A novel phage-encoded transcription antiterminator acts by suppressing bacterial RNA polymerase pausing

Nucleic Acids Research

Volumn 40, Issue 9, 2012, Pages 4052-4063

  Berdygulova, Zhanna ^a   Esyunina, Daria ^b,c   Miropolskaya, Nataliya ^b   Mukhamedyarov, Damir ^a   Kuznedelov, Konstantin ^a   Nickels, Bryce E ^a,d   Severinov, Konstantin ^b   Kulbachinskiy, Andrey ^b   Minakhin, Leonid ^a  

^a RUTGERS UNIVERSITY   (United States)

^b INSTITUTE OF MOLECULAR GENETICS   (Russian Federation)

^c MOSCOW STATE UNIVERSITY   (Russian Federation)

^d RUTGERS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN; MICROORGANISM PROTEIN; PROTEIN GP39; PROTEIN NUSA; PROTEIN Q; RNA; RNA POLYMERASE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIOPHAGE LAMBDA; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME MECHANISM; ENZYME REGULATION; GENETIC CODE; IN VITRO STUDY; NONHUMAN; PEPTIDE MAPPING; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; RNA TRANSLATION; THERMUS THERMOPHILUS; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; TRANSCRIPTION TERMINATION;

BACTERIAL PROTEINS; BACTERIOPHAGES; BINDING SITES; DNA-DIRECTED RNA POLYMERASES; MODELS, MOLECULAR; OLIGONUCLEOTIDES; PROTEIN INTERACTION DOMAINS AND MOTIFS; RNA; TERMINATOR REGIONS, GENETIC; THERMUS THERMOPHILUS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TRANSCRIPTIONAL ELONGATION FACTORS; VIRAL PROTEINS;

BACTERIA (MICROORGANISMS); THERMUS THERMOPHILUS;

EID: 84861366862     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkr1285     Document Type: Article

References (42)

1. Roberts, J.W., Shankar, S. and Filter, J.J. (2008) RNA polymerase elongation factors. Annu. Rev. Microbiol., 62, 211-233.
2. Peters, J.M., Vangeloff, A.D. and Landick, R. (2011) Bacterial transcription terminators: The RNA 3'-end chronicles. J. Mol. Biol., 412, 793-813.
3. Epshtein, V., Cardinale, C.J., Ruckenstein, A.E., Borukhov, S. and Nudler, E. (2007) An allosteric path to transcription termination. Mol. Cell, 28, 991-1001. (Pubitemid 350297020)
4. Santangelo, T.J. and Artsimovitch, I. (2011) Termination and antitermination: RNA polymerase runs a stop sign. Nat. Rev. Microbiol., 9, 319-329.
5. Ha, K.S., Toulokhonov, I., Vassylyev, D.G. and Landick, R. (2010) The NusA N-terminal domain is necessary and sufficient for enhancement of transcriptional pausing via interaction with the RNA exit channel of RNA polymerase. J. Mol. Biol., 401, 708-725.
6. Herbert, K.M., Zhou, J., Mooney, R.A., Porta, A.L., Landick, R. and Block, S.M. (2010) E. coli NusG inhibits backtracking and accelerates pause-free transcription by promoting forward translocation of RNA polymerase. J. Mol. Biol., 399, 17-30.
7. Artsimovitch, I. and Landick, R. (2002) The transcriptional regulator RfaH stimulates RNA chain synthesis after recruitment to elongation complexes by the exposed nontemplate DNA strand. Cell, 109, 193-203. (Pubitemid 34518258)
8. Svetlov, V., Belogurov, G.A., Shabrova, E., Vassylyev, D.G. and Artsimovitch, I. (2007) Allosteric control of the RNA polymerase by the elongation factor RfaH. Nucleic Acids Res., 35, 5694-5705. (Pubitemid 47506287)
9. Gusarov, I. and Nudler, E. (2001) Control of intrinsic transcription termination by N and NusA: the basic mechanisms. Cell, 107, 437-449. (Pubitemid 33152780)
10. Rees, W.A., Weitzel, S.E., Das, A. and von Hippel, P.H. (1997) Regulation of the elongation-termination decision at intrinsic terminators by antitermination protein N of phage lambda. J. Mol. Biol., 273, 797-813. (Pubitemid 27493720)
11. Shankar, S., Hatoum, A. and Roberts, J.W. (2007) A transcription antiterminator constructs a NusA-dependent shield to the emerging transcript. Mol. Cell, 27, 914-927. (Pubitemid 47488186)
12. Deighan, P., Diez, C.M., Leibman, M., Hochschild, A. and Nickels, B.E. (2008) The bacteriophage lambda Q antiterminator protein contacts the beta-flap domain of RNA polymerase. Proc. Natl Acad. Sci. USA, 105, 15305-15310.
13. Yang, X., Molimau, S., Doherty, G.P., Johnston, E.B., Marles-Wright, J., Rothnagel, R., Hankamer, B., Lewis, R.J. and Lewis, P.J. (2009) The structure of bacterial RNA polymerase in complex with the essential transcription elongation factor NusA. EMBO Rep., 10, 997-1002.
14. Mooney, R.A., Schweimer, K., Rosch, P., Gottesman, M. and Landick, R. (2009) Two structuraly independent domains of E. coli NusG create regulatory plastisity via distinct interactions with RNA polymerase and regulators. J. Mol. Biol., 391, 341-358.
15. Sevostyanova, A., Svetlov, V., Vassylyev, D.G. and Artsimovitch, I. (2008) The elongation factor RfaH and the initiation factor sigma bind to the same site on the transcription elongation complex. Proc. Natl Acad. Sci. USA, 105, 865-870. (Pubitemid 351282047)
16. Sevostyanova, A., Belogurov, G.A., Mooney, R.A., Landick, R. and Artsimovitch, I. (2011) The beta subunit gate loop is required for RNA polymerase modification by RfaH and NusG. Mol. Cell, 43, 253-262.
17. Yuzenkova, Y., Zenkin, N. and Severinov, K. (2008) Mapping of RNA polymerase residues that interact with bacteriophage Xp10 transcription antitermination factor p7. J. Mol. Biol., 375, 29-35. (Pubitemid 350160702)
18. Zhang, G., Campbell, E.A., Minakhin, L., Richter, C., Severinov, K. and Darst, S.A. (1999) Crystal structure of Thermus aquaticus core RNA polymerase at 3.3 A resolution. Cell, 98, 811-824.
19. Vassylyev, D.G., Sekine, S., Laptenko, O., Lee, J., Vassylyeva, M.N., Borukhov, S. and Yokoyama, S. (2002) Crystal structure of a bacterial RNA polymerase holoenzyme at 2.6 A resolution. Nature, 417, 712-719. (Pubitemid 34640620)
20. Murakami, K.S., Masuda, S., Campbell, E.A., Muzzin, O. and Darst, S.A. (2002) Structural basis of transcription initiation: an RNA polymerase holoenzyme-DNA complex. Science, 296, 1285-1290. (Pubitemid 34522778)
21. Vassylyev, D.G., Vassylyeva, M.N., Perederina, A., Tahirov, T.H. and Artsimovitch, I. (2007) Structural basis for transcription elongation by bacterial RNA polymerase. Nature, 448, 157-162. (Pubitemid 47067370)
