Skip to main content
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1984 Sep;159(3):883–887. doi: 10.1128/jb.159.3.883-887.1984

envZ mediates transcriptional control by local anesthetics but is not required for osmoregulation in Escherichia coli.

M Villarejo, C C Case
PMCID: PMC215741  PMID: 6434513

Abstract

Expression of a particular set of exported protein genes (ompF, ompC, phoA, and malE) can be specifically altered in three ways: variation in the osmotic strength of the growth medium, mutations in the regulatory locus envZ, or treatment with sublethal concentrations of the local anesthetic procaine. To clarify relationships among these factors in the regulation of transcription, expression of the affected genes was compared in envZ+ and envZ22(Am) mutant strains grown in media of differing osmolarities with and without procaine. Loss of the envZ product resulted in complete resistance of gene expression to procaine, supporting the hypothesis that envZ mediates procaine inhibition. The specific activity of the phoA product, alkaline phosphatase, was elevated in envZ22 mutant strains, while the amounts of both the OmpC and OmpF porins were reduced. Osmotic control of phoA and ompC was retained in the absence of envZ function, but osmoregulation of ompF was lost. Therefore, the envZ product is somehow involved in the complex regulation of all four target genes, but is not solely responsible for osmoregulation.

Full text

PDF
883

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Alphen W. V., Lugtenberg B. Influence of osmolarity of the growth medium on the outer membrane protein pattern of Escherichia coli. J Bacteriol. 1977 Aug;131(2):623–630. doi: 10.1128/jb.131.2.623-630.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bassford P. J., Jr, Diedrich D. L., Schnaitman C. L., Reeves P. Outer membrane proteins of Escherichia coli. VI. Protein alteration in bacteriophage-resistant mutants. J Bacteriol. 1977 Aug;131(2):608–622. doi: 10.1128/jb.131.2.608-622.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Casadaban M. J. Transposition and fusion of the lac genes to selected promoters in Escherichia coli using bacteriophage lambda and Mu. J Mol Biol. 1976 Jul 5;104(3):541–555. doi: 10.1016/0022-2836(76)90119-4. [DOI] [PubMed] [Google Scholar]
  4. ECHOLS H., GAREN A., GAREN S., TORRIANI A. Genetic control of repression of alkaline phosphatase in E. coli. J Mol Biol. 1961 Aug;3:425–438. doi: 10.1016/s0022-2836(61)80055-7. [DOI] [PubMed] [Google Scholar]
  5. Garrett S., Taylor R. K., Silhavy T. J. Isolation and characterization of chain-terminating nonsense mutations in a porin regulator gene, envZ. J Bacteriol. 1983 Oct;156(1):62–69. doi: 10.1128/jb.156.1.62-69.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Granett S., Villarejo M. Regulation of gene expression in Escherichia coli by the local anesthetic procaine. J Mol Biol. 1982 Sep 15;160(2):363–367. doi: 10.1016/0022-2836(82)90181-4. [DOI] [PubMed] [Google Scholar]
  7. Granett S., Villarejo M. Selective inhibition of carbohydrate transport by the local anesthetic procaine in Escherichia coli. J Bacteriol. 1981 Aug;147(2):289–296. doi: 10.1128/jb.147.2.289-296.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Hall M. N., Silhavy T. J. Genetic analysis of the ompB locus in Escherichia coli K-12. J Mol Biol. 1981 Sep 5;151(1):1–15. doi: 10.1016/0022-2836(81)90218-7. [DOI] [PubMed] [Google Scholar]
  9. Hall M. N., Silhavy T. J. The ompB locus and the regulation of the major outer membrane porin proteins of Escherichia coli K12. J Mol Biol. 1981 Feb 15;146(1):23–43. doi: 10.1016/0022-2836(81)90364-8. [DOI] [PubMed] [Google Scholar]
  10. Hall M. N., Silhavy T. J. Transcriptional regulation of Escherichia coli K-12 major outer membrane protein 1b. J Bacteriol. 1979 Nov;140(2):342–350. doi: 10.1128/jb.140.2.342-350.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Kawaji H., Mizuno T., Mizushima S. 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. 1979 Dec;140(3):843–847. doi: 10.1128/jb.140.3.843-847.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
  13. Liljeström P., Mättänen P. L., Palva E. T. Cloning of the regulatory locus ompB of Salmonella typhimurium LT-2. II. Identification of the envZ gene product, a protein involved in the expression of the porin proteins. Mol Gen Genet. 1982;188(2):190–194. doi: 10.1007/BF00332674. [DOI] [PubMed] [Google Scholar]
