma54-interacting GAFTGA motif of bacterial enhancer binding proteins. Nucleic Acids Res., 37, 5981-5992.
29. Joly, N. and Buck, M. (2011) Single chain forms of the enhancer binding protein PspF provide insights into geometric requirements for gene activation. J. Biol. Chem., 286, 12734-12742.
30. Farrell, I. S., Toroney, R., Hazen, J. L., Mehl, R. A. and Chin, J. W. (2005) Photo-cross-linking interacting proteins with a genetically encoded benzophenone. Nat. Methods, 2, 377-384. (Pubitemid 41130984)
31. Dorman, G. and Prestwich, G. D. (1994) Benzophenone photophores in biochemistry. Biochemistry, 33, 5661-5673. (Pubitemid 24184566)
32. Lin, A. A., Sastri, V. R., Tesoro, G. and Reiser, A. (1988) On the cross-linking mechanism of benzophenone-containing polyimides. Macromolecules, 21, 1165-1169.
33. Cannon, W. V., Gallegos, M. T. and Buck, M. (2000) Isomerization of a binary sigma-promoter DNA complex by transcription activators. Nat. Struct. Biol., 7, 594-601. (Pubitemid 30445918)
34. Casaz, P. and Buck, M. (1997) Probing the assembly of transcription initiation complexes through changes in sigmaN protease sensitivity. Proc. Natl Acad. Sci. USA, 94, 12145-12150.
35. Buck, M. and Cannon, W. (1994) A simple procedure for visualising protein-nucleic acid complexes by photochemical crosslinking. Nucleic Acids Res., 22, 1119-1120. (Pubitemid 24162180)
36. Chaney, M., Grande, R., Wigneshweraraj, S. R., Cannon, W., Casaz, P., Gallegos, M. T., Schumacher, J., Jones, S.,-elderkin, S., Dago, A. E. et al. (2001) 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, 2282-2294. (Pubitemid 32843840)
37. Leach, R. N., Gell, C., Wigneshweraraj, S., Buck, M., Smith, A. and Stockley, P. G. (2006) Mapping ATP-dependent activation at a sigma54 promoter. J. Biol. Chem., 281, 33717-33726. (Pubitemid 46036750)
38. Lee, J. H. and Hoover, T. R. (1995) Protein crosslinking studies suggest that Rhizobium meliloti C4-dicarboxylic acid transport protein D, a sigma 54-dependent transcriptional activator, interacts with sigma 54 and the beta subunit of RNA polymerase. Proc. Natl Acad. Sci. USA, 92, 9702-9706.
39. Burrows, P. C., Joly, N. and Buck, M. (2010) A prehydrolysis state of an AAA+ATPase supports transcription activation of an enhancer-dependent RNA polymerase. Proc. Natl Acad. Sci. USA, 107, 9376-9381.
40. Chaney, M. and Buck, M. (1999) The sigma 54 DNA-binding domain includes a determinant of enhancer responsiveness. Mol. Microbiol., 33, 1200-1209. (Pubitemid 29433625)
41. Joly, N., Schumacher, J. and Buck, M. (2006) Heterogeneous nucleotide occupancy stimulates functionality of phage shock protein F, an AAA+transcriptional activator. J. Biol. Chem., 281, 34997-35007. (Pubitemid 46036539)
42. Werbeck, N. D., Schlee, S. and Reinstein, J. (2008) Coupling and dynamics of subunits in the hexameric AAA+chaperone Clp B. J. Mol. Biol., 378, 178-190.
43. Bordes, P., Wigneshweraraj, S. R., Chaney, M., Dago, A. E., Morett, E. and Buck, M. (2004) Communication between Esigma(54), promoter DNA and the conserved threonine residue in the GAFTGA motif of the PspF sigma-dependent activator during transcription activation. Mol. Microbiol., 54, 489-506. (Pubitemid 39388291)
44. Wigneshweraraj, S. R., Casaz, P. and Buck, M. (2002) Correlating protein footprinting with mutational analysis in the bacterial transcription factor sigma54 (sigmaN). Nucleic Acids Res., 30, 1016-1028. (Pubitemid 34679671)
45. Darst, S. A., Opalka, N., Chacon, P., Polyakov, A., Richter, C., Zhang, G. and Wriggers, W. (2002) Conformational flexibility of bacterial RNA polymerase. Proc. Natl Acad. Sci. USA, 99, 4296-4301. (Pubitemid 34285979)
46. Mekler, V., Kortkhonjia, E., Mukhopadhyay, J., Knight, J., Revyakin, A., Kapanidis, A. N., Niu, W.,-ebright, Y. W., Levy, R. and Ebright, R. H. (2002) Structural organization of bacterial RNA polymerase holoenzyme and the RNA polymerase-promoter open complex. Cell, 108, 599-614. (Pubitemid 34241422)
47. Mooney, R. A. and Landick, R. (2003) Tethering sigma70 to RNA polymerase reveals high in vivo activity of sigma factors and sigma70-dependent pausing at promoter-distal locations. Genes Dev., 17, 2839-2851. (Pubitemid 37463292)
48. Nagai, H. and Shimamoto, N. (1997) Regions of the Escherichia coli primary sigma factor sigma70 that are involved in interaction with RNA polymerase core enzyme. Genes Cells, 2, 725-734. (Pubitemid 127688616)
49. Chen, J., Darst, S. A. and Thirumalai, D. (2010) Promoter melting triggered by bacterial RNA polymerase occurs in three steps. Proc. Natl Acad. Sci. USA, 107, 12523-12528.
