The Escherichia coli CpxA-CpxR envelope stress response system regulates expression of the porins OmpF and OmpC

Journal of Bacteriology

Volumn 187, Issue 16, 2005, Pages 5723-5731

  Batchelor, Eric ^a   Walthers, Don ^b   Kenney, Linda J ^b   Goulian, Mark ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYL PHOSPHATE; DEOXYRIBONUCLEASE I; OUTER MEMBRANE PROTEIN; OUTER MEMBRANE PROTEIN C; OUTER MEMBRANE PROTEIN F; PHOSPHATE; PORIN; PROTEIN CPXA; PROTEIN CPXR; PROTEIN ENVZ; PROTEIN HISTIDINE KINASE; SIGMA FACTOR; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENE; BACTERIAL OUTER MEMBRANE; BACTERIUM MUTANT; CONTROLLED STUDY; DNA FOOTPRINTING; ESCHERICHIA COLI; FLUORESCENCE MICROSCOPY; GENE EXPRESSION REGULATION; GENE INSERTION; GENETIC ANALYSIS; GENETIC TRANSCRIPTION; MUTAGENESIS; NONHUMAN; OMPC GENE; OMPF GENE; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DNA BINDING; PROTEIN PHOSPHORYLATION; SENSOR; SIGNAL TRANSDUCTION; STRESS; TRANSPOSON;

BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL PROTEINS; BASE SEQUENCE; DEOXYRIBONUCLEASE I; DNA FOOTPRINTING; DNA TRANSPOSABLE ELEMENTS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; MOLECULAR SEQUENCE DATA; MULTIENZYME COMPLEXES; MUTAGENESIS; PORINS; PROTEIN KINASES; TRANSCRIPTION, GENETIC; WATER-ELECTROLYTE BALANCE;

ESCHERICHIA COLI;

EID: 23644456999     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.187.16.5723-5731.2005     Document Type: Article

References (68)

1. Ades, S. E. 2004. Control of the alternative sigma factor sigmaE in Escherichia coli. Curr. Opin. Microbiol. 7:157-162.
2. Alba, B. M., and C. A. Gross. 2004. Regulation of the Escherichia coli sigma-dependent envelope stress response. Mol. Microbiol. 52:613-619.
3. Amann, E., B. Ochs, and K. J. Abel. 1988. Tightly regulated tac promoter vectors useful for the expression of unfused and fused proteins in Escherichia coli. Gene 69:301-315.
4. Batchelor, E., and M. Goulian. 2003. Robustness and the cycle of phosphorylation and dephosphorylation in a two-component regulatory system. Proc. Natl. Acad. Sci. USA 100:691-696.
5. Batchelor, E., T. J. Silhavy, and M. Goulian. 2004. Continuous control in bacterial regulatory circuits. J. Bacteriol. 186:7618-7625.
6. Birkey, S. M., W. Liu, X. Zhang, M. F. Duggan, and F. M. Hulett. 1998. Pho signal transduction network reveals direct transcriptional regulation of one two-component system by another two-component regulator: Bacillus subtilis PhoP directly regulates production of ResD. Mol. Microbiol. 30:943-953.
7. Bolivar, F. 1978. Construction and characterization of new cloning vehicles. III. Derivatives of plasmid pBR322 carrying unique EcoRI sites for selection of EcoRI generated recombinant DNA molecules. Gene 4:121-136.
8. Casadaban, M. J. 1976. Transposition and fusion of the lac genes to selected promoters in Escherichia coli using bacteriophage lambda and Mu. J. Mol. Biol. 104:541-555.
9. Chen, S., A. Zhang, L. B. Blyn, and G. Storz. 2004. MicC, a second small-RNA regulator of Omp protein expression in Escherichia coli. J. Bacteriol. 186:6689-6697.
10. Danese, P. N., G. R. Oliver, K. Barr, G. D. Bowman, P. D. Rick, and T. J. Silhavy. 1998. Accumulation of the enterobacterial common antigen lipid II biosynthetic intermediate stimulates degP transcription in Escherichia coli. J. Bacteriol. 180:5875-5884.
11. Danese, P. N., and T. J. Silhavy. 1998. CpxP, a stress-combative member of the Cpx regulon. J. Bacteriol. 180:831-839.
12. Danese, P. N., W. B. Snyder, C. L. Cosma, L. J. Davis, and T. J. Silhavy. 1995. The Cpx two-component signal transduction pathway of Escherichia coli regulates transcription of the gene specifying the stress-inducible periplasmic protease, DegP. Genes Dev. 9:387-398.
13. Datsenko, K. A., and B. L. Wanner. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. USA 97:6640-6645.
14. Delihas, N., and S. Forst. 2001. MicF: an antisense RNA gene involved in response of Escherichia coli to global stress factors. J. Mol. Biol. 313:1-12.
15. De Wulf, P., A. M. McGuire, X. Liu, and E. C. Lin. 2002. Genome-wide profiling of promoter recognition by the two-component response regulator CpxR-P in Escherichia coli. J. Biol. Chem. 277:26652-26661.
16. DiGiuseppe, P. A., and T. J. Silhavy. 2003. Signal detection and target gene induction by the CpxRA two-component system. J. Bacteriol. 185:2432-2440.
17. Dorel, C., O. Vidal, C. Prigent-Combaret, I. Vallet, and P. Lejeune. 1999. Involvement of the Cpx signal transduction pathway of E. coli in biofilm formation. FEMS Microbiol. Lett. 178:169-175.
18. Duguay, A. R., and T. J. Silhavy. 2004. Quality control in the bacterial periplasm. Biochim. Biophys. Acta 1694:121-134.
19. Egger, L. A., H. Park, and M. Inouye. 1997. Signal transduction via the histidyl-aspartyl phosphorelay. Genes Cells 2:167-184.
20. Eguchi, Y., and R. Utsumi. 2005. A novel mechanism for connecting bacterial two-component signal-transduction systems. Trends Biochem. Sci. 30:70-72.
21. Ferrario, M., B. R. Ernsting, D. W. Borst, D. E. Wiese, 2nd, R. M. Blumenthal, and R. G. Matthews. 1995. The leucine-responsive regulatory protein of Escherichia coli negatively regulates transcription of ompC and micF and positively regulates translation oiompF. J. Bacteriol. 177:103-113.
22. Forst, S., J. Delgado, A. Rampersaud, and M. Inouye. 1990. In vivo phosphorylation of OmpR, the transcription activator of the ompF and ompC genes in Escherichia coli. J. Bacteriol. 172:3473-3477.
23. Forst, S., and M. Inouye. 1988. Environmentally regulated gene expression for membrane proteins in Escherichia coli. Annu. Rev. Cell Biol. 4:21-42.
24. Gunn, J. S., and S. I. Miller. 1996. PhoP-PhoQ activates transcription of pmrAB, encoding a two-component regulatory system involved in Salmonella typhimimum antimicrobial peptide resistance. J. Bacteriol. 178:6857-6864.
25. Head, C. G., A. Tardy, and L. J. Kenney. 1998. Relative binding affinities of OmpR and OmpR-phosphate at the ompF and ompC regulatory sites. J. Mol. Biol. 281:857-870.
26. Hernday, A. D., B. A. Braaten, G. Broitman-Maduro, P. Engelberts, and D. A. Low. 2004. Regulation of the pap epigenetic switch by CpxAR: phosphorylated CpxR inhibits transition to the phase ON state by competition with Lrp. Mol. Cell 16:537-547.
27. Hsing, W., and T. J. Silhavy. 1997. Function of conserved histidine-243 in phosphatase activity of EnvZ, the sensor for porin osmoregulation in Escherichia coli. J. Bacteriol. 179:3729-3735.
28. Huang, K.-J., and M. M. Igo. 1996. Identification of the bases in the ompF regulatory region which interact with the transcription factor OmpR. J. Mol. Biol. 262:615-628.
29. Huang, K.-J., J. L. Schieberl, and M. M. Igo. 1994. A distant upstream site involved in the negative regulation of the Escherichia coli ompF gene. J. Bacteriol. 176:1309-1315.
30. Huang, L., P. Tsui, and M. Freundlich. 1990. Integration host factor is a negative effector of in vivo and in vitro expression of ompC in Escherichia coli. J. Bacteriol. 172:5293-5298.
31. Hung, D. L., T. L. Raivio, C. H. Jones, T. J. Silhavy, and S. J. Hultgren. 2001. Cpx signaling pathway monitors biogenesis and affects assembly and expression of P pili. EMBO J. 20:1508-1518.
32. Jubelin, G., A. Vianney, C. Beloin, J. M. Ghigo, J. C. Lazzaroni, P. Lejeune, and C. Dorel. 2005. CpxR/OmpR interplay regulates curli gene expression in response to osmolarity in Escherichia coli. J. Bacteriol. 187:2038-2049.
33. Kawaji, H., T. Mizuno, and S. Mizushima. 1979. Influence of molecular size and osmolarity of sugars and dextrans on the synthesis of outer membrane proteins O-8 and O-9 of Escherichia coli K-12. J. Bacteriol. 140:843-847.
34. Kenney, L. J. 2002. Structure/function relationships in OmpR and other winged-helix transcription factors. Curr. Opin. Microbiol. 5:135-141.
35. Koo, I. C., D. Walthers, T. L. Nicholson, L. J. Kenney, and R. S. Stephens. Submitted for publication.
36. Lan, C. Y., and M. M. Igo. 1998. Differential expression of the OmpF and OmpC porin proteins in Escherichia coli K-12 depends upon the level of active OmpR. J. Bacteriol. 180:171-174.
37. E extracytoplasmic stress responses. J. Bacteriol. 183:5230-5238.
38. Larsen, R. A., M. M. Wilson, A. M. Guss, and W. W. Metcalf. 2002. Genetic analysis of pigment biosynthesis in Xanthobacter autotrophicus Py2 using a new, highly efficient transposon mutagenesis system that is functional in a wide variety of bacteria. Arch. Microbiol. 178:193-201.
39. Lee, Y. M., P. A. DiGiuseppe, T. J. Silhavy, and S. J. Hultgren. 2004. P pilus assembly motif necessary for activation of the CpxRA pathway by PapE in Escherichia coli. J. Bacteriol. 186:4326-4337.
40. Liu, X., and T. Ferenci. 2001. An analysis of multifactorial influences on the transcriptional control of ompF and ompC porin expression under nutrient limitation. Microbiology 147:2981-2989.
41. Maeda, S., and T. Mizuno. 1990. Evidence for multiple OmpR-binding sites in the upstream activation sequence of the ompC promoter in Escherichia coli: a single OmpR-binding site is capable of activating the promoter. J. Bacteriol. 172:501-503.
42. Mattison, K., R. Oropeza, N. Byers, and L. J. Kenney. 2002. A phosphorylation site mutant of OmpR reveals different binding conformations at ompF and ompC. J. Mol. Biol. 315:497-511.
43. McCleary, W. R., and J. B. Stock. 1994. Acetyl phosphate and the activation of two-component response regulators. J. Biol. Chem. 269:31567-31572.
44. McEwen, J., L. Sambucetti, and P. M. Silverman. 1983. Synthesis of outer membrane proteins in cpxA cpxB mutants of Escherichia coli K-12. J. Bacteriol. 154:375-382.
45. Mecsas, J., P. E. Rouviere, J. W. Erickson, T. J. Donohue, and C. A. Gross. 1993. The activity of sigma E, an Escherichia coli heat-inducible sigma factor, is modulated by expression of outer membrane proteins. Genes Dev. 7:2618-2628.
46. Miller, J. H. 1992, A short course in bacterial genetics: a laboratory manual and handbook for Escherichia coli and related bacteria. CSHL Press, Plainview, N.Y.
47. 2+ stimulon of Escherichia coli. J. Bacteriol. 185:3696-3702.
48. Mizuno, T., M. Kato, Y. L. Jo, and S. Mizushima. 1988. Interaction of OmpR, a positive regulator, with the osmoregulated ompC and ompF genes of Escherichia coli. Studies with wild-type and mutant OmpR proteins. J. Biol. Chem. 263:1008-1012.
49. Mouslim, C., and E. A. Groisman. 2003. Control of the Salmonella ugd gene by three two-component regulatory systems. Mol. Microbiol. 47:335-344.
50. Nakayama, S., and H. Watanabe. 1998. Identification of cpxR as a positive regulator essential for expression of the Shigella sonnei virF gene. J. Bacteriol. 180:3522-3528.
51. Nevesinjac, A. Z., and T. L. Raivio. 2005. The Cpx envelope stress response affects expression of the type IV bundle-forming pili of enteropathogenic Escherichia coli. J. Bacteriol. 187:672-686.
52. Nikaido, H. 1996. Outer membrane, p. 29-47. In F. C. Neidhardt, R. Curtiss III, J. L. Ingraham, E. C. C. Lin, K. B. Low, B. Magasanik, W. S. Reznikoff, M. Riley, M, Schaecter, and H. E. Umbarger (ed.), Escherichia coli and Salmonella typhimurium: cellular and molecular biology. ASM Press, Washington, D.C.
53. Otto, K., and T. J. Silhavy. 2002. Surface sensing and adhesion of Escherichia coli controlled by the Cpx-signaling pathway. Proc. Natl. Acad. Sci. USA 99:2287-2292.
54. Pratt, L. A., W. Hsing, K. E. Gibson, and T. J. Silhavy. 1996. From acids to osmZ: multiple factors influence synthesis of the OmpF and OmpC porins in Escherichia coli. Mol. Microbiol. 20:911-917.
55. Pratt, L. A., and T. J. Silhavy. 1996. The response regulator SprE controls the stability of RpoS. Proc. Natl. Acad. Sci. USA 93:2488-2492.
56. Prigent-Combaret, C., E. Brombacher, O. Vidal, A. Ambert, P. Lijeune, P. Landini, and C. Dorel. 2001. Complex regulatory network controls initial adhesion and biofilm formation in Escherichia coli via regulation of the csgD gene. J. Bacteriol. 183:7213-7223.
57. Raivio, T. L., and T. J. Silhavy. 2001. Periplasmic stress and ECF sigma factors. Annu. Rev. Microbiol. 55:591-624.
58. Raivio, T. L., and T. J. Silhavy. 1997. Transduction of envelope stress in Escherichia coli by the Cpx two-component system. J. Bacteriol. 179:7724-7733.
59. Ramani, N., L. Huang, and M. Freundlich. 1992. In vitro interactions of integration host factor with the ompF promoter-regulatory region of Escherichia coli. Mol. Gen. Genet. 231:248-255.
60. Rhodius. V., and C. A. Gross. Personal communication.
61. Russo, F. D., and T. J. Silhavy. 1991. EnvZ controls the concentration of phosphorylated OmpR to mediate osmoregulation of the porin genes. J. Mol. Biol. 222:567-580.
62. Slauch, J. M., and T. J. Silhavy. 1989. Genetic analysis of the switch that controls porin gene expression in Escherichia coli K-12. J. Mol. Biol. 210:281-292.
63. Slauch, J. M., and T. J. Silhavy. 1996. The porin regulon: a paradigm for the two-component regulatory systems, p. 383-417. In E. C. C. Lin and A. S. Lynch (ed.), Regulation of gene expression in Escherichia coli. Chapman & Hall, New York, N.Y.
64. Snyder, W. B., L. J. Davis, P. N. Danese, C. L. Cosma, and T. J. Silhavy. 1995. Overproduction of NlpE, a new outer membrane lipoprotein, suppresses the toxicity of periplasmic LacZ by activation of the Cpx signal transduction pathway. J. Bacteriol. 177:4216-4223.
65. Soncini, F. C., and E. A. Groisman. 1996. Two-component regulatory systems can interact to process multiple environmental signals. J. Bacteriol. 178:6796-6801.
66. Tsung, K., R. E. Brissette, and M. Inouye. 1989. Identification of the DNA-binding domain of the OmpR protein required for transcriptional activation of the ompF and ompC genes of Escherichia coli by in vivo DNA footprinting. J. Biol. Chem. 264:10104-10109.
67. Wanner, B. L., and M. R. Wilmes-Riesenberg. 1992. Involvement of phosphotransacetylase, acetate kinase, and acetyl phosphate synthesis in control of the phosphate regulon in Escherichia coli. J. Bacteriol. 174:2124-2130.
68. Wolfe, A. J. 2005. The acetate switch. Microbiol. Mol. Biol Rev. 69:12-50.