Interaction of the RcsB response regulator with auxiliary transcription regulators in Escherichia coli

Journal of Biological Chemistry

Volumn 291, Issue 5, 2016, Pages 2357-2370

  Pannen, Derk ^a   Fabisch, Maria ^a   Gausling, Lisa ^a   Schnetz, Karin ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROLIFERATION; CELL SIGNALING; ESCHERICHIA COLI; PLANTS (BOTANY); SIGNAL TRANSDUCTION;

AMINO ACID RESIDUES; AUXILIARY REGULATOR; CONSERVED RESIDUES; HETERODIMERIZATION; PHOSPHORYLATION SITES; RESPONSE REGULATORS; TRANSCRIPTION REGULATIONS; TWO-COMPONENT SIGNAL TRANSDUCTION SYSTEMS;

PHOSPHORYLATION;

DCTR PROTEIN; MATA PROTEIN; RCSA PROTEIN; RCSB PROTEIN; REGULATOR PROTEIN; UNCLASSIFIED DRUG; BETA GALACTOSIDASE; BGLJ PROTEIN, E COLI; DCTR PROTEIN, E COLI; ECPR PROTEIN, E COLI; ESCHERICHIA COLI PROTEIN; LIPOPROTEIN; OLIGONUCLEOTIDE; RCSA PROTEIN, E COLI; RCSB PROTEIN, E COLI; RNA; TRANSACTIVATOR PROTEIN; TRANSCRIPTION FACTOR;

AMINO ACID SEQUENCE; ARTICLE; BACTERIUM CULTURE; CONTROLLED STUDY; DIMERIZATION; ESCHERICHIA COLI; GENE MUTATION; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; BACTERIAL GENOME; CELL MEMBRANE; CONFORMATION; DNA MICROARRAY; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; METABOLISM; MUTATION; PHOSPHORYLATION; PLASMID; PROTEIN MULTIMERIZATION; SPECIES DIFFERENCE;

BETA-GALACTOSIDASE; CELL MEMBRANE; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; GENOME, BACTERIAL; LIPOPROTEINS; MOLECULAR CONFORMATION; MUTATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OLIGONUCLEOTIDES; PHOSPHORYLATION; PLASMIDS; PROTEIN MULTIMERIZATION; RNA; SIGNAL TRANSDUCTION; SPECIES SPECIFICITY; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84957029818     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.696815     Document Type: Article

References (62)

1. Stock, A. M., Robinson, V. L., and Goudreau, P. N. (2000) Two-component signal transduction. Annu. Rev. Biochem. 69, 183-215
2. Gottesman, S., Trisler, P., and Torres-Cabassa, A. (1985) Regulation of capsular polysaccharide synthesis in Escherichia coli K-12: characterization of three regulatory genes. J. Bacteriol. 162, 1111-1119
3. Majdalani, N., and Gottesman, S. (2005) The Rcs phosphorelay: a complex signal transduction system. Annu. Rev. Microbiol. 59, 379-405
4. Clarke, D. J. (2010) The Rcs phosphorelay: more than just a two-component pathway. Future Microbiol. 5, 1173-1184
5. Laubacher, M. E., and Ades, S. E. (2008) The Rcs phosphorelay is a cell envelope stress response activated by peptidoglycan stress and contributes to intrinsic antibiotic resistance. J. Bacteriol. 190, 2065-2074
6. Evans, K. L., Kannan, S., Li, G., de Pedro, M. A., and Young, K. D. (2013) Eliminating a set of four penicillin binding proteins triggers the Rcs phosphorelay and Cpx stress responses in Escherichia coli. J. Bacteriol. 195, 4415-4424
7. Cho, S. H., Szewczyk, J., Pesavento, C., Zietek, M., Banzhaf, M., Roszczenko, P., Asmar, A., Laloux, G., Hov, A. K., Leverrier, P., Van der Henst, C., Vertommen, D., Typas, A., and Collet, J. F. (2014) Detecting envelope stress by monitoring β-barrel assembly. Cell 159, 1652-1664
8. Castanié-Cornet, M. P., Cam, K., Bastiat, B., Cros, A., Bordes, P., and Gutierrez, C. (2010) Acid stress response in Escherichia coli: mechanism of regulation of gadA transcription by RcsB and GadE. Nucleic Acids Res. 38, 3546-3554
9. Venkatesh, G. R., Kembou Koungni, F. C., Paukner, A., Stratmann, T., Blissenbach, B., and Schnetz, K. (2010) BglJ-RcsB heterodimers relieve repression of the Escherichia coli bgl operon by H-NS. J. Bacteriol. 192, 6456-6464
10. Henikoff, S., Wallace, J. C., and Brown, J. P. (1990) Finding protein similarities with nucleotide sequence databases. Methods Enzymol. 183, 111-132
11. Gao, R., Mack, T. R., and Stock, A. M. (2007) Bacterial response regulators: versatile regulatory strategies from common domains. Trends Biochem. Sci. 32, 225-234
12. Wehland, M., and Bernhard, F. (2000) The RcsAB box: characterization of a new operator essential for the regulation of exopolysaccharide biosynthesis in enteric bacteria. J. Biol. Chem. 275, 7013-7020
13. Majdalani, N., Hernandez, D., and Gottesman, S. (2002) Regulation and mode of action of the second small RNA activator of RpoS translation, RprA. Mol. Microbiol. 46, 813-826
14. Stout, V., Torres-Cabassa, A., Maurizi, M. R., Gutnick, D., and Gottesman, S. (1991) RcsA, an unstable positive regulator of capsular polysaccharide synthesis. J. Bacteriol. 173, 1738-1747
15. Ferrières, L., Aslam, S. N., Cooper, R. M., and Clarke, D. J. (2007) The yjbEFGH locus in Escherichia coli K-12 is an operon encoding proteins involved in exopolysaccharide production. Microbiology 153, 1070-1080
16. Francez-Charlot, A., Laugel, B., Van Gemert, A., Dubarry, N., Wiorowski, F., Castanié-Cornet, M. P., Gutierrez, C., and Cam, K. (2003) RcsCDB His-Asp phosphorelay system negatively regulates the flhDC operon in Escherichia coli. Mol. Microbiol. 49, 823-832
17. Stratmann, T., Pul, Ü., Wurm, R., Wagner, R., and Schnetz, K. (2012) RcsB-BglJ activates the Escherichia coli leuO gene, encoding an H-NS antagonist and pleiotropic regulator of virulence determinants. Mol. Microbiol. 83, 1109-1123
18. Salscheider, S. L., Jahn, A., and Schnetz, K. (2014) Transcriptional regulation by BglJ-RcsB, a pleiotropic heteromeric activator in Escherichia coli. Nucleic Acids Res. 42, 2999-3008
19. Al-Bassam, M. M., Bibb, M. J., Bush, M. J., Chandra, G., and Buttner, M. J. (2014) Response regulator heterodimer formation controls a key stage in Streptomyces development. PLoS Genet. 10, e1004554
20. Martínez-Santos, V. I., Medrano-López, A., Saldaña, Z., Girón, J. A., and Puente, J. L. (2012) Transcriptional regulation of the ecp operon by EcpR, IHF, and H-NS in attaching and effacing Escherichia coli. J. Bacteriol. 194, 5020-5033
21. Lehti, T. A., Bauchart, P., Heikkinen, J., Hacker, J., Korhonen, T. K., Dobrindt, U., and Westerlund-Wikström, B. (2010) Mat fimbriae promote biofilm formation by meningitis-associated Escherichia coli. Microbiology 156, 2408-2417
22. Lehti, T. A., Heikkinen, J., Korhonen, T. K., and Westerlund-Wikstrom, B. (2012) The response regulator RcsB activates expression of Mat fimbriae in meningitic Escherichia coli. J. Bacteriol. 194, 3475-3485
23. Lehti, T. A., Bauchart, P., Kukkonen, M., Dobrindt, U., Korhonen, T. K., and Westerlund-Wikström, B. (2013) Phylogenetic group-associated differences in regulation of the common colonization factor Mat fimbria in Escherichia coli. Mol. Microbiol. 87, 1200-1222
24. Masuda, N., and Church, G. M. (2003) Regulatory network of acid resistance genes in Escherichia coli. Mol. Microbiol. 48, 699-712
25. Mates, A. K., Sayed, A. K., and Foster, J. W. (2007) Products of the Escherichia coli acid fitness island attenuate metabolite stress at extremely low pH and mediate a cell density-dependent acid resistance. J. Bacteriol. 189, 2759-2768
26. Yamanaka, Y., Oshima, T., Ishihama, A., and Yamamoto, K. (2014) Characterization of the YdeO regulon in Escherichia coli. PLoS One 9, e111962
27. Wilson, G. G., Young, K. Y., Edlin, G. J., and Konigsberg, W. (1979) Highfrequency generalised transduction by bacteriophage T4. Nature 280, 80-82
28. Miller, J. H. (1972) in Experiments in Molecular Genetics, pp. 352-355, Cold Spring Harbor Laboratory, Cold Spring Harbor, NY
29. Diederich, L., Rasmussen, L. J., and Messer, W. (1992) New cloning vectors for integration in the λ attachment site attB of the Escherichia coli chromosome. Plasmid 28, 14-24
30. Dole, S., Kühn, S., and Schnetz, K. (2002) Post-transcriptional enhancement of Escherichia coli bgl operon silencing by limitation of BglG-mediated antitermination at low transcription rates. Mol. Microbiol. 43, 217-226
31. Datsenko, K. A., and Wanner, B. L. (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. U.S.A. 97, 6640-6645
32. Pristovsek, P., Sengupta, K., Löhr, F., Schäfer, B., von Trebra, M. W., Rüterjans, H., and Bernhard, F. (2003) Structural analysis of the DNA-binding domain of the Erwinia amylovora RcsB protein and its interaction with the RcsAB box. J. Biol. Chem. 278, 17752-17759
33. Kelley, L. A., Mezulis, S., Yates, C. M., Wass, M. N., and Sternberg, M. J. (2015) The Phyre2 web portal for protein modeling, prediction and analysis. Nat. Protoc. 10, 845-858
34. Yang, J., Yan, R., Roy, A., Xu, D., Poisson, J., and Zhang, Y. (2015) The I-TASSER Suite: protein structure and function prediction. Nat. Methods 12, 7-8
35. Söding, J., Biegert, A., and Lupas, A. N. (2005) The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res. 33, W244-W248
36. Schnell, R., Agren, D., and Schneider, G. (2008) 1.9 Å structure of the signal receiver domain of the putative response regulator NarL from Mycobacterium tuberculosis. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 64, 1096-1100
37. Baikalov, I., Schröder, I., Kaczor-Grzeskowiak, M., Cascio, D., Gunsalus, R. P., and Dickerson, R. E. (1998) NarL dimerization? suggestive evidence from a new crystal form. Biochemistry 37, 3665-3676
38. Baikalov, I., Schröder, I., Kaczor-Grzeskowiak, M., Grzeskowiak, K., Gunsalus, R. P., and Dickerson, R. E. (1996) Structure of the Escherichia coli response regulator NarL. Biochemistry 35, 11053-11061
39. Bourret, R. B. (2010) Receiver domain structure and function in response regulator proteins. Curr. Opin. Microbiol. 13, 142-149
40. Dmitrova, M., Younès-Cauet, G., Oertel-Buchheit, P., Porte, D., Schnarr, M., and Granger-Schnarr, M. (1998)Anew LexA-based genetic system for monitoring and analyzing protein heterodimerization in Escherichia coli. Mol. Gen. Genet. 257, 205-212
41. Nishino, K., Inazumi, Y., and Yamaguchi, A. (2003) Global analysis of genes regulated by EvgA of the two-component regulatory system in Escherichia coli. J. Bacteriol. 185, 2667-2672
42. Scharf, B. E. (2010) Summary of useful methods for two-component system research. Curr. Opin. Microbiol. 13, 246-252
43. Lehti, T. A., Bauchart, P., Dobrindt, U., Korhonen, T. K., and Westerlund-Wikström, B. (2012) The fimbriae activator MatA switches off motility in Escherichia coli by repression of the flagellar master operon flhDC. Microbiology 158, 1444-1455