50. Enemark, E. J. and Joshua-Tor, L. (2006) Mechanism of DNA translocation in a replicative hexameric helicase. Nature, 442, 270-275. (Pubitemid 44114897)
51. Bowman, G. D., O'Donnell, M. and Kuriyan, J. (2004) Structural analysis of a eukaryotic sliding DNA clamp-clamp loader complex. Nature, 429, 724-730. (Pubitemid 38833117)
52. Costa, A., Ilves, I., Tamberg, N., Petojevic, T., Nogales, E., Botchan, M. R. and Berger, J. M. (2011) The structural basis for MCM2-7 helicase activation by GINS and Cdc45. Nat. Struct. Mol. Biol., 18, 471-477.
53. Lander, G. C.,-estrin, E., Matyskiela, M. E., Bashore, C., Nogales, E. and Martin, A. (2012) Complete subunit architecture of the proteasome regulatory particle. Nature, 482, 186-191.
54. Meinke, G., Bullock, P. A. and Bohm, A. (2006) Crystal structure of the simian virus 40 large T-antigen origin-binding domain. J. Virol., 80, 4304-4312.
55. Skordalakes, E. and Berger, J. M. (2003) Structure of the Rho transcription terminator: mechanism of mRNA recognition and helicase loading. Cell, 114, 135-146. (Pubitemid 36869001)
56. Story, R. M., Weber, I. T. and Steitz, T. A. (1992) The structure of the E. coli recA protein monomer and polymer. Nature, 355, 318-325.
57. Guo, Y., Lew, C. M. and Gralla, J. D. (2000) Promoter opening by sigma(54) and sigma(70) RNA polymerases: sigma factor-directed alterations in the mechanism and tightness of control. Genes Dev., 14, 2242-2255.
58. North, A. K., Weiss, D. S., Suzuki, H., Flashner, Y. and Kustu, S. (1996) Repressor forms of the enhancer-binding protein NrtC: some fail in coupling ATP hydrolysis to open complex formation by sigma 54-holoenzyme. J. Mol. Biol., 260, 317-331. (Pubitemid 26254113)
59. Chen, B., Doucleff, M., Wemmer, D. E., De Carlo, S., Huang, H. H., Nogales, E., Hoover, T. R., Kondrashkina, E., Guo, L. and Nixon, B. T. (2007) ATP ground- and transition states of bacterial enhancer binding AAA+ATPases support complex formation with their target protein, sigma54. Structure, 15, 429-440. (Pubitemid 46551727)
60. Bush, M., Ghosh, T., Tucker, N., Zhang, X. and Dixon, R. (2011) Transcriptional regulation by the dedicated nitric oxide sensor, NorR: a route towards NO detoxification. Biochem. Soc. Trans., 39, 289-293.
61. Jovanovic, M., James, E. H., Burrows, P. C., Rego, F. G., Buck, M. and Schumacher, J. (2011) Regulation of the co-evolved HrpR and HrpS AAA+proteins required for Pseudomonas syringae pathogenicity. Nat. Commun., 2, 177.
62. Sallai, L. and Tucker, P. A. (2005) Crystal structure of the central and C-terminal domain of the sigma(54)-activator Zra R. J. Struct. Biol., 151, 160-170. (Pubitemid 41074824)
63. Wikstrom, P., O'Neill, E., Ng, L. C. and Shingler, V. (2001) The regulatory N-terminal region of the aromatiC-responsive transcriptional activator DmpR constrains nucleotide-triggered multimerisation. J. Mol. Biol., 314, 971-984. (Pubitemid 34073062)
64. Joly, N. and Buck, M. (2010) Engineered interfaces of an AAA+ ATPase reveal a new nucleotide-dependent coordination mechanism. J. Biol. Chem., 285, 15178-15186.