CBR antimicrobials alter coupling between the bridge helix and the β subunit in RNA polymerase

Nature Communications

Volumn 5, Issue , 2014, Pages

  Malinen, Anssi M ^a   Nandymazumdar, Monali ^b   Turtola, Matti ^a   Malmi, Henri ^a   Grocholski, Thadee ^a   Artsimovitch, Irina ^b   Belogurov, Georgiy A ^a  

^a UNIVERSITY OF TURKU   (Finland)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIINFECTIVE AGENT; N HYDROXY N' PHENYL 3 TRIFLUOROMETHYL BENZAMIDINE; RNA POLYMERASE BETA SUBUNIT; STREPTOLYDIGIN; TAGETITOXIN; UNCLASSIFIED DRUG; AMIDINE; BACTERIAL PROTEIN; CBR 703; DNA DIRECTED RNA POLYMERASE; HYDROXYLAMINE; PROTEIN BINDING; PROTEIN SUBUNIT;

AMINO ACID; ANTIMICROBIAL ACTIVITY; BACTERIUM; CATALYSIS; ENZYME ACTIVITY; INHIBITOR; MODEL VALIDATION; RNA;

AMINO ACID SUBSTITUTION; ARTICLE; BINDING AFFINITY; BINDING SITE; CATALYSIS; COMPUTER MODEL; ISOMERIZATION; MOLECULAR DOCKING; RNA CONFORMATION; RNA STRUCTURE; RNA TRANSCRIPTION; RNA TRANSPORT; TRANSCRIPTION ELONGATION; BIOCATALYSIS; CHEMICAL STRUCTURE; CHEMISTRY; DRUG EFFECTS; GENETICS; KINETICS; METABOLISM; PROTEIN SECONDARY STRUCTURE; PROTEIN SUBUNIT; PROTEIN TERTIARY STRUCTURE;

AMIDINES; AMINO ACID SUBSTITUTION; ANTI-INFECTIVE AGENTS; BACTERIAL PROTEINS; BIOCATALYSIS; DNA-DIRECTED RNA POLYMERASES; HYDROXYLAMINES; KINETICS; MODELS, MOLECULAR; MOLECULAR STRUCTURE; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS;

EID: 84896803701     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms4408     Document Type: Article

References (64)

