Abstract
AcrAB is a constitutively expressed, major multidrug efflux system of Escherichia coli. We have purified the cytoplasmic membrane component, AcrB, to near homogeneity, and reconstituted the protein into proteoliposomes. In the presence of DeltapH (outside acid), the protein catalyzed the extrusion of fluorescent phospholipids, which were then trapped by protein-free acceptor vesicles. Known substrates of AcrAB, such as bile acids, erythromycin, and cloxacillin, inhibited this activity. Addition of various drugs to AcrB-containing proteoliposomes, in the presence of DeltapH (inside acid) resulted in proton efflux, suggesting that AcrB is a proton antiporter. Interestingly, fluorescent lipid extrusion was accelerated strongly by the periplasmic protein AcrA in the presence of Mg2+, and at pH 5.0 AcrA alone produced a slow mixing of lipids of different vesicles, without causing the mixing of intravesicular material. These results suggest that AcrA brings two membranes together, and under certain conditions may even cause the fusion of at least the outer leaflets of the membranes, contributing to the ability of the AcrAB-TolC system to pump drugs out directly into the medium.
MeSH Terms
Bacterial Proteins/genetics,metabolism
Biological Transport
Carrier Proteins/genetics,metabolism
Cytoplasmic Granules/metabolism
Drug Resistance, Microbial
Escherichia coli/genetics,metabolism,ultrastructure
Escherichia coli Proteins
Gene Expression Regulation, Bacterial
Hydrogen-Ion Concentration
Lipoproteins/genetics,metabolism
Magnesium/metabolism
Membrane Proteins/genetics,metabolism
Membrane Transport Proteins
Multidrug Resistance-Associated Proteins
Protons
Chemicals
AcrA protein, E coli
AcrB protein, E coli
Bacterial Proteins
Carrier Proteins
Escherichia coli Proteins
Lipoproteins
Membrane Proteins
Membrane Transport Proteins
Multidrug Resistance-Associated Proteins
Protons
Magnesium
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Zgurskaya H I
Department of Molecular and Cell Biology, University of California, Berkeley, CA 94720-3206, USA.
Nikaido H
References (29)
29 references, click to expand
-
A rapid, sensitive, and specific method for the determination of protein in dilute solution.
Anal Biochem. 1973 Dec;56(2):502-14
PMID: 4128882
-
Lipid-anchored influenza hemagglutinin promotes hemifusion, not complete fusion.
Cell. 1994 Jan 28;76(2):383-91
PMID: 8293471
-
Use of resonance energy transfer to monitor membrane fusion.
Biochemistry. 1981 Jul 7;20(14):4093-9
PMID: 7284312
-
pH-induced destabilization of phosphatidylethanolamine-containing liposomes: role of bilayer contact.
Biochemistry. 1984 Mar 27;23(7):1532-8
PMID: 6722105
-
Electrogenic H+ translocation by the plasma membrane ATPase of Neurospora. Studies on plasma membrane vesicles and reconstituted enzyme.
J Biol Chem. 1984 Jun 25;259(12):7884-92
PMID: 6234306
-
Solute distributions and trapping efficiencies observed in freeze-thawed multilamellar vesicles.
Biochim Biophys Acta. 1985 Jul 11;817(1):193-6
PMID: 4005257
-
Phosphatidylcholine translocase: a physiological role for the mdr2 gene.
Cell. 1994 Jul 1;77(7):1071-81
PMID: 7912658
-
A family of extracytoplasmic proteins that allow transport of large molecules across the outer membranes of gram-negative bacteria.
J Bacteriol. 1994 Jul;176(13):3825-31
PMID: 8021163
-
Two novel families of bacterial membrane proteins concerned with nodulation, cell division and transport.
Mol Microbiol. 1994 Mar;11(5):841-7
PMID: 8022262
-
Role of efflux pump(s) in intrinsic resistance of Pseudomonas aeruginosa: resistance to tetracycline, chloramphenicol, and norfloxacin.
Antimicrob Agents Chemother. 1994 Aug;38(8):1732-41
PMID: 7986003
-
Role of outer membrane barrier in efflux-mediated tetracycline resistance of Escherichia coli.
J Bacteriol. 1995 Feb;177(4):998-1007
PMID: 7860612
-
Efflux pumps and drug resistance in gram-negative bacteria.
Trends Microbiol. 1994 Dec;2(12):489-93
PMID: 7889326
-
Genes acrA and acrB encode a stress-induced efflux system of Escherichia coli.
Mol Microbiol. 1995 Apr;16(1):45-55
PMID: 7651136
-
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):306-8
PMID: 8550435
-
Multidrug resistance pumps in bacteria: variations on a theme.
Trends Biochem Sci. 1994 Mar;19(3):119-23
PMID: 8203018
-
Evidence that TolC is required for functioning of the Mar/AcrAB efflux pump of Escherichia coli.
J Bacteriol. 1996 Oct;178(19):5803-5
PMID: 8824631
-
Multidrug efflux pumps of gram-negative bacteria.
J Bacteriol. 1996 Oct;178(20):5853-9
PMID: 8830678
-
Active efflux of bile salts by Escherichia coli.
J Bacteriol. 1997 Apr;179(8):2512-8
PMID: 9098046
-
Mechanisms of multidrug transporters.
FEMS Microbiol Rev. 1997 Aug;21(1):55-84
PMID: 9299702
-
Role of the acrAB locus in organic solvent tolerance mediated by expression of marA, soxS, or robA in Escherichia coli.
J Bacteriol. 1997 Oct;179(19):6122-6
PMID: 9324261
-
Preparation and reconstitution of membrane-associated maltose transporter complex of Escherichia coli.
Methods Enzymol. 1998;292:20-9
PMID: 9711543
-
Multidrug efflux pump AcrAB of Salmonella typhimurium excretes only those beta-lactam antibiotics containing lipophilic side chains.
J Bacteriol. 1998 Sep;180(17):4686-92
PMID: 9721312
-
Transbilayer movement of NBD-labeled phospholipids in red blood cell membranes: outward-directed transport by the multidrug resistance protein 1 (MRP1).
Biochemistry. 1998 Oct 20;37(42):14833-7
PMID: 9778357
-
AcrA is a highly asymmetric protein capable of spanning the periplasm.
J Mol Biol. 1999 Jan 8;285(1):409-20
PMID: 9878415
-
Porin channels in intact cells of Escherichia coli are not affected by Donnan potentials across the outer membrane.
J Biol Chem. 1988 Jan 25;263(3):1182-7
PMID: 2447086
-
pH gradients across phospholipid membranes caused by fast flip-flop of un-ionized fatty acids.
Proc Natl Acad Sci U S A. 1992 Dec 1;89(23):11367-70
PMID: 1454821
-
Molecular cloning and characterization of acrA and acrE genes of Escherichia coli.
J Bacteriol. 1993 Oct;175(19):6299-313
PMID: 8407802
-
Fluorescent cellular indicators are extruded by the multidrug resistance protein.
J Biol Chem. 1993 Oct 15;268(29):21493-6
PMID: 8104940
-
Pyranine (8-hydroxy-1,3,6-pyrenetrisulfonate) as a probe of internal aqueous hydrogen ion concentration in phospholipid vesicles.
Biochemistry. 1981 Mar 17;20(6):1534-8
PMID: 6261798