Abstract
A study examining the influence of TolC on AcrA, AcrR, and MarR1 mutants indicates that functional TolC is required for the operation of the AcrAB efflux system and for the expression of the Mar phenotype. That the effect of TolC on the AcrAB pump is not regulatory in nature is shown by studies measuring the influence of a tolC::Tn10 insertion mutation on the expression of an acrA::lacZ reporter fusion. These results are compatible with the hypothesis that TolC is a component of the AcrAB efflux complex.
Full Text
The Full Text of this article is available as a PDF (161.4 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Austin E. A., Graves J. F., Hite L. A., Parker C. T., Schnaitman C. A. Genetic analysis of lipopolysaccharide core biosynthesis by Escherichia coli K-12: insertion mutagenesis of the rfa locus. J Bacteriol. 1990 Sep;172(9):5312–5325. doi: 10.1128/jb.172.9.5312-5325.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Benz R., Bauer K. Permeation of hydrophilic molecules through the outer membrane of gram-negative bacteria. Review on bacterial porins. Eur J Biochem. 1988 Sep 1;176(1):1–19. doi: 10.1111/j.1432-1033.1988.tb14245.x. [DOI] [PubMed] [Google Scholar]
- Benz R., Maier E., Gentschev I. TolC of Escherichia coli functions as an outer membrane channel. Zentralbl Bakteriol. 1993 Apr;278(2-3):187–196. doi: 10.1016/s0934-8840(11)80836-4. [DOI] [PubMed] [Google Scholar]
- Foreman D. T., Martinez Y., Coombs G., Torres A., Kupersztoch Y. M. TolC and DsbA are needed for the secretion of STB, a heat-stable enterotoxin of Escherichia coli. Mol Microbiol. 1995 Oct;18(2):237–245. doi: 10.1111/j.1365-2958.1995.mmi_18020237.x. [DOI] [PubMed] [Google Scholar]
- Fralick J. A., Burns-Keliher L. L. Additive effect of tolC and rfa mutations on the hydrophobic barrier of the outer membrane of Escherichia coli K-12. J Bacteriol. 1994 Oct;176(20):6404–6406. doi: 10.1128/jb.176.20.6404-6406.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Funahara Y., Nikaido H. Asymmetric localization of lipopolysaccharides on the outer membrane of Salmonella typhimurium. J Bacteriol. 1980 Mar;141(3):1463–1465. doi: 10.1128/jb.141.3.1463-1465.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
- George A. M., Levy S. B. Amplifiable resistance to tetracycline, chloramphenicol, and other antibiotics in Escherichia coli: involvement of a non-plasmid-determined efflux of tetracycline. J Bacteriol. 1983 Aug;155(2):531–540. doi: 10.1128/jb.155.2.531-540.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gilson L., Mahanty H. K., Kolter R. Genetic analysis of an MDR-like export system: the secretion of colicin V. EMBO J. 1990 Dec;9(12):3875–3884. doi: 10.1002/j.1460-2075.1990.tb07606.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hiraga S., Niki H., Ogura T., Ichinose C., Mori H., Ezaki B., Jaffé A. Chromosome partitioning in Escherichia coli: novel mutants producing anucleate cells. J Bacteriol. 1989 Mar;171(3):1496–1505. doi: 10.1128/jb.171.3.1496-1505.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Koplow J., Goldfine H. Alterations in the outer membrane of the cell envelope of heptose-deficient mutants of Escherichia coli. J Bacteriol. 1974 Feb;117(2):527–543. doi: 10.1128/jb.117.2.527-543.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Leive L. The barrier function of the gram-negative envelope. Ann N Y Acad Sci. 1974 May 10;235(0):109–129. doi: 10.1111/j.1749-6632.1974.tb43261.x. [DOI] [PubMed] [Google Scholar]
- Lewis K. Multidrug resistance pumps in bacteria: variations on a theme. Trends Biochem Sci. 1994 Mar;19(3):119–123. doi: 10.1016/0968-0004(94)90204-6. [DOI] [PubMed] [Google Scholar]
- Létoffé S., Ghigo J. M., Wandersman C. Identification of two components of the Serratia marcescens metalloprotease transporter: protease SM secretion in Escherichia coli is TolC dependent. J Bacteriol. 1993 Nov;175(22):7321–7328. doi: 10.1128/jb.175.22.7321-7328.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ma D., Alberti M., Lynch C., Nikaido H., Hearst J. E. The local repressor AcrR plays a modulating role in the regulation of acrAB genes of Escherichia coli by global stress signals. Mol Microbiol. 1996 Jan;19(1):101–112. doi: 10.1046/j.1365-2958.1996.357881.x. [DOI] [PubMed] [Google Scholar]
- Ma D., Cook D. N., Alberti M., Pon N. G., Nikaido H., Hearst J. E. Genes acrA and acrB encode a stress-induced efflux system of Escherichia coli. Mol Microbiol. 1995 Apr;16(1):45–55. doi: 10.1111/j.1365-2958.1995.tb02390.x. [DOI] [PubMed] [Google Scholar]
- Ma D., Cook D. N., Alberti M., Pon N. G., Nikaido H., Hearst J. E. Molecular cloning and characterization of acrA and acrE genes of Escherichia coli. J Bacteriol. 1993 Oct;175(19):6299–6313. doi: 10.1128/jb.175.19.6299-6313.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ma D., Cook D. N., Hearst J. E., Nikaido H. Efflux pumps and drug resistance in gram-negative bacteria. Trends Microbiol. 1994 Dec;2(12):489–493. doi: 10.1016/0966-842x(94)90654-8. [DOI] [PubMed] [Google Scholar]
- Misra R., Reeves P. R. Role of micF in the tolC-mediated regulation of OmpF, a major outer membrane protein of Escherichia coli K-12. J Bacteriol. 1987 Oct;169(10):4722–4730. doi: 10.1128/jb.169.10.4722-4730.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Morona R., Manning P. A., Reeves P. Identification and characterization of the TolC protein, an outer membrane protein from Escherichia coli. J Bacteriol. 1983 Feb;153(2):693–699. doi: 10.1128/jb.153.2.693-699.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Morona R., Reeves P. The tolC locus of Escherichia coli affects the expression of three major outer membrane proteins. J Bacteriol. 1982 Jun;150(3):1016–1023. doi: 10.1128/jb.150.3.1016-1023.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mühlradt P. F., Golecki J. R. Asymmetrical distribution and artifactual reorientation of lipopolysaccharide in the outer membrane bilayer of Salmonella typhimurium. Eur J Biochem. 1975 Feb 21;51(2):343–352. doi: 10.1111/j.1432-1033.1975.tb03934.x. [DOI] [PubMed] [Google Scholar]
- Nagel de Zwaig R., Luria S. E. Genetics and physiology of colicin-tolerant mutants of Escherichia coli. J Bacteriol. 1967 Oct;94(4):1112–1123. doi: 10.1128/jb.94.4.1112-1123.1967. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nikaido H., Nakae T. The outer membrane of Gram-negative bacteria. Adv Microb Physiol. 1979;20:163–250. doi: 10.1016/s0065-2911(08)60208-8. [DOI] [PubMed] [Google Scholar]
- Nikaido H. Outer membrane of Salmonella typhimurium. Transmembrane diffusion of some hydrophobic substances. Biochim Biophys Acta. 1976 Apr 16;433(1):118–132. doi: 10.1016/0005-2736(76)90182-6. [DOI] [PubMed] [Google Scholar]
- Nikaido H. Prevention of drug access to bacterial targets: permeability barriers and active efflux. Science. 1994 Apr 15;264(5157):382–388. doi: 10.1126/science.8153625. [DOI] [PubMed] [Google Scholar]
- Nikaido H., Vaara M. Molecular basis of bacterial outer membrane permeability. Microbiol Rev. 1985 Mar;49(1):1–32. doi: 10.1128/mr.49.1.1-32.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Okusu H., Ma D., Nikaido H. AcrAB efflux pump plays a major role in the antibiotic resistance phenotype of Escherichia coli multiple-antibiotic-resistance (Mar) mutants. J Bacteriol. 1996 Jan;178(1):306–308. doi: 10.1128/jb.178.1.306-308.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pilsl H., Braun V. Novel colicin 10: assignment of four domains to TonB- and TolC-dependent uptake via the Tsx receptor and to pore formation. Mol Microbiol. 1995 Apr;16(1):57–67. doi: 10.1111/j.1365-2958.1995.tb02391.x. [DOI] [PubMed] [Google Scholar]
- Plésiat P., Nikaido H. Outer membranes of gram-negative bacteria are permeable to steroid probes. Mol Microbiol. 1992 May;6(10):1323–1333. doi: 10.1111/j.1365-2958.1992.tb00853.x. [DOI] [PubMed] [Google Scholar]
- Schnaitman C. A., Klena J. D. Genetics of lipopolysaccharide biosynthesis in enteric bacteria. Microbiol Rev. 1993 Sep;57(3):655–682. doi: 10.1128/mr.57.3.655-682.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tamaki S., Sato T., Matsuhashi M. Role of lipopolysaccharides in antibiotic resistance and bacteriophage adsorption of Escherichia coli K-12. J Bacteriol. 1971 Mar;105(3):968–975. doi: 10.1128/jb.105.3.968-975.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wandersman C., Delepelaire P. TolC, an Escherichia coli outer membrane protein required for hemolysin secretion. Proc Natl Acad Sci U S A. 1990 Jun;87(12):4776–4780. doi: 10.1073/pnas.87.12.4776. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wandersman C. Secretion across the bacterial outer membrane. Trends Genet. 1992 Sep;8(9):317–322. doi: 10.1016/0168-9525(92)90264-5. [DOI] [PubMed] [Google Scholar]
- Webster R. E. The tol gene products and the import of macromolecules into Escherichia coli. Mol Microbiol. 1991 May;5(5):1005–1011. doi: 10.1111/j.1365-2958.1991.tb01873.x. [DOI] [PubMed] [Google Scholar]
- Whitney E. N. The tolC locus in Escherichia coli K12. Genetics. 1971 Jan;67(1):39–53. doi: 10.1093/genetics/67.1.39. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Young K. K., Edlin G. Physical and genetical analysis of bacteriophage T4 generalized transduction. Mol Gen Genet. 1983;192(1-2):241–246. doi: 10.1007/BF00327673. [DOI] [PubMed] [Google Scholar]