1. Werner, F. & Grohmann, D. Evolution of multisubunit RNA polymerases in the three domains of life. Nat. Rev. Microbiol. 9, 85-98 (2011).
2. Svetlov, V. & Nudler, E. Basic mechanism of transcription by RNA polymerase II. Biochim. Biophys. Acta Gene Regul. Mech. 1829, 20-28 (2013).
3. Ho, M. X., Hudson, B. P., Das, K., Arnold, E. & Ebright, R. H. Structures of RNA polymerase-antibiotic complexes. Curr. Opin. Struct. Biol. 19, 715-723 (2009).
4. Vassylyev, D. G. et al. Structural basis for substrate loading in bacterial RNA polymerase. Nature 448, 163-168 (2007). (Pubitemid 47067369)
5. Wang, D., Bushnell, D. A., Westover, K. D., Kaplan, C. D. & Kornberg, R. D. Structural basis of transcription: role of the trigger loop in substrate specificity and catalysis. Cell 127, 941-954 (2006). (Pubitemid 44792264)
6. Malinen, A. M. et al. Active site opening and closure control translocation of multisubunit RNA polymerase. Nucleic Acids Res. 40, 7442-7451 (2012).
7. Ederth, J., Mooney, R. A., Isaksson, L. A. & Landick, R. Functional interplay between the jaw domain of bacterial RNA polymerase and allele-specific residues in the product RNA-binding pocket. J. Mol. Biol. 356, 1163-1179 (2006). (Pubitemid 43199921)
8. Artsimovitch, I. & Landick, R. Pausing by bacterial RNA polymerase is mediated by mechanistically distinct classes of signals. Proc. Natl Acad. Sci. USA 97, 7090-7095 (2000). (Pubitemid 30431422)
9. Neuman, K. C., Abbondanzieri, E. A., Landick, R., Gelles, J. & Block, S. M. Ubiquitous transcriptional pausing is independent of RNA polymerase backtracking. Cell 115, 437-447 (2003). (Pubitemid 37456806)
10. Von Hippel, P. H. & Pasman, Z. Reaction pathways in transcript elongation. Biophys. Chem. 101-102, 401-423 (2002). (Pubitemid 35462062)
11. Proshkin, S., Rahmouni, A. R., Mironov, A. & Nudler, E. Cooperation between translating ribosomes and RNA polymerase in transcription elongation. Science 328, 504-508 (2010).
12. Landick, R., Carey, J. & Yanofsky, C. Translation activates the paused transcription complex and restores transcription of the trp operon leader region. Proc. Natl Acad. Sci. USA 82, 4663-4667 (1985). (Pubitemid 16239623)
13. Roberts, J. W. et al. Antitermination by bacteriophage lambda Q protein. Cold Spring Harb. Symp. Quant. Biol. 63, 319-325 (1998).
14. Artsimovitch, I. & Landick, R. The transcriptional regulator RfaH stimulates RNA chain synthesis after recruitment to elongation complexes by the exposed nontemplate DNA strand. Cell 109, 193-203 (2002). (Pubitemid 34518258)
15. Nag, A., Narsinh, K. & Martinson, H. G. The poly(A)-dependent transcriptional pause is mediated by CPSF acting on the body of the polymerase. Nat. Struct. Mol. Biol. 14, 662-669 (2007). (Pubitemid 47037062)
16. Miropolskaya, N., Artsimovitch, I., Klimasauskas, S., Nikiforov, V. & Kulbachinskiy, A. Allosteric control of catalysis by the F loop of RNA polymerase. Proc. Natl Acad. Sci. USA 106, 18942-18947 (2009).
17. Toulokhonov, I., Zhang, J., Palangat, M. & Landick, R. A central role of the RNA polymerase trigger loop in active-site rearrangement during transcriptional pausing. Mol. Cell 27, 406-419 (2007). (Pubitemid 47126936)
18. Sydow, J. F. et al. Structural basis of transcription: mismatch-specific fidelity mechanisms and paused RNA polymerase II with frayed RNA. Mol. Cell 34, 710-721 (2009).
19. Sevostyanova, A., Belogurov, G. A., Mooney, R. A., Landick, R. & Artsimovitch, I. The beta subunit gate loop is required for RNA polymerase modification by RfaH and NusG. Mol. Cell 43, 253-262 (2011).
20. Weixlbaumer, A., Leon, K., Landick, R. & Darst, S. A. Structural basis of transcriptional pausing in bacteria. Cell 152, 431-441 (2013).
