Regulation of acrAB expression by cellular metabolites in Escherichia coli

Journal of Antimicrobial Chemotherapy

Volumn 69, Issue 2, 2014, Pages 390-399

  Ruiz, Cristian ^a,b   Levy, Stuart B ^a  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

AcrAB TolC; AcrR; Gene regulation; MarA; Multidrug efflux; SoxS

Indexed keywords

2,3 DIHYDROXYBENZOIC ACID; ACRAB PROTEIN; ADAPTOR PROTEIN; ARGININE DERIVATIVE; CYSTEINE; ENTEROCHELIN; FRUCTOSE 1,6 BISPHOSPHATE; PURINE; TOLC PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BIOSYNTHESIS; CELL METABOLISM; CELL MOTILITY; CONTROLLED STUDY; DELETION MUTANT; ESCHERICHIA COLI; FEEDBACK SYