CarD stabilizes mycobacterial open complexes via a two-tiered kinetic mechanism

Nucleic Acids Research

Volumn 43, Issue 6, 2015, Pages 3272-3285

  Rammohan, Jayan ^a   Manzano, Ana Ruiz ^a   Garner, Ashley L ^a   Stallings, Christina L ^a   Galburt, Eric A ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; BINDING PROTEIN; CARD BINDING PROTEIN; RIBOSOME RNA; RNA POLYMERASE; UNCLASSIFIED DRUG; BACTERIAL DNA; BACTERIAL RNA; DNA DIRECTED RNA POLYMERASE; ESCHERICHIA COLI PROTEIN; TRANSCRIPTION FACTOR;

ARTICLE; BACTERIAL KINETICS; BINDING AFFINITY; CONTROLLED STUDY; ENERGY TRANSFER; ESCHERICHIA COLI; GENE CONTROL; GENETIC TRANSCRIPTION; IN VIVO STUDY; MYCOBACTERIUM; MYCOBACTERIUM BOVIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; AMINO ACID SUBSTITUTION; BIOLOGICAL MODEL; CHEMISTRY; GENETICS; KINETICS; METABOLISM; SITE DIRECTED MUTAGENESIS; THERMODYNAMICS; TRANSCRIPTION INITIATION;

AMINO ACID SUBSTITUTION; BACTERIAL PROTEINS; DNA, BACTERIAL; DNA-DIRECTED RNA POLYMERASES; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; KINETICS; MODELS, BIOLOGICAL; MUTAGENESIS, SITE-DIRECTED; MYCOBACTERIUM; MYCOBACTERIUM BOVIS; MYCOBACTERIUM TUBERCULOSIS; PROMOTER REGIONS, GENETIC; RNA, BACTERIAL; RNA, RIBOSOMAL; THERMODYNAMICS; TRANSCRIPTION FACTORS; TRANSCRIPTION INITIATION, GENETIC;

EID: 84942288248     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv078     Document Type: Article

References (30)

1. Saecker, R.M., Record, M.T. Jr and deHaseth, P.L. (2011) Mechanism of bacterial transcription initiation: promoter binding, isomerization to initiation-competent open complexes, and initiation of RNA synthesis. J. Mol. Biol., 412, 754-771.
2. Rojo, F. (2001) Mechanisms of transcriptional repression. Curr. Opin. Microbiol., 4, 145-151.
3. Lee, D.J., Minchin, S.D. and Busby, S.J.W. (2012) Activating transcription in bacteria. Annu. Rev. Microbiol., 66, 125-152.
4. Kahmann, R., Rudt, F., Koch, C. and Mertens, G. (1985) G inversion in bacteriophage Mu DNA is stimulated by a site within the invertase gene and a host factor. Cell, 41, 771-780.
5. Kang, P.J. and Craig, E.A. (1990) Identifcation and characterization of a new Escherichia coli gene that is a dosage-dependent suppressor of a dnaK deletion mutation. J. Bacteriol., 172, 2055-2064.
6. Rao, L., Ross, W., Appleman, J.A., Gaal, T., Leirmo, S., Schlax, P.J., Record, M.T. and Gourse, R.L. (1994) Factor independent activation of rrnB P1. An 'extended' promoter with an upstream element that dramatically increases promoter strength. J. Mol. Biol., 235, 1421-1435.
7. Newlands, J.T., Josaitis, C.A., Ross, W. and Gourse, R.L. (1992) Both fs-dependent and factor-independent upstream activation of the rrnB P1 promoter are face of the helix dependent. Nucleic Acids Res., 20, 719-726.
8. Travers, A.A. (1980) Promoter sequence for stringent control of bacterial ribonucleic acid synthesis. J. Bacteriol., 141, 973-976.
9. Stallings, C.L., Stephanou, N.C., Chu, L., Hochschild, A., Nickels, B.E. and Glickman, M.S. (2009) CarD Is an essential regulator of rRNA transcription required for Mycobacterium tuberculosis persistence. Cell, 138, 146-159.
10. Garćia-Moreno, D., Abellón-Ruiz, J., Garćia-Heras, F., Murillo, F.J., Padmanabhan, S. and Eĺias-Arnanz, M. (2010) CdnL, a member of the large CarD-like family of bacterial proteins, is vital for Myxococcus xanthus and differs functionally from the global transcriptional regulator CarD. Nucleic Acids Res., 38, 4586-4598.
11. Yang, X.F., Goldberg, M.S., He, M., Xu, H., Blevins, J.S. and Norgard, M.V. (2008) Differential expression of a putative CarD-like transcriptional regulator, LtpA, in Borrelia burgdorferi. Infect. Immun., 76, 4439-4444.
12. Weiss, L.A., Harrison, P.G., Nickels, B.E., Glickman, M.S., Campbell, E.A., Darst, S.A. and Stallings, C.L. (2012) Interaction of CarD with RNA polymerase mediates Mycobacterium tuberculosis viability, rifampin resistance, and pathogenesis. J. Bacteriol., 194, 5621-5631.
13. Srivastava, D.B., Leon, K., Osmundson, J., Garner, A.L., Weiss, L.A., Westblade, L.F., Glickman, M.S., Landick, R., Darst, S.A., Stallings, C.L. et al. (2013) Structure and function of CarD, an essential mycobacterial transcription factor. Proc. Natl. Acad. Sci. USA, 110, 12619-12612.
14. Garner, A.L., Weiss, L.A., Manzano, A.R., Galburt, E.A. and Stallings, C.L. (2014) CarD integrates three functional modules to promote effcient transcription, antibiotic tolerance, and pathogenesis in mycobacteria. Mol. Microbiol., 93, 682-697.
15. Czyz, A., Mooney, R.A., Iaconi, A. and Landick, R. (2014) Mycobacterial RNA polymerase requires a U-tract at intrinsic terminators and Is aided by NusG at suboptimal terminators. mBio, 5, e00931.
16. Gonzalez-y-Merchand, J.A., Colston, M.J. and Cox, R.A. (1996) The rRNA operons of Mycobacterium smegmatis and Mycobacterium tuberculosis: comparison of promoter elements and of neighbouring upstream genes. Microbiology, 142, 667-674.
17. Ko, J. and Heyduk, T. (2014) Kinetics of promoter escape by bacterial RNA polymerase: effects of promoter contacts and transcription bubble collapse. Biochem. J., 463, 135-144.
18. Sullivan, J.J., Bjornson, K.P., Sowers, L.C. and deHaseth, P.L. (1997) Spectroscopic determination of open complex formation at promoters for Escherichia coli RNA polymerase. Biochemistry, 36, 8005-8012.
19. Kovacic, R.T. (1987) The 0 degree C closed complexes between Escherichia coli RNA polymerase and two promoters, T7-A3 and lacUV5. J. Biol. Chem., 262, 13654-13661.
20. Cowing, D.W., Mecsas, J., Record, M.T. and Gross, C.A. (1989) Intermediates in the formation of the open complex by RNA polymerase holoenzyme containing the sigma factor sigma 32 at the groE promoter. J. Mol. Biol., 210, 521-530.
21. Schickor, P., Metzger, W., Werel, W., Lederer, H. and Heumann, H. (1990) Topography of intermediates in transcription initiation of E. coli. EMBO J., 9, 2215-2220.
22. Cook, V.M. and deHaseth, P.L. (2007) Strand opening-defcient Escherichia coli RNA polymerase facilitates investigation of closed complexes with promoter DNA: effects of DNA sequence and temperature. J. Biol. Chem., 282, 21319-21326.
23. Westblade, L.F., Campbell, E.A., Pukhrambam, C., Padovan, J.C., Nickels, B.E., Lamour, V. and Darst, S.A. (2010) Structural basis for the bacterial transcription-repair coupling factor/RNA polymerase interaction. Nucleic Acids Res., 38, 8357-8369.
24. Fu, L.M. and Fu-Liu, C.S. (2007) The gene expression data of Mycobacterium tuberculosis based on Affymetrix gene chips provide insight into regulatory and hypothetical genes. BMC Microbiol., 7, 37-48.
25. Davis, E., Chen, J., Leon, K., Darst, S.A. and Campbell, E.A. (2015) Mycobacterial RNA polymerase forms unstable open promoter complexes that are stabilized by CarD. Nucleic Acids Res., 43, 433-445.
26. McClure, W.R. (1980) Rate-limiting steps in RNA chain initiation. Proc. Natl. Acad. Sci. USA, 77, 5634-5638.
27. Tare, P., China, A. and Nagaraja, V. (2012) Distinct and contrasting transcription initiation patterns at Mycobacterium tuberculosis promoters. PLoS ONE, 7, e43900.
28. Roy, S., Lim, H.M., Liu, M. and Adhya, S. (2004) Asynchronous basepair openings in transcription initiation: CRP enhances the rate-limiting step. EMBO J., 23, 869-875.
29. Rutherford, S.T., Villers, C.L., Lee, J.-H., Ross, W. and Gourse, R.L. (2009) Allosteric control of Escherichia coli rRNA promoter complexes by DksA. Genes Dev., 23, 236-248.
30. Panaghie, G., Aiyar, S.E., Bobb, K.L., Hayward, R.S. and de Haseth, P.L. (2000) Aromatic amino acids in region 2.3 of Escherichia coli sigma 70 participate collectively in the formation of an RNA polymerase-promoter open complex. J. Mol. Biol., 299, 1217-1230.