22. Berdygulova, Z., Westblade, L.F., Florens, L., Koonin, E.V., Chait, B.T., Ramanculov, E., Washburn, M.P., Darst, S.A., Severinov, K. and Minakhin, L. (2011) Temporal regulation of gene expression of the Thermus thermophilus bacteriophage P23-45. J. Mol. Biol., 405, 125-142.
23. Sevostyanova, A., Djordjevic, M., Kuznedelov, K., Naryshkina, T., Gelfand, M.S., Severinov, K. and Minakhin, L. (2007) Temporal regulation of viral transcription during development of Thermus thermophilus bacteriophage phiYS40. J. Mol. Biol., 366, 420-435. (Pubitemid 46136208)
24. Barinova, N., Kuznedelov, K., Severinov, K. and Kulbachinskiy, A. (2008) Structural modules of RNA polymerase required for transcription from promoters containing downstream basal promoter element GGGA. J. Biol. Chem., 283, 22482-22489.
25. Kuznedelov, K., Minakhin, L. and Severinov, K. (2003) Preparation and characterization of recombinant Thermus aquaticus RNA polymerase. Methods Enzymol., 370, 94-108. (Pubitemid 37542772)
26. Minakhin, L., Nechaev, S., Campbell, E.A. and Severinov, K. (2001) Recombinant Thermus aquaticus RNA polymerase, a new tool for structure-based analysis of transcription. J. Bacteriol., 183, 71-76. (Pubitemid 32003109)
27. Deaconescu, A.M., Chambers, A.L., Smith, A.J., Nickels, B.E., Hochschild, A., Savery, N.J. and Darst, S.A. (2006) Structural basis for bacterial transcription-coupled DNA repair. Cell, 124, 507-520. (Pubitemid 43199437)
28. Nickels, B.E. (2009) Genetic assays to define and characterize protein-protein interactions involved in gene regulation. Methods, 47, 53-62.
29. Thibodeau, S.A., Fang, R. and Joung, J.K. (2004) High-throughput beta-galactosidase assay for bacterial cell-based reporter systems. Biotechniques, 36, 410-415. (Pubitemid 38299055)
30. Miropolskaya, N., Artsimovitch, I., Klimasauskas, S., Nikiforov, V. and Kulbachinskiy, A. (2009) Allosteric control of catalysis by the F loop of RNA polymerase. Proc. Natl Acad. Sci. USA, 106, 18942-18947.
31. Dove, S.L. and Hochschild, A. (2004) A bacterial two-hybrid system based on transcription activation. Methods Mol. Biol., 261, 231-246.
32. Yarnell, W.S. and Roberts, J.W. (1999) Mechanism of intrinsic transcription termination and antitermination. Science, 284, 611-615. (Pubitemid 29289580)
33. Sevostyanova, A. and Artsimovitch, I. (2010) Functional analysis of Thermus thermophilus transcription factor NusG. Nucleic Acids Res., 38, 7432-7445.
34. Ring, B.Z., Yarnell, W.S. and Roberts, J.W. (1996) Function of E. coli RNA polymerase sigma factor sigma 70 in promoter-proximal pausing. Cell, 86, 485-493. (Pubitemid 26272088)
35. Perdue, S.A. and Roberts, J.W. (2011) Sigma(70)-dependent transcription pausing in Escherichia coli. J. Mol. Biol., 412, 782-792.
36. Toulokhonov, I., Artsimovitch, I. and Landick, R. (2001) Allosteric control of RNA polymerase by a site that contacts nascent RNA hairpins. Science, 292, 730-733. (Pubitemid 32385544)
37. Toulokhonov, I. and Landick, R. (2003) The flap domain is required for pause RNA hairpin inhibition of catalysis by RNA polymerase and can modulate intrinsic termination. Mol. Cell, 12, 1125-1136. (Pubitemid 37487923)
38. Landick, R. (2006) The regulatory roles and mechanism of transcriptional pausing. Biochem. Soc. Trans., 34, 1062-1066. (Pubitemid 46768989)
39. Sydow, J.F., Brueckner, F., Cheung, A.C., Damsma, G.E., Dengl, S., Lehmann, E., Vassylyev, D. and Cramer, P. (2009) Structural basis of transcription: mismatch-specific fidelity mechanisms and paused RNA polymerase II with frayed RNA. Mol. Cell, 34, 710-721.
40. Marr, M.T. and Roberts, J.W. (2000) Function of transcription cleavage factors GreA and GreB at a regulatory pause site. Mol. Cell, 6, 1275-1285. (Pubitemid 32045921)
41. Nechaev, S., Yuzenkova, Y., Niedziela-Majka, A., Heyduk, T. and Severinov, K. (2002) A novel bacteriophage-encoded RNA polymerase binding protein inhibits transcription initiation and abolishes transcription termination by host RNA polymerase. J. Mol. Biol., 320, 11-22. (Pubitemid 34722231)
42. Zhilina, E., Esyunina, D., Brodolin, K. and Kulbachinskiy, A. (2011) Structural transitions in the transcription elongation complexes of bacterial RNA polymerase during sigma-dependent pausing. Nucl. Acids Res., December 2 (doi:10.1093/nar/gkr1158; epub ahead of print).