  14. Lugtenberg B., Peters R., Bernheimer H., Berendsen W. Influence of cultural conditions and mutations on the composition of the outer membrane proteins of Escherichia coli. Mol Gen Genet. 1976 Sep 23;147(3):251–262. doi: 10.1007/BF00582876. [DOI] [PubMed] [Google Scholar]
  15. Lundrigan M. D., Earhart C. F. Gene envY of Escherichia coli K-12 affects thermoregulation of major porin expression. J Bacteriol. 1984 Jan;157(1):262–268. doi: 10.1128/jb.157.1.262-268.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Lundrigan M., Earhart C. F. Reduction in three iron-regulated outer membrane proteins and protein a by the Escherichia coli K-12 perA mutation. J Bacteriol. 1981 May;146(2):804–807. doi: 10.1128/jb.146.2.804-807.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Mizuno T., Wurtzel E. T., Inouye M. Osmoregulation of gene expression. II. DNA sequence of the envZ gene of the ompB operon of Escherichia coli and characterization of its gene product. J Biol Chem. 1982 Nov 25;257(22):13692–13698. [PubMed] [Google Scholar]
  18. Ozawa Y., Mizushima S. Regulation of outer membrane porin protein synthesis in Escherichia coli K-12: ompF regulates the expression of ompC. J Bacteriol. 1983 May;154(2):669–675. doi: 10.1128/jb.154.2.669-675.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Pugsley A. P., Conrard D. J., Schnaitman C. A., Gregg T. I. In vivo effects of local anesthetics on the production of major outer membrane proteins by Escherichia coli. Biochim Biophys Acta. 1980 Jun 20;599(1):1–12. doi: 10.1016/0005-2736(80)90051-6. [DOI] [PubMed] [Google Scholar]
  20. Pugsley A. P., Schnaitman C. A. Identification of three genes controlling production of new outer membrane pore proteins in Escherichia coli K-12. J Bacteriol. 1978 Sep;135(3):1118–1129. doi: 10.1128/jb.135.3.1118-1129.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Sarma V., Reeves P. Genetic locus (ompB) affecting a major outer-membrane protein in Escherichia coli K-12. J Bacteriol. 1977 Oct;132(1):23–27. doi: 10.1128/jb.132.1.23-27.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Taylor R. K., Hall M. N., Enquist L., Silhavy T. J. Identification of OmpR: a positive regulatory protein controlling expression of the major outer membrane matrix porin proteins of Escherichia coli K-12. J Bacteriol. 1981 Jul;147(1):255–258. doi: 10.1128/jb.147.1.255-258.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Taylor R. K., Hall M. N., Silhavy T. J. Isolation and characterization of mutations altering expression of the major outer membrane porin proteins using the local anaesthetic procaine. J Mol Biol. 1983 May 25;166(3):273–282. doi: 10.1016/s0022-2836(83)80085-0. [DOI] [PubMed] [Google Scholar]
  24. Tribhuwan R. C., Pradhan D. S. Induction of alkaline phosphatase in Escherichia coli: effect of procaine hydrochloride. J Bacteriol. 1977 Aug;131(2):431–437. doi: 10.1128/jb.131.2.431-437.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Verhoef C., Lugtenberg B., van Boxtel R., de Graaff P., Verheij H. Genetics and biochemistry of the peptidoglycan-associated proteins b and c of Escherichia coli K12. Mol Gen Genet. 1979 Jan 31;169(2):137–146. doi: 10.1007/BF00271664. [DOI] [PubMed] [Google Scholar]
  26. Villarejo M., Davis J. L., Granett S. Osmoregulation of alkaline phosphatase synthesis in Escherichia coli K-12. J Bacteriol. 1983 Nov;156(2):975–978. doi: 10.1128/jb.156.2.975-978.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Wandersman C., Moreno F., Schwartz M. Pleiotropic mutations rendering Escherichia coli K-12 resistant to bacteriophage TP1. J Bacteriol. 1980 Sep;143(3):1374–1383. doi: 10.1128/jb.143.3.1374-1383.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Wanner B. L., Sarthy A., Beckwith J. Escherichia coli pleiotropic mutant that reduces amounts of several periplasmic and outer membrane proteins. J Bacteriol. 1979 Oct;140(1):229–239. doi: 10.1128/jb.140.1.229-239.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Wurtzel E. T., Chou M. Y., Inouye M. Osmoregulation of gene expression. I. DNA sequence of the ompR gene of the ompB operon of Escherichia coli and characterization of its gene product. J Biol Chem. 1982 Nov 25;257(22):13685–13691. [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES