Molecular insights into the mechanism of phenotypic tolerance to rifampicin conferred on mycobacterial RNA polymerase by MsRbpA

Microbiology

Volumn 157, Issue 7, 2011, Pages 2056-2071

  Dey, Abhinav ^a   Verma, Amit Kumar ^a   Chatterji, Dipankar ^a  

^a INDIAN INSTITUTE OF SCIENCE   (India)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; BACTERIAL PROTEIN RBPA; BACTERIAL RNA; RIFAMPICIN; RNA POLYMERASE; UNCLASSIFIED DRUG;

ARTICLE; BETA CHAIN; BINDING AFFINITY; BINDING SITE; BIOLOGICAL ACTIVITY; CONTROLLED STUDY; MYCOBACTERIUM SMEGMATIS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; RNA SYNTHESIS; TRANSCRIPTION INITIATION; TRANSCRIPTION TERMINATION;

AMINO ACID SEQUENCE; ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; BINDING SITES; DNA-DIRECTED RNA POLYMERASES; MASS SPECTROMETRY; MYCOBACTERIUM SMEGMATIS; PROTEIN BINDING; PROTEIN SUBUNITS; RIFAMPIN; RNA-BINDING PROTEINS; SEQUENCE ALIGNMENT; SPECTROMETRY, FLUORESCENCE; SURFACE PLASMON RESONANCE; TRANSCRIPTION, GENETIC;

MYCOBACTERIUM SMEGMATIS;

EID: 79960041820     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.047480-0     Document Type: Article

References (39)

1. Artsimovitch, I., Svetlov, V., Anthony, L., Burgess, R. R. & Landick, R. (2000). RNA polymerases from Bacillus subtilis and Escherichia coli differ in recognition signal in vitro. J Bacteriol 182, 6027-6035.
2. Artsimovitch, I., Vassylyeva, M. N., Svetlov, D., Svetlov, V., Perederina, A., Igarashi, N., Matsugaki, N., Wakatsuki, S., Tahirov, T. H. & Vassylyev, D. G. (2005). Allosteric modulation of the RNA polymerase catalytic reaction is an essential component of transcription control by rifamycins. Cell 122, 351-363.
3. Bandwar, R. P., Tang, G. Q. & Patel, S. S. (2006). Sequential release of promoter contacts during transcription initiation to elongation transition. J Mol Biol 360, 466-483.
4. Bhat, J., Rane, R., Solapure, S. M., Sarkar, D., Sharma, U., Harish, M. N., Lamb, S., Plant, D., Alcock, P. & other authors (2006). Highthroughput screening of RNA polymerase inhibitors using a fluorescent UTP analog. J Biomol Screen 11, 968-976.
5. Calleja, C., Pascussi, J. M., Mani, J. C., Maurel, P. & Vilarem, M. J. (1998). The antibiotic rifampicin is a nonsteroidal ligand and activator of the human glucocorticoid receptor. Nat Med 4, 92-96.
6. Campbell, E. A., Korzheva, N., Mustaev, A., Murakami, K., Nair, S., Goldfarb, A. & Darst, S. A. (2001). Structural mechanism for rifampicin inhibition of bacterial RNA polymerase. Cell 104, 901-912.
7. Cantor, C. R. & Schimmel, P. R. (1980). Biophysical Chemistry, pp. 433-463. San Francisco: Freeman.
8. Carpousis, A. J. & Gralla, J. D. (1985). Interaction of RNA polymerase with lacUV5 promoter DNA during mRNA initiation and elongation. Footprinting, methylation, and rifampicin-sensitivity changes accompanying transcription initiation. J Mol Biol 183, 165-177.
9. Chatterji, D. & Gopal, V. (1996). Fluorescence spectroscopy analysis of active and regulatory sites of RNA polymerase. Methods Enzymol 274, 456-478.
10. Dey, A., Verma, A. K. & Chatterji, D. (2010). Role of an RNA polymerase interacting protein, MsRbpA, from Mycobacterium smegmatis in phenotypic tolerance to rifampicin. Microbiology 156, 873-883.
11. Flåtten, I., Morigen & Skarstad, K. (2009). DnaA protein interacts with RNA polymerase and partially protects it from the effect of rifampicin. Mol Microbiol 71, 1018-1030.
12. Fö rster, T. (1948). Zwischenmolekulare Energiewanderung und Fluoreszenz. Ann. Physiol (Leipzig) 437, 55-75.
13. Gentry, D. R. & Burgess, R. R. (1993). Cross-linking of Escherichia coli RNA polymerase subunits: identification of b9 as the binding site of v. Biochemistry 32, 11224-11227.
14. Hinkle, D. C., Mangel, W. F. & Chamberlin, M. J. (1972). Studies of the binding of Escherichia coli RNA polymerase to DNA. IV. The effect of rifampicin on binding and on RNA chain initiation. J Mol Biol 70, 209-220.
15. Jain, V., Sujatha, S., Ojha, A. K. & Chatterji, D. (2005). Identification and characterization of rel promoter element of Mycobacterium tuberculosis. Gene 351, 149-157.
16. Jin, D. J. & Gross, C. A. (1988). Mapping and sequencing of mutations in the Escherichia coli rpoB gene that lead to rifampicin resistance. J Mol Biol 202, 45-58.
17. Kumar, K. P. & Chatterji, D. (1990). Resonance energy transfer study on the proximity relationship between the GTP binding site and the rifampicin binding site of Escherichia coli RNA polymerase. Biochemistry 29, 317-322.
18. Kumar, K. P., Reddy, P. S. & Chatterji, D. (1992). Proximity relationship between the active site of Escherichia coli RNA polymerase and rifampicin binding domain: a resonance energytransfer study. Biochemistry 31, 7519-7526.
19. Lakowicz, J. R. (1983). Principles of Fluorescence Spectroscopy, pp. 303-339. New York: Plenum Press.
20. Lee, S. J. & Gralla, J. D. (2004). Osmo-regulation of bacterial transcription via poised RNA polymerase. Mol Cell 14, 153-162.
21. Lisitsyn, N. A., Sverdlov, E. D., Moiseyeva, E. P., Danilevskaya, O. N. & Nikiforov, V. G. (1984). Mutation to rifampicin resistance at the beginning of the RNA polymerase beta subunit gene in Escherichia coli. Mol Gen Genet 196, 173-174.
22. McClure, W. R. & Cech, C. L. (1978). On the mechanism of rifampicin inhibition of RNA synthesis. J Biol Chem 253, 8949-8956.
23. Mukherjee, R. & Chatterji, D. (2008). Stationary phase induced alterations in mycobacterial RNA polymerase assembly: a cue to its phenotypic resistance towards rifampicin. Biochem Biophys Res Commun 369, 899-904.
24. Newell, K. V., Thomas, D. P., Brekasis, D. & Paget, M. S. B. (2006). The RNA polymerase-binding protein RbpA confers basal levels of rifampicin resistance on Streptomyces coelicolor. Mol Microbiol 60, 687-696.
25. Nudler, E. (2009). RNA polymerase active center: the molecular engine of transcription. Annu Rev Biochem 78, 335-361.
26. Opalka, N., Brown, J., Lane, W. J., Twist, K. A., Landick, R., Asturias, F. J. & Darst, S. A. (2010). Complete structural model of Escherichia coli RNA polymerase from a hybrid approach. PLoS Biol 14, 8.
27. Rabussay, D. & Zillig, W. (1969). A rifampicin resistent RNApolymerase from E. coli altered in the beta-subunit. FEBS Lett 5, 104-106.
28. Stryer, L. (1978). Fluorescence energy transfer as a spectroscopic ruler. Annu Rev Biochem 47, 819-846.
29. Topal, M. D. & Fresco, J. R. (1980). Fluorescence of terbium ion- nucleic acid complexes: a sensitive specific probe for unpaired residues in nucleic acids. Biochemistry 19, 5531-5537.
30. Tyagi, S. C. & Wu, F. Y.-H. (1987). Synthesis and characterization of fluorescent dinucleotide substrate for the DNA-dependent RNA polymerase from Escherichia coli. J Biol Chem 262, 10684-10688.
31. We{ogonek}grzyn, A., Szalewska-Pałasz, A., Błaszczak, A., Liberek, K. and We grzyn, G. (1998). Differential inhibition of transcription from s70- and s32-dependent promoters by rifampicin. FEBS Lett 440, 172-174.
32. Wehrli, W., Handschin, J. & Wunderli, W. (1976). RNA Polymerase, pp. 397-412. Edited by M. J. Chamberlin & R. Losick. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
33. Wichelhaus, T., Schä fer, V., Brade, V. and Bö ddinghaus, B. (2001). Differential effect of rpoB mutations on antibacterial activities of rifampicin and KRM-1648 against Staphylococcus aureus. J Antimicrob Chemother 47, 153-156.
34. Williams, D. L., Spring, L., Collins, L., Miller, L. P., Heifets, L. B., Gangadharam, P. R. & Gillis, T. P. (1998). Contribution of rpoB mutations to development of rifamycin cross-resistance in Mycobacterium tuberculosis. Antimicrob Agents Chemother 42, 1853-1857.
35. Wyss, E. & Wehrli, W. (1976). The use of dextran-coated charcoal for kinetic measurements: interaction between rifampicin and DNAdependent RNA polymerase of Escherichia coli. Anal Biochem 70, 547-553.
36. Xu, M., Zhou, Y. N., Goldstein, B. P. & Jin, D. J. (2005). Crossresistance of Escherichia coli RNA polymerases conferring rifampin resistance to different antibiotics. J Bacteriol 187, 2783-2792.
37. Yarbrough, L. R., Wu, F. Y. & Wu, C. W. (1976). Molecular mechanism of the rifampicin-RNA polymerase interaction. Biochemistry 15, 2669-2676.
38. Yarbrough, L. R., Schlageck, J. G. & Baughman, M. (1979). Synthesis and properties of fluorescent nucleotide substrates for DNAdependent RNA polymerases. J Biol Chem 254, 12069-12073.
39. Zenkin, N., Kulbachinskiy, A., Bass, I. & Nikiforov, V. (2005). Different rifampin sensitivities of Escherichia coli and Mycobacterium tuberculosis RNA polymerases are not explained by the difference in the b-subunit rifampin regions I and II. Antimicrob Agents Chemother 49, 1587-1590.