21. Greive, S. J. & von Hippel, P. H. Thinking quantitatively about transcriptional regulation. Nat. Rev. Mol. Cell Biol. 6, 221-232 (2005). (Pubitemid 40314923)
22. Artsimovitch, I., Chu, C., Lynch, A. S. & Landick, R. A new class of bacterial RNA polymerase inhibitor affects nucleotide addition. Science 302, 650-654 (2003). (Pubitemid 37310922)
23. Villain-Guillot, P., Gualtieri, M., Bastide, L. & Leonetti, J. P. In vitro activities of different inhibitors of bacterial transcription against Staphylococcus epidermidis biofilm. Antimicrob. Agents Chemother. 51, 3117-3121 (2007). (Pubitemid 350067517)
24. Svetlov, V., Belogurov, G. A., Shabrova, E., Vassylyev, D. G. & Artsimovitch, I. Allosteric control of the RNA polymerase by the elongation factor RfaH. Nucleic Acids Res. 35, 5694-5705 (2007). (Pubitemid 47506287)
25. Nedialkov, Y. A. et al. The RNA polymerase bridge helix YFI motif in catalysis, fidelity and translocation. Biochim. Biophys. Acta 1829, 187-98 (2013).
26. Landick, R., Stewart, J. & Lee, D. N. Amino acid changes in conserved regions of the beta-subunit of Escherichia coli RNA polymerase alter transcription pausing and termination. Genes Dev. 4, 1623-1636 (1990).
27. Jovanovic, M. et al. Activity map of the Escherichia coli RNA polymerase bridge helix. J. Biol. Chem. 286, 14469-14479 (2011).
28. Temiakov, D. et al. Structural basis of transcription inhibition by antibiotic streptolydigin. Mol. Cell 19, 655-666 (2005). (Pubitemid 41219441)
29. Nedialkov, Y. A., Gong, X. Q., Yamaguchi, Y., Handa, H. & Burton, Z. F. Assay of transient state kinetics of RNA polymerase II elongation. Methods Enzymol. 371, 252-264 (2003). (Pubitemid 37542734)
30. Holmes, S. F., Foster, J. E. & Erie, D. A. Kinetics of multisubunit RNA polymerases: experimental methods and data analysis. Methods Enzymol. 371, 71-81 (2003). (Pubitemid 37542721)
31. Artsimovitch, I. et al. Tagetitoxin inhibits RNA polymerase through trapping of the trigger loop. J. Biol. Chem. 286, 40395-40400 (2011).
32. Tuske, S. et al. Inhibition of bacterial RNA polymerase by streptolydigin: stabilization of a straight-bridge-helix active-center conformation. Cell 122, 541-552 (2005). (Pubitemid 41191153)
33. Landick, R., Wang, D. & Chan, C. L. Quantitative analysis of transcriptional pausing by Escherichia coli RNA polymerase: his leader pause site as paradigm. Methods Enzymol. 274, 334-353 (1996). (Pubitemid 26353089)
34. Trott, O. & Olson, A. J. AutoDock Vina: improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. J. Comput. Chem. 31, 455-461 (2010).
35. Jones, G., Willett, P. & Glen, R. C. Molecular recognition of receptor sites using a genetic algorithm with a description of desolvation. J. Mol. Biol. 245, 43-53 (1995).
36. Jones, G., Willett, P., Glen, R. C., Leach, A. R. & Taylor, R. Development and validation of a genetic algorithm for flexible docking. J. Mol. Biol. 267, 727-748 (1997). (Pubitemid 27170693)
37. Murakami, K. S. X-ray crystal structure of Escherichia coli RNA polymerase s70 holoenzyme. J. Biol. Chem. 288, 9126-9134 (2013).
38. Herbert, K. M. et al. Sequence-resolved detection of pausing by single RNA polymerase molecules. Cell 125, 1083-1094 (2006). (Pubitemid 43866198)
39. Weinzierl, R. O. The nucleotide addition cycle of RNA polymerase is controlled by two molecular hinges in the Bridge Helix domain. BMC Biol. 8, 134 (2010).
40. Hein, P. P. & Landick, R. The bridge helix coordinates movements of modules in RNA polymerase. BMC Biol. 8, 141 (2010).
41. Brueckner, F. & Cramer, P. Structural basis of transcription inhibition by alphaamanitin and implications for RNA polymerase II translocation. Nat. Struct. Mol. Biol. 15, 811-818 (2008).
