Bacillus subtilis δ factor functions as a transcriptional regulator by facilitating the open complex formation

Journal of Biological Chemistry

Volumn 291, Issue 3, 2016, Pages 1064-1075

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

^a BOSE INSTITUTE   (India)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIOLOGY; BINS; DNA SEQUENCES; NUCLEIC ACIDS; RECYCLING; RNA; TRANSCRIPTION;

BACILLUS SUBTILIS; COMPLEX FORMATIONS; CRITICAL LENGTH; GRAM-POSITIVE BACTERIUM; MUTATIONAL ANALYSIS; PROMOTER ELEMENTS; TRANSCRIPTION ASSAYS; TRANSCRIPTIONAL REGULATOR;

DELTA FUNCTIONS;

ABRB PROTEIN; ALANINE; BACTERIAL PROTEIN; RNA POLYMERASE; RNA POLYMERASE DELTA SUBUNIT; RRNB1 PROTEIN; UNCLASSIFIED DRUG; ABRB PROTEIN, BACILLUS SUBTILIS; DNA BINDING PROTEIN; DNA DIRECTED RNA POLYMERASE; FLUORESCENT DYE; RECOMBINANT PROTEIN; RHODAMINE; RNA 16S; SIGMA FACTOR; TETRAMETHYLRHODAMINE; TRANSCRIPTION FACTOR;

AMINO ACID SEQUENCE; ARTICLE; BACILLUS SUBTILIS; BINDING SITE; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVITY; MUTATIONAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN DNA BINDING; PROTEIN FUNCTION; PROTEIN RNA BINDING; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; AT RICH SEQUENCE; CHEMISTRY; DNA FOOTPRINTING; FLUORESCENCE POLARIZATION; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; PHYSIOLOGY; POINT MUTATION; PROMOTER REGION; SITE DIRECTED MUTAGENESIS; TRANSCRIPTION INITIATION SITE;

AT RICH SEQUENCE; BACILLUS SUBTILIS; BACTERIAL PROTEINS; DNA FOOTPRINTING; DNA-BINDING PROTEINS; DNA-DIRECTED RNA POLYMERASES; ELECTROPHORETIC MOBILITY SHIFT ASSAY; FLUORESCENCE POLARIZATION; FLUORESCENT DYES; GENE EXPRESSION REGULATION, BACTERIAL; MUTAGENESIS, SITE-DIRECTED; POINT MUTATION; PROMOTER REGIONS, GENETIC; RECOMBINANT PROTEINS; RHODAMINES; RNA, RIBOSOMAL, 16S; SIGMA FACTOR; TRANSCRIPTION FACTORS; TRANSCRIPTION INITIATION SITE; TRANSCRIPTION INITIATION, GENETIC; TRANSCRIPTION, GENETIC;

EID: 84954475070     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.686170     Document Type: Article

References (38)