44. Gao, R., and Stock, A. M. (2010) Molecular strategies for phosphorylationmediated regulation of response regulator activity. Curr. Opin. Microbiol. 13, 160-167
45. Stevenson, G., Andrianopoulos, K., Hobbs, M., and Reeves, P. R. (1996) Organization of the Escherichia coli K-12 gene cluster responsible for production of the extracellular polysaccharide colanic acid. J. Bacteriol. 178, 4885-4893
46. Girgis, H. S., Liu, Y., Ryu, W. S., and Tavazoie, S. (2007) A comprehensive genetic characterization of bacterial motility. PLoS Genet. 3, 1644-1660
47. Sledjeski, D., and Gottesman, S. (1995)AsmallRNAacts as an antisilencer of the H-NS-silenced rcsA gene of Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 92, 2003-2007
48. Trajtenberg, F., Albanesi, D., Ruétalo, N., Botti, H., Mechaly, A. E., Nieves, M., Aguilar, P. S., Cybulski, L., Larrieux, N., de Mendoza, D., and Buschiazzo, A. (2014) Allosteric activation of bacterial response regulators: the role of the cognate histidine kinase beyond phosphorylation. mBio 5, e02105
49. Sturny, R., Cam, K., Gutierrez, C., and Conter, A. (2003) NhaR and RcsB independently regulate the osmCp1 promoter of Escherichia coli at overlapping regulatory sites. J. Bacteriol. 185, 4298-4304
50. Hu, L. I., Chi, B. K., Kuhn, M. L., Filippova, E. V., Walker-Peddakotla, A. J., Bäsell, K., Becher, D., Anderson, W. F., Antelmann, H., and Wolfe, A. J. (2013) Acetylation of the response regulator RcsB controls transcription from a small RNA promoter. J. Bacteriol. 195, 4174-4186
51. ε-Lysine acetylation of a bacterial transcription factor inhibits its DNAbinding activity. PLoS One 5, e15123
52. Leonard, P. G., Golemi-Kotra, D., and Stock, A. M. (2013) Phosphorylation-dependent conformational changes and domain rearrangements in Staphylococcus aureus VraR activation. Proc. Natl. Acad. Sci. U.S.A. 110, 8525-8530
53. Zhang, J. H., Xiao, G., Gunsalus, R. P., and Hubbell, W. L. (2003) Phosphorylation triggers domain separation in the DNA binding response regulator narL. Biochemistry 42, 2552-2559
54. Stratmann, T., Madhusudan, S., and Schnetz, K. (2008) Regulation of the yjjQ-bglJ operon, encoding LuxR-type transcription factors, and the divergent yjjP gene by H-NS and LeuO. J. Bacteriol. 190, 926-935
55. Sayed, A. K., and Foster, J. W. (2009) A 750 bp sensory integration region directs global control of the Escherichia coli GadE acid resistance regulator. Mol. Microbiol. 71, 1435-1450
56. Ebel, W., and Trempy, J. E. (1999) Escherichia coli RcsA, a positive activator of colanic acid capsular polysaccharide synthesis, functions to activate its own expression. J. Bacteriol. 181, 577-584
57. Kelley, L. A., and Sternberg, M. J. (2009) Protein structure prediction on the Web: a case study using the Phyre server. Nat. Protoc. 4, 363-371
58. Wiebe, H., Gürlebeck, D., Gross, J., Dreck, K., Pannen, D., Ewers, C., Wieler, L. H., and Schnetz, K. (2015) YjjQ represses transcription of flhDC and additional loci in Escherichia coli. J. Bacteriol. 197, 2713-2720
59. Baba, T., Ara, T., Hasegawa, M., Takai, Y., Okumura, Y., Baba, M., Datsenko, K. A., Tomita, M., Wanner, B. L., and Mori, H. (2006) Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol. Syst. Biol. 10.1038/msb4100050
60. Welch, R. A., Burland, V., Plunkett, G., 3rd, Redford, P., Roesch, P., Rasko, D., Buckles, E. L., Liou, S. R., Boutin, A., Hackett, J., Stroud, D., Mayhew, G. F., Rose, D. J., Zhou, S., Schwartz, D. C., Perna, N. T., Mobley, H. L., Donnenberg, M. S., and Blattner, F. R. (2002) Extensive mosaic structure revealed by the complete genome sequence of uropathogenic Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 99, 17020-17024
61. Cherepanov, P. P., and Wackernagel, W. (1995) Gene disruption in Escherichia coli: TcR and KmR cassettes with the option of Flp-catalyzed excision of the antibiotic-resistance determinant. Gene 158, 9-14
62. Guzman, L. M., Belin, D., Carson, M. J., and Beckwith, J. (1995) Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J. Bacteriol. 177, 4121-4130