42. Heikinheimo, P. et al. A site-directed mutagenesis study of Saccharomyces cerevisiae pyrophosphatase. Functional conservation of the active site of soluble inorganic pyrophosphatases. Eur. J. Biochem. 239, 138-143 (1996). (Pubitemid 26228151)
43. Belogurov, G. A. et al. Structural basis for converting a general transcription factor into an operon-specific virulence regulator. Mol. Cell 26, 117-129 (2007). (Pubitemid 46553793)
44. Komissarova, N., Kireeva, M. L., Becker, J., Sidorenkov, I. & Kashlev, M. Engineering of elongation complexes of bacterial and yeast RNA polymerases. Methods Enzymol. 371, 233-251 (2003). (Pubitemid 37542733)
45. Abramoff, M. D., Magalhaes, P. J. & Ram, S. J. Image processing with ImageJ. Biophotonics Int. 11, 36-42 (2004).
46. Brooks, B. R. et al. CHARMM: a program for macromolecular energy, minimization, and dynamics calculations. J. Comput. Chem. 4, 187-217 (1983).
47. Sanner, M. F. Python: a programming language for software integration and development. J. Mol. Graph. Model. 17, 57-61 (1999). (Pubitemid 30029318)
48. Hendlich, M., Rippmann, F. & Barnickel, G. LIGSITE: automatic and efficient detection of potential small molecule-binding sites in proteins. J. Mol. Graph. Model. 15, 389 (1997).
49. Johnson, K. A. Fitting enzyme kinetic data with KinTek Global Kinetic Explorer. Methods Enzymol. 467, 601-626 (2009).
50. Bae, B. et al. Phage T7 Gp2 inhibition of Escherichia coli RNA polymerase involves misappropriation of s70 domain 1.1. Proc. Natl Acad. Sci. USA 110, 19772-19777 (2013).
51. Zuo, Y., Wang, Y. & Steitz, T. A. The mechanism of E. coli RNA polymerase regulation by ppGpp is suggested by the structure of their complex. Mol. Cell 50, 430-436 (2013).
52. Opalka, N. et al. Complete structural model of Escherichia coli RNA polymerase from a hybrid approach. PLoS Biol. 8, e1000483 (2010).
53. Santangelo, T. J. & Artsimovitch, I. Termination and antitermination: RNA polymerase runs a stop sign. Nat. Rev. Microbiol. 9, 319-329 (2011).
54. Toulokhonov, I., Artsimovitch, I. & Landick, R. Allosteric control of RNA polymerase by a site that contacts nascent RNA hairpins. Science 292, 730-733 (2001). (Pubitemid 32385544)
55. Ha, K. S., Toulokhonov, I., Vassylyev, D. G. & Landick, R. 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 (2010).
56. Bochkareva, A., Yuzenkova, Y., Tadigotla, V. R. & Zenkin, N. Factorindependent transcription pausing caused by recognition of the RNA-DNA hybrid sequence. EMBO J. 31, 630-639 (2012).
57. Vassylyev, D. G., Vassylyeva, M. N., Perederina, A., Tahirov, T. H. & Artsimovitch, I. Structural basis for transcription elongation by bacterial RNA polymerase. Nature 448, 157-162 (2007). (Pubitemid 47067370)
58. Zhang, Y. et al. Structural basis of transcription initiation. Science 338, 1076-1080 (2012).
59. Campbell, E. A. et al. Structural mechanism for rifampicin inhibition of bacterial RNA polymerase. Cell 104, 901-912 (2001). (Pubitemid 32289282)
60. Artsimovitch, I. et al. Allosteric modulation of the RNA polymerase catalytic reaction is an essential component of transcription control by rifamycins. Cell 122, 351-363 (2005). (Pubitemid 41127138)
61. Mukhopadhyay, J. et al. The RNA polymerase ''switch region'' is a target for inhibitors. Cell 135, 295-307 (2008).
62. Srivastava, A. et al. New target for inhibition of bacterial RNA polymerase: 'switch region'. Curr. Opin. Microbiol. 14, 532-543 (2011).
63. Chakraborty, A. et al. Opening and closing of the bacterial RNA polymerase clamp. Science 337, 591-595 (2012).
64. Belogurov, G. A. et al. Transcription inactivation through local refolding of the RNA polymerase structure. Nature 457, 332-335 (2009).