The dynamic protein partnership of RNA polymerase inBacillus subtilis

Proteomics

Volumn 11, Issue 15, 2011, Pages 2992-3001

  Delumeau, Olivier ^a   Lecointe, François ^a   Muntel, Jan ^b   Guillot, Alain ^a,c   Guédon, Eric ^a   Monnet, Véronique ^a,c   Hecker, Michael ^b   Becher, Dörte ^b   Polard, Patrice ^a,d   Noirot, Philippe ^a  

^a UMR1319 MICALIS   (France)

^b UNIVERSITY OF GREIFSWALD   (Germany)

^c CEMAGREF   (France)

^d UNIVERSITÉ DE TOULOUSE   (France)

Author keywords

Microbiology; Multiprotein complex; Quantitative analysis; Sigma factor; Tandem affinity purification; Transcription regulation

Indexed keywords

BACTERIAL ENZYME; ELONGATION FACTOR; HELICASE; PROTEIN HELD; PROTEIN PCRA; PROTEIN SIGA; PROTEIN SIGB; PROTEIN SIGD; PROTEIN SIGF; PROTEIN SIGH; PROTEIN SIGL; PROTEIN SIGM; PROTEIN SIGW; PROTEIN SIGX; PROTEIN TOPA; RNA POLYMERASE; SIGMA FACTOR; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ARTICLE; BACILLUS SUBTILIS; BACTERIAL CELL; BACTERIAL GROWTH; BACTERIAL STRAIN; CONTROLLED STUDY; ENZYME ACTIVITY; MASS SPECTROMETRY; MOLECULAR DYNAMICS; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PURIFICATION; QUANTITATIVE ANALYSIS; RNA ANALYSIS; STOICHIOMETRY; TANDEM MASS SPECTROMETRY;

AFFINITY LABELS; BACILLUS SUBTILIS; BACTERIAL PROTEINS; CHROMATOGRAPHY, AFFINITY; DNA-DIRECTED RNA POLYMERASES; ELECTROPHORESIS, POLYACRYLAMIDE GEL; MULTIPROTEIN COMPLEXES; PROTEIN SUBUNITS; PROTEOMICS; RNA, BACTERIAL; SIGMA FACTOR; TANDEM MASS SPECTROMETRY;

BACILLUS SUBTILIS; PROKARYOTA;

EID: 79960421161     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.201000790     Document Type: Article

References (45)

1. Nudler, E., RNA polymerase active center: the molecular engine of transcription. Annu. Rev. Biochem. 2009, 78, 335-361.
2. Doherty, G., Fogg, M., Wilkinson, A., Lewis, P., Small subunits of RNA polymerase: localisation, levels and implications for core enzyme composition. Microbiology 2010, 156, 3532-3543.
3. Helmann, J. D., Moran, C. P., Jr., RNA polymerase and sigma factors. in: Sonenshin, A. L., Hoch, J. A., Losick, R. (Eds) Bacillus subtilis and its Closest Relatives: From Genes to Cells, ASM Press, Washington, DC, USA 2002, pp. 289-312.
4. Gruber, T. M., Gross, C. A., Multiple sigma subunits and the partitioning of bacterial transcription space. Annu. Rev. Microbiol. 2003, 57, 441-466.
5. Helmann, J. D., The extracytoplasmic function (ECF) sigma factors. Adv. Microb. Physiol. 2002, 46, 47-110.
6. Browning, D. F., Busby, S. J., The regulation of bacterial transcription initiation. Nat. Rev. Microbiol. 2004, 2, 57-65.
7. Beck, L. L., Smith, T. G., Hoover, T. R., Look, no hands! Unconventional transcriptional activators in bacteria. Trends Microbiol. 2007, 15, 530-537.
8. Rutherford, S. T., Lemke, J. J., Vrentas, C. E., Gaal, T. et al., Effects of DksA, GreA, and GreB on transcription initiation: insights into the mechanisms of factors that bind in the secondary channel of RNA polymerase. J. Mol. Biol. 2007, 366, 1243-1257.
9. Trotochaud, A. E., Wassarman, K. M., A highly conserved 6S RNA structure is required for regulation of transcription. Nat. Struct. Mol. Biol. 2005, 12, 313-319.
10. Rigaut, G., Shevchenko, A., Rutz, B., Wilm, M. et al., A generic protein purification method for protein complex characterization and proteome exploration. Nature Biotechnol. 1999, 17, 1030-1032.
11. Hochleitner, E. O., Kastner, B., Frohlich, T., Schmidt, A. et al., Protein stoichiometry of a multiprotein complex, the human spliceosomal U1 small nuclear ribonucleoprotein: absolute quantification using isotope-coded tags and mass spectrometry. J. Biol. Chem. 2005, 280, 2536-2542.
12. Holzmann, J., Pichler, P., Madalinski, M., Kurzbauer, R., Mechtler, K., Stoichiometry determination of the MP1-p14 complex using a novel and cost-efficient method to produce an equimolar mixture of standard peptides. Anal. Chem. 2009, 81, 10254-10261.
13. Lecointe, F., Serena, C., Velten, M., Costes, A. et al., Anticipating chromosomal replication fork arrest: SSB targets repair DNA helicases to active forks. EMBO J. 2007, 26, 4239-4251.
14. Wiegert, T., Homuth, G., Versteeg, S., Schumann, W., Alkaline shock induces the Bacillus subtilis sigma(W) regulon. Mol. Microbiol. 2001, 41, 59-71.
15. Schaeffer, P., Millet, J., Aubert, J. P., Catabolic repression of bacterial sporulation. Proc. Natl. Acad. Sci. USA 1965, 54, 704-711.
16. Ishihama, Y., Oda, Y., Tabata, T., Sato, T. et al., Exponentially modified protein abundance index (emPAI) for estimation of absolute protein amount in proteomics by the number of sequenced peptides per protein. Mol. Cell. Proteomics 2005, 4, 1265-1272.
17. Rice, P., Longden, I., Bleasby, A., EMBOSS: the European Molecular Biology Open Software Suite. Trends Genet. 2000, 16, 276-277.
18. Thompson, A., Schafer, J., Kuhn, K., Kienle, S. et al., Tandem mass tags: a novel quantification strategy for comparative analysis of complex protein mixtures by MS/MS. Anal. Chem. 2003, 75, 1895-1904.
19. Ishikawa, S., Oshima, T., Kurokawa, K., Kusuya, Y., Ogasawara, N., RNA polymerase trafficking in Bacillus subtilis cells. J. Bacteriol. 2010, 192, 5778-5787.
20. Mooney, R. A., Davis, S. E., Peters, J. M., Rowland, J. L. et al., Regulator trafficking on bacterial transcription units in vivo. Mol. Cell 2009, 33, 97-108.
21. Boylan, S. A., Redfield, A. R., Brody, M. S., Price, C. W., Stress-induced activation of the sigma B transcription factor of Bacillus subtilis. J. Bacteriol. 1993, 175, 7931-7937.
22. Boylan, S. A., Redfield, A. R., Price, C. W., Transcription factor sigma B of Bacillus subtilis controls a large stationary-phase regulon. J. Bacteriol. 1993, 175, 3957-3963.
23. Marquez, L. M., Helmann, J. D., Ferrari, E., Parker, H. M. et al., Studies of sigma D-dependent functions in Bacillus subtilis. J. Bacteriol. 1990, 172, 3435-3443.
24. Weir, J., Predich, M., Dubnau, E., Nair, G., Smith, I., Regulation of spo0H, a gene coding for the Bacillus subtilis sigma H factor. J. Bacteriol. 1991, 173, 521-529.
25. Horsburgh, M. J., Moir, A., Sigma M, an ECF RNA polymerase sigma factor of Bacillus subtilis 168, is essential for growth and survival in high concentrations of salt. Mol. Microbiol. 1999, 32, 41-50.
26. Cao, M., Helmann, J. D., The Bacillus subtilis extracytoplasmic-function sigmaX factor regulates modification of the cell envelope and resistance to cationic antimicrobial peptides. J. Bacteriol. 2004, 186, 1136-1146.
27. Margolis, P., Driks, A., Losick, R., Establishment of cell type by compartmentalized activation of a transcription factor. Science 1991, 254, 562-565.
28. Ali, N. O., Bignon, J., Rapoport, G., Debarbouille, M., Regulation of the acetoin catabolic pathway is controlled by sigma L in Bacillus subtilis. J. Bacteriol. 2001, 183, 2497-2504.
29. Choi, S. K., Saier, M. H., Jr., Regulation of sigL expression by the catabolite control protein CcpA involves a roadblock mechanism in Bacillus subtilis: potential connection between carbon and nitrogen metabolism. J. Bacteriol. 2005, 187, 6856-6861.
30. Kovacs, T., Hargitai, A., Kovacs, K. L., Mecs, I., pH-dependent activation of the alternative transcriptional factor sigmaB in Bacillus subtilis. FEMS Microbiol. Lett. 1998, 165, 323-328.
31. Lopez de Saro, F. J., Yoshikawa, N., Helmann, J. D., Expression, abundance, and RNA polymerase binding properties of the delta factor of Bacillus subtilis. J. Biol. Chem. 1999, 274, 15953-15958.
32. Borukhov, S., Nudler, E., RNA polymerase: the vehicle of transcription. Trends Microbiol. 2008, 16, 126-134.
33. Noirot-Gros, M. F., Dervyn, E., Wu, L. J., Mervelet, P. et al., An expanded view of bacterial DNA replication. Proc. Natl. Acad. Sci. USA 2002, 99, 8342-8347.
34. Baharoglu, Z., Lestini, R., Duigou, S., Michel, B., RNA polymerase mutations that facilitate replication progression in the rep uvrD recF mutant lacking two accessory replicative helicases. Mol. Microbiol. 2010, 77, 324-336.
35. Kobayashi, K., Ehrlich, S. D., Albertini, A., Amati, G. et al., Essential Bacillus subtilis genes. Proc. Natl. Acad. Sci. USA 2003, 100, 4678-4683.
36. Cheng, B., Zhu, C. X., Ji, C., Ahumada, A., Tse-Dinh, Y. C., Direct interaction between Escherichia coli RNA polymerase and the zinc ribbon domains of DNA topoisomerase I. The J. Biol. Chem 2003, 278, 30705-30710.
37. Wu, H. Y., Shyy, S. H., Wang, J. C., Liu, L. F., Transcription generates positively and negatively supercoiled domains in the template. Cell 1988, 53, 433-440.
38. Park, J. S., Marr, M. T., Roberts, J. W., E. coli transcription repair coupling factor (Mfd protein) rescues arrested complexes by promoting forward translocation. Cell 2002, 109, 757-767.
39. Nakano, S., Nakano, M. M., Zhang, Y., Leelakriangsak, M., Zuber, P., A regulatory protein that interferes with activator-stimulated transcription in bacteria. Proc. Natl. Acad. Sci. USA 2003, 100, 4233-4238.
40. Sun, G., Sharkova, E., Chesnut, R., Birkey, S. et al., Regulators of aerobic and anaerobic respiration in Bacillus subtilis. J. Bacteriol. 1996, 178, 1374-1385.
41. Huang, X., Gaballa, A., Cao, M., Helmann, J. D., Identification of target promoters for the Bacillus subtilis extracytoplasmic function sigma factor, sigma W. Mol. Microbiol. 1999, 31, 361-371.
42. Barrick, J. E., Sudarsan, N., Weinberg, Z., Ruzzo, W. L., Breaker, R. R., 6S RNA is a widespread regulator of eubacterial RNA polymerase that resembles an open promoter. RNA 2005, 11, 774-784.
43. Mosley, A. L., Sardiu, M. E., Pattenden, S. G., Workman, J. L. et al., Highly reproducible label free quantitative proteomic analysis of RNA polymerase complexes. Mol. Cell. Proteomics 2011, 10, 10.1074/mcp.M110.000687.
44. Petit, M. A., Ehrlich, D., Essential bacterial helicases that counteract the toxicity of recombination proteins. EMBO J. 2002, 21, 3137-3147.
45. Lehnik-Habrink, M., Pfortner, H., Rempeters, L., Pietack, N. et al., The RNA degradosome in Bacillus subtilis: identification of CshA as the major RNA helicase in the multiprotein complex. Mol. Microbiol. 2010, 77, 958-971.