Novel mechanism of gene regulation: The protein Rv1222 of Mycobacterium tuberculosis inhibits transcription by anchoring the RNA polymerase onto DNA

Nucleic Acids Research

Volumn 43, Issue 12, 2015, Pages 5855-5867

  Rudra, Paulami ^a   Prajapati, Ranjit Kumar ^a   Banerjee, Rajdeep ^a   Sengupta, Shreya ^a   Mukhopadhyay, Jayanta ^a  

^a BOSE INSTITUTE   (India)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; DNA POLYMERASE; RNA POLYMERASE; RV1222 PROTEIN; UNCLASSIFIED DRUG; BACTERIAL DNA; DNA DIRECTED DNA POLYMERASE; DNA DIRECTED RNA POLYMERASE; PROTEIN BINDING; RNA; SIGMA FACTOR; SPORULATION-SPECIFIC SIGMA FACTORS; TRANSCRIPTION FACTOR;

ARTICLE; BACTERIAL GROWTH; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DNA SEQUENCE; DNA SYNTHESIS; ESCHERICHIA COLI; GENE CONTROL; GROWTH RATE; IN VITRO STUDY; IN VIVO STUDY; INHIBITION KINETICS; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RNA SYNTHESIS; RNA TRANSCRIPTION; TRANSCRIPTION ELONGATION; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; CHEMISTRY; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM;

BACTERIAL PROTEINS; DNA, BACTERIAL; DNA-DIRECTED DNA POLYMERASE; DNA-DIRECTED RNA POLYMERASES; GENE EXPRESSION REGULATION, BACTERIAL; MYCOBACTERIUM TUBERCULOSIS; PROTEIN BINDING; RNA; SIGMA FACTOR; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84942163138     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv516     Document Type: Article