1. Pero, J., Nelson, J., and Fox, T. D. (1975) Highly asymmetric transcription by RNA polymerase containing phage-SP01-induced polypeptides and a new host protein. Proc. Natl. Acad. Sci. U.S.A. 72, 1589-1593
2. Tjian, R., Losick, R., Pero, J., and Hinnebush, A. (1977) Purification and comparative properties of the delta and sigma subunits of RNA polymerase from Bacillus subtilis. Eur. J. Biochem. 74, 149-154
3. Achberger, E. C., and Whiteley, H. R. (1981) The role of the delta peptide of the Bacillus subtilis RNA polymerase in promoter selection. J. Biol. Chem. 256, 7424-7432
4. Dobinson, K. F., and Spiegelman, G. B. (1987) Effect of the delta subunit of Bacillus subtilis RNA polymerase on initiation of RNA synthesis at two bacteriophage phi 29 promoters. Biochemistry 26, 8206-8213
5. Juang, Y. L., and Helmann, J. D. (1994) The delta subunit of Bacillus subtilis RNA polymerase. An allosteric effector of the initiation and corerecycling phases of transcription. J. Mol. Biol. 239, 1-14
6. Williamson, V. M., and Doi, R. H. (1979) Sigma factor is not released during transcription in Bacillus subtilis. Mol. Gen. Genet. 174, 47-52
7. Dickel, C. D., Burtis, K. C., and Doi, R. H. (1980) Delta factor increases promoter selectivity of Bacillus subtilis vegetative cell RNA polymerase. Biochem. Biophys. Res. Commun. 95, 1789-1795
8. Hyde, E. I., Hilton, M. D., and Whiteley, H. R. (1986) Interactions of Bacillus subtilis RNA polymerase with subunits determining the specificity of initiation: sigma and delta peptides can bind simultaneously to core. J. Biol. Chem. 261, 16565-16570
9. López de Saro, F. J., Yoshikawa, N., and Helmann, J. D. (1999) Expression, abundance, and RNA polymerase binding properties of the delta factor of Bacillus subtilis. J. Biol. Chem. 274, 15953-15958
10. López de Saro, F. J., Woody, A. Y., and Helmann, J. D. (1995) Structural analysis of the Bacillus subtilis delta factor: a protein polyanion which displaces RNA from RNA polymerase. J. Mol. Biol. 252, 189-202
11. Gao, H., and Aronson, A. I. (2004) The delta subunit of RNA polymerase functions in sporulation. Curr. Microbiol. 48, 401-404
12. Rabatinová, A., ͈anderová, H., Jirát Matêjɥková, J., Korelusová, J., Sojka, L., Barvík, I., Papou͉ková, V., Sklenár, V., Zídek, L., and Krásný, L. (2013) The delta subunit of RNA polymerase is required for rapid changes in gene expression and competitive fitness of the cell. J. Bacteriol. 195, 2603-2611
13. Weiss, A., Ibarra, J. A., Paoletti, J., Carroll, R. K., and Shaw, L. N. (2014) The delta subunit of RNA polymerase guides promoter selectivity and virulence in Staphylococcus aureus. Infect. Immun. 82, 1424-1435
14. Yang, X., and Lewis, P. J. (2008) Overproduction and purification of recombinant Bacillus subtilis RNA polymerase. Protein Expr. Purif. 59, 86-93
15. Mukhopadhyay, J., Mekler, V., Kortkhonjia, E., Kapanidis, A. N., Ebright, Y. W., and Ebright, R. H. (2003) Fluorescence resonance energy transfer (FRET) in analysis of transcription-complex structure and function. Methods Enzymol. 371, 144-159
16. 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
17. Rudra, P., Prajapati, R. K., Banerjee, R., Sengupta, S., and Mukhopadhyay, J. (2015) Novel mechanism of gene regulation: the protein Rv1222 of Mycobacterium tuberculosis inhibits transcription by anchoring the RNA polymerase onto DNA. Nucleic Acids Res. 43, 5855-5867
18. Banerjee, R., Rudra, P., Saha, A., and Mukhopadhyay, J. (2015) Recombinant reporter assay using transcriptional machinery of Mycobacterium tuberculosis. J. Bacteriol. 197, 646-653
19. Daubendiek, S. L., Ryan, K., and Kool, E. T. (1995) Rolling circle RNA synthesis: circular oligonucleotides as efficient substrates for T7 RNA-polymerase. J. Am. Chem. Soc. 117, 7818-7819
20. 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
21. Stewart, G. C., and Bott, K. F. (1983) DNA sequence of the tandem ribosomal RNA promoter for B. subtilis operon rrnB. Nucleic Acids Res. 11, 6289-6300
22. Arndt, K. M., and Chamberlin, M. J. (1990) RNA chain elongation by Escherichia coli RNA polymerase: factors affecting the stability of elongating ternary complexes. J. Mol. Biol. 213, 79-108
23. Nudler, E., Gusarov, I., Avetissova, E., Kozlov, M., and Goldfarb, A. (1998) Spatial organization of transcription elongation complex in Escherichia coli. Science 281, 424-428
24. Motácková, V., Sanderová, H., Zídek, L., Novácek, J., Padrta, P., Svenková, A., Korelusová, J., Jonák, J., Krásný, L., and Sklenár, V. (2010) Solution structure of the N-terminal domain of Bacillus subtilis delta subunit of RNA polymerase and its classification based on structural homologs. Proteins 78, 1807-1810
25. Demo, G., Papou͉ková, V., Komárek, J., Kaderávek, P., Otrusinová, O., Srb, P., Rabatinová, A., Krásný, L., Zídek, L., Sklenár, V., and Wimmerová, M. (2014) X-ray vs. NMR structure of N-terminal domain of delta-subunit of RNA polymerase. J. Struct. Biol. 187, 174-186
26. Aravind, L., and Iyer, L. M. (2012) The HARE-HTH and associated domains: novel modules in the coordination of epigenetic DNA and protein modifications. Cell Cycle 11, 119-131
27. Helmann, J. D. (1995) Compilation and analysis of Bacillus subtilis sigma A-dependent promoter sequences: evidence for extended contact between RNA polymerase and upstream promoter DNA. Nucleic Acids Res. 23, 2351-2360
28. Xue, X., Tomasch, J., Sztajer, H., and Wagner-Döbler, I. (2010) The delta subunit of RNA polymerase, RpoE, is a global modulator of Streptococcus mutans environmental adaptation. J. Bacteriol. 192, 5081-5092
29. Xue, X., Sztajer, H., Buddruhs, N., Petersen, J., Rohde, M., Talay, S. R., and Wagner-Döbler, I. (2011) Lack of the delta subunit of RNA polymerase increases virulence related traits of Streptococcus mutans. PLoS One 6, e20075
30. Xue, X., Li, J., Wang, W., Sztajer, H., and Wagner-Döbler, I. (2012) The global impact of the delta subunit RpoE of the RNA polymerase on the proteome of Streptococcus mutans. Microbiology 158, 191-206
31. Choy, H. E., Park, S. W., Aki, T., Parrack, P., Fujita, N., Ishihama, A., and Adhya, S. (1995) Repression and activation of transcription by Gal and Lac repressors: involvement of alpha subunit of RNA polymerase.EMBOJ. 14, 4523-4529
32. Quinones, M., Kimsey, H. H., Ross, W., Gourse, R. L., and Waldor, M. K. (2006) LexA represses CTXphi transcription by blocking access of the alpha C-terminal domain of RNA polymerase to promoter DNA. J. Biol. Chem. 281, 39407-39412
33. Varughese, K. I., Madhusudan, Zhou, X. Z., Whiteley, J. M., and Hoch, J. A. (1998) Formation of a novel four-helix bundle and molecular recognition sites by dimerization of a response regulator phosphotransferase. Mol. Cell 2, 485-493
34. Komissarova, N., and Kashlev, M. (1998) Functional topography of nascent RNA in elongation intermediates of RNA polymerase. Proc. Natl. Acad. Sci. U.S.A. 95, 14699-14704
35. Kolb, K. E., Hein, P. P., and Landick, R. (2014) Antisense oligonucleotide stimulated transcriptional pausing reveals RNA exit channel specificity of RNA polymerase and mechanistic contributions of NusA and RfaH. J. Biol. Chem. 289, 1151-1163
36. Murakami, K. S., and Darst, S. A. (2003) Bacterial RNA polymerases: the wholo story. Curr. Opin. Struct. Biol. 13, 31-39
37. Davydova, E. K., and Rothman-Denes, L. B. (2003) Escherichia coli singlestranded DNA-binding protein mediates template recycling during transcription by bacteriophage N4 virion RNA polymerase. Proc. Natl. Acad. Sci. U.S.A. 100, 9250-9255
38. Sambrook, J., and Russell, D. W. (2001) Molecular cloning: a laboratory manual, 3rd Ed., Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY