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J Bacteriol. Oct 1996; 178(19): 5803–5805.
PMCID: PMC178425

Evidence that TolC is required for functioning of the Mar/AcrAB efflux pump of Escherichia coli.


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.

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Selected References

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  • Austin EA, Graves JF, Hite LA, Parker CT, Schnaitman CA. 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. [PMC free article] [PubMed]
  • 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. [PubMed]
  • 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. [PubMed]
  • Foreman DT, Martinez Y, Coombs G, Torres A, Kupersztoch YM. 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. [PubMed]
  • Fralick JA, Burns-Keliher LL. 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. [PMC free article] [PubMed]
  • Funahara Y, Nikaido H. Asymmetric localization of lipopolysaccharides on the outer membrane of Salmonella typhimurium. J Bacteriol. 1980 Mar;141(3):1463–1465. [PMC free article] [PubMed]
  • George AM, Levy SB. 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. [PMC free article] [PubMed]
  • Gilson L, Mahanty HK, Kolter R. Genetic analysis of an MDR-like export system: the secretion of colicin V. EMBO J. 1990 Dec;9(12):3875–3884. [PMC free article] [PubMed]
  • 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. [PMC free article] [PubMed]
  • 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. [PMC free article] [PubMed]
  • Leive L. The barrier function of the gram-negative envelope. Ann N Y Acad Sci. 1974 May 10;235(0):109–129. [PubMed]
  • Létoffé S, Ghigo JM, 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. [PMC free article] [PubMed]
  • Lewis K. Multidrug resistance pumps in bacteria: variations on a theme. Trends Biochem Sci. 1994 Mar;19(3):119–123. [PubMed]
  • Ma D, Alberti M, Lynch C, Nikaido H, Hearst JE. 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. [PubMed]
  • Ma D, Cook DN, Alberti M, Pon NG, Nikaido H, Hearst JE. Molecular cloning and characterization of acrA and acrE genes of Escherichia coli. J Bacteriol. 1993 Oct;175(19):6299–6313. [PMC free article] [PubMed]
  • Ma D, Cook DN, Alberti M, Pon NG, Nikaido H, Hearst JE. Genes acrA and acrB encode a stress-induced efflux system of Escherichia coli. Mol Microbiol. 1995 Apr;16(1):45–55. [PubMed]
  • Ma D, Cook DN, Hearst JE, Nikaido H. Efflux pumps and drug resistance in gram-negative bacteria. Trends Microbiol. 1994 Dec;2(12):489–493. [PubMed]
  • Misra R, Reeves PR. 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. [PMC free article] [PubMed]
  • Morona R, Manning PA, Reeves P. Identification and characterization of the TolC protein, an outer membrane protein from Escherichia coli. J Bacteriol. 1983 Feb;153(2):693–699. [PMC free article] [PubMed]
  • 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. [PMC free article] [PubMed]
  • Mühlradt PF, Golecki JR. 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. [PubMed]
  • Nagel de Zwaig R, Luria SE. Genetics and physiology of colicin-tolerant mutants of Escherichia coli. J Bacteriol. 1967 Oct;94(4):1112–1123. [PMC free article] [PubMed]
  • Nikaido H. Outer membrane of Salmonella typhimurium. Transmembrane diffusion of some hydrophobic substances. Biochim Biophys Acta. 1976 Apr 16;433(1):118–132. [PubMed]
  • Nikaido H. Prevention of drug access to bacterial targets: permeability barriers and active efflux. Science. 1994 Apr 15;264(5157):382–388. [PubMed]
  • Nikaido H, Nakae T. The outer membrane of Gram-negative bacteria. Adv Microb Physiol. 1979;20:163–250. [PubMed]
  • Nikaido H, Vaara M. Molecular basis of bacterial outer membrane permeability. Microbiol Rev. 1985 Mar;49(1):1–32. [PMC free article] [PubMed]
  • 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. [PMC free article] [PubMed]
  • 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. [PubMed]
  • Plésiat P, Nikaido H. Outer membranes of gram-negative bacteria are permeable to steroid probes. Mol Microbiol. 1992 May;6(10):1323–1333. [PubMed]
  • Schnaitman CA, Klena JD. Genetics of lipopolysaccharide biosynthesis in enteric bacteria. Microbiol Rev. 1993 Sep;57(3):655–682. [PMC free article] [PubMed]
  • 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. [PMC free article] [PubMed]
  • Wandersman C. Secretion across the bacterial outer membrane. Trends Genet. 1992 Sep;8(9):317–322. [PubMed]
  • 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. [PMC free article] [PubMed]
  • Webster RE. The tol gene products and the import of macromolecules into Escherichia coli. Mol Microbiol. 1991 May;5(5):1005–1011. [PubMed]
  • Whitney EN. The tolC locus in Escherichia coli K12. Genetics. 1971 Jan;67(1):39–53. [PMC free article] [PubMed]
  • Young KK, Edlin G. Physical and genetical analysis of bacteriophage T4 generalized transduction. Mol Gen Genet. 1983;192(1-2):241–246. [PubMed]

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