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34. Yang, X. and Lewis, P.J. (2008) Overproduction and purification of recombinant Bacillus subtilis RNA polymerase. Protein Expr. Purif., 59, 86-93.
35. Mukhopadhyay, J., Kapanidis, A.N., Mekler, V., Kortkhonjia, E., Ebright, Y.W. and Ebright, R.H. (2001) Translocation of sigma(70) with RNA polymerase during transcription: fluorescence resonance energy transfer assay for movement relative to DNA. Cell, 106, 453-463.
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39. Samaha, R.R., Joseph, S., O'Brien, B., O'Brien, T.W. and Noller, H.F. (1999) Site-directed hydroxyl radical probing of 30S ribosomal subunits by using Fe(II) tethered to an interruption in the 16S rRNA chain. Proc. Natl Acad. Sci. U.S.A., 96, 366-370.
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45. Kadesch, T.R. and Chamberlin, M.J. (1982) Studies of in vitro transcription by calf thymus RNA polymerase II using a novel duplex DNA template. J. Biol. Chem., 257, 5286-5295.
46. Daubendiek, S.L. and Kool, E.T. (1997) Generation of catalytic RNAs by rolling transcription of synthetic DNA nanocircles. Nat. Biotechnol., 15, 273-277.
47. Owen, B. and McMurray, C. (2009) Rapid method for measuring DNA binding to protein using fluorescence anisotropy. Protocol Exchange, doi: 10.1038/nprot.2009.80.
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49. Steitz, T.A. (1999) DNA polymerases: structural diversity and common mechanisms. J. Biol. Chem., 274, 17395-17398.
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51. Cases, I., de Lorenzo, V. and Ouzounis, C.A. (2003) Transcription regulation and environmental adaptation in bacteria. Trends Microbiol., 11, 248-253.
52. Schlax, P.J., Capp, M.W. and Record, M.T. Jr (1995) Inhibition of transcription initiation by lac repressor. J. Mol. Biol., 245, 331-350.
53. Schiering, N., Tao, X., Zeng, H., Murphy, J.R., Petsko, G.A. and Ringe, D. (1995) Structures of the apo- and the metal ion-activated forms of the diphtheria tox repressor from Corynebacterium diphtheriae. Proc. Natl Acad. Sci. U.S.A., 92, 9843-9850.
54. Caslake, L.F., Ashraf, S.I. and Summers, A.O. (1997) Mutations in the alpha and sigma-70 subunits of RNA polymerase affect expression of the mer operon. J. Bacteriol., 179, 1787-1795.
55. Zwieb, C., Kim, J. and Adhya, S. (1989) DNA bending by negative regulatory proteins: Gal and Lac repressors. Genes Dev., 3, 606-611.
56. Belitsky, B.R. and Sonenshein, A.L. (2011) Roadblock repression of transcription by Bacillus subtilis CodY. J. Mol. Biol., 411, 729-743.
57. He, B. and Zalkin, H. (1992) Repression of Escherichia coli purB is by a transcriptional roadblock mechanism. J. Bacteriol., 174, 7121-7127.
58. Hughes, K.T. and Mathee, K. (1998) The anti-sigma factors. Annu. Rev. Microbiol., 52, 231-286.
59. Helmann, J.D. (1999) Anti-sigma factors. Curr. Opin. Microbiol., 2, 135-141.
60. Atlung, T. and Ingmer, H. (1997) H-NS: a modulator of environmentally regulated gene expression. Mol. Microbiol., 24, 7-17.
61. Tupper, A.E., Owen-Hughes, T.A., Ussery, D.W., Santos, D.S., Ferguson, D.J., Sidebotham, J.M., Hinton, J.C. and Higgins, C.F. (1994) The chromatin-associated protein H-NS alters DNA topology in vitro. EMBO J., 13, 258-268.
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63. Tapias, A., Lopez, G. and Ayora, S. (2000) Bacillus subtilis LrpC is a sequence-independent DNA-binding and DNA-bending protein which bridges DNA. Nucleic Acids Res., 28, 552-559.
64. Furman, R., Danhart, E.M., NandyMazumdar, M., Yuan, C., Foster, M.P. and Artsimovitch, I. (2015) pH dependence of the stress regulator DksA. PloS One, 10, e0120746.
65. Lennon, C.W., Ross, W., Martin-Tumasz, S., Toulokhonov, I., Vrentas, C.E., Rutherford, S.T., Lee, J.H., Butcher, S.E. and Gourse, R.L. (2012) Direct interactions between the coiled-coil tip of DksA and the trigger loop of RNA polymerase mediate transcriptional regulation. Genes Dev., 26, 2634-2646.
66. Tagami, S., Sekine, S., Kumarevel, T., Hino, N., Murayama, Y., Kamegamori, S., Yamamoto, M., Sakamoto, K. and Yokoyama, S. (2010) Crystal structure of bacterial RNA polymerase bound with a transcription inhibitor protein. Nature, 468, 978-982.
67. Laptenko, O., Kim, S.S., Lee, J., Starodubtseva, M., Cava, F., Berenguer, J., Kong, X.P. and Borukhov, S. (2006) pH-dependent conformational switch activates the inhibitor of transcription elongation. EMBO J., 25, 2131-2141.
68. Ross, W., Vrentas, C.E., Sanchez-Vazquez, P., Gaal, T. and Gourse, R.L. (2013) The magic spot: a ppGpp binding site on E. coli RNA polymerase responsible for regulation of transcription initiation. Mol. Cell, 50, 420-429.
69. Perederina, A., Svetlov, V., Vassylyeva, M.N., Tahirov, T.H., Yokoyama, S., Artsimovitch, I. and Vassylyev, D.G. (2004) Regulation through the secondary channel-structural framework for ppGpp-DksA synergism during transcription. Cell, 118, 297-309.
70. Mekler, V., Minakhin, L., Sheppard, C., Wigneshweraraj, S. and Severinov, K. (2011) Molecular mechanism of transcription inhibition by phage T7 gp2 protein. J. Mol. Biol., 413, 1016-1027.
71. Vitiello, C.L. and Gottesman, M.E. (2014) Bacteriophage HK022 Nun protein arrests transcription by blocking lateral mobility of RNA polymerase during transcription elongation. Bacteriophage, 4, e32187.
72. Dona, V., Rodrigue, S., Dainese, E., Palu, G., Gaudreau, L., Manganelli, R. and Provvedi, R. (2008) Evidence of complex transcriptional, translational, and posttranslational regulation of the extracytoplasmic function sigma factor sigmaE in Mycobacterium tuberculosis. J. Bacteriol., 190, 5963-5971.
73. Barik, S., Sureka, K., Mukherjee, P., Basu, J. and Kundu, M. (2010) RseA, the SigE specific anti-sigma factor of Mycobacterium tuberculosis, is inactivated by phosphorylation-dependent ClpC1P2 proteolysis. Mol. Microbiol., 75, 592-606.
74. Murry, J.P., Sassetti, C.M., Lane, J.M., Xie, Z. and Rubin, E.J. (2008) Transposon site hybridization in Mycobacterium tuberculosis. Methods Mol. Biol., 416, 45-59.
75. Murphy, D.J. and Brown, J.R. (2007) Identification of gene targets against dormant phase Mycobacterium tuberculosis infections. BMC Infect. Dis., 7, 84.
76. Hampshire, T., Soneji, S., Bacon, J., James, B.W., Hinds, J., Laing, K., Stabler, R.A., Marsh, P.D. and Butcher, P.D. (2004) Stationary phase gene expression of Mycobacterium tuberculosis following a progressive nutrient depletion: a model for persistent organisms? Tuberculosis (Edinb.), 84, 228-238.
77. Voskuil, M.I., Visconti, K.C. and Schoolnik, G.K. (2004) Mycobacterium tuberculosis gene expression during adaptation to stationary phase and low-oxygen dormancy. Tuberculosis (Edinb.), 84, 218-227.
78. Schnappinger, D., Ehrt, S., Voskuil, M.I., Liu, Y., Mangan, J.A., Monahan, I.M., Dolganov, G., Efron, B., Butcher, P.D., Nathan, C. et al. (2003) Transcriptional adaptation of Mycobacterium tuberculosis within macrophages: insights into the Phagosomal Environment. J. Exp. Med., 198, 693-704.
79. Banerjee, R., Rudra, P., Prajapati, R.K., Sengupta, S. and Mukhopadhyay, J. (2014) Optimization of recombinant Mycobacterium tuberculosis RNA polymerase expression and purification. Tuberculosis (Edinb.), 94, 397-404.
80. Jacques, J.F., Rodrigue, S., Brzezinski, R. and Gaudreau, L. (2006) A recombinant Mycobacterium tuberculosis in vitro transcription system. FEMS Microbiol. Lett., 255, 140-147.
81. Song, T., Song, S.E., Raman, S., Anaya, M. and Husson, R.N. (2008) Critical role of a single position in the -35 element for promoter recognition by Mycobacterium tuberculosis SigE and SigH. J. Bacteriol., 190, 2227-2230.
82. Margeat, E., Kapanidis, A.N., Tinnefeld, P., Wang, Y., Mukhopadhyay, J., Ebright, R.H. and Weiss, S. (2006) Direct observation of abortive initiation and promoter escape within single immobilized transcription complexes. Biophys. J., 90, 1419-1431.
83. Strauch, M.A., Perego, M., Burbulys, D. and Hoch, J.A. (1989) The transition state transcription regulator AbrB of Bacillus subtilis is autoregulated during vegetative growth. Mol. Microbiol., 3, 1203-1209.
84. Yang, X. and Lewis, P.J. (2008) Overproduction and purification of recombinant Bacillus subtilis RNA polymerase. Protein Expr. Purif., 59, 86-93.
85. Mukhopadhyay, J., Kapanidis, A.N., Mekler, V., Kortkhonjia, E., Ebright, Y.W. and Ebright, R.H. (2001) Translocation of sigma(70) with RNA polymerase during transcription: fluorescence resonance energy transfer assay for movement relative to DNA. Cell, 106, 453-463.
86. Arnaud-Barbe, N., Cheynet-Sauvion, V., Oriol, G., Mandrand, B. and Mallet, F. (1998) Transcription of RNA templates by T7 RNA polymerase. Nucleic Acids Res., 26, 3550-3554.
87. Kim, Y., Ho, S.O., Gassman, N.R., Korlann, Y., Landorf, E.V., Collart, F.R. and Weiss, S. (2008) Efficient site-specific labeling of proteins via cysteines. Bioconjug. Chem., 19, 786-791.
88. Banerjee, R., Rudra, P., Saha, A. and Mukhopadhyay, J. (2015) Recombinant reporter assay using transcriptional machinery of mycobacterium tuberculosis. J. Bacteriol., 197, 646-653.
89. Samaha, R.R., Joseph, S., O'Brien, B., O'Brien, T.W. and Noller, H.F. (1999) Site-directed hydroxyl radical probing of 30S ribosomal subunits by using Fe(II) tethered to an interruption in the 16S rRNA chain. Proc. Natl Acad. Sci. U.S.A., 96, 366-370.
90. Owens, J.T., Miyake, R., Murakami, K., Chmura, A.J., Fujita, N., Ishihama, A. and Meares, C.F. (1998) Mapping the sigma70 subunit contact sites on Escherichia coli RNA polymerase with a sigma70-conjugated chemical protease. Proc. Natl Acad. Sci. U.S.A., 95, 6021-6026.
91. Lacenere, C., Garg, M.K., Stoltz, B.M. and Quake, S.R. (2006) Effects of a modified dye-labeled nucleotide spacer arm on incorporation by thermophilic DNA polymerases. Nucleosides Nucleotides Nucleic Acids, 25, 9-15.
92. Minakhin, L., Camarero, J.A., Holford, M., Parker, C., Muir, T.W. and Severinov, K. (2001) Mapping the molecular interface between the sigma(70) subunit of E. coli RNA polymerase and T4 AsiA. J. Mol. Biol., 306, 631-642.
93. Ebright, R.H. (2000) RNA polymerase: structural similarities between bacterial RNA polymerase and eukaryotic RNA polymerase II. J. Mol. Biol., 304, 687-698.
94. Mukhopadhyay, J., Das, K., Ismail, S., Koppstein, D., Jang, M., Hudson, B., Sarafianos, S., Tuske, S., Patel, J., Jansen, R. et al. (2008) The RNA polymerase 'switch region' is a target for inhibitors. Cell, 135, 295-307.
95. Kadesch, T.R. and Chamberlin, M.J. (1982) Studies of in vitro transcription by calf thymus RNA polymerase II using a novel duplex DNA template. J. Biol. Chem., 257, 5286-5295.
96. Daubendiek, S.L. and Kool, E.T. (1997) Generation of catalytic RNAs by rolling transcription of synthetic DNA nanocircles. Nat. Biotechnol., 15, 273-277.
97. Owen, B. and McMurray, C. (2009) Rapid method for measuring DNA binding to protein using fluorescence anisotropy. Protocol Exchange, doi: 10.1038/nprot.2009.80.
98. Carroll, P., Schreuder, L.J., Muwanguzi-Karugaba, J., Wiles, S., Robertson, B.D., Ripoll, J., Ward, T.H., Bancroft, G.J., Schaible, U.E. and Parish, T. (2010) Sensitive detection of gene expression in mycobacteria under replicating and non-replicating conditions using optimized far-red reporters. PloS One, 5, e9823.
99. Steitz, T.A. (1999) DNA polymerases: structural diversity and common mechanisms. J. Biol. Chem., 274, 17395-17398.
100. Kapatral, V., Bina, X. and Chakrabarty, A.M. (2000) Succinyl coenzyme A synthetase of Pseudomonas aeruginosa with a broad specificity for nucleoside triphosphate (NTP) synthesis modulates specificity for NTP synthesis by the 12-kilodalton form of nucleoside diphosphate kinase. J. Bacteriol., 182, 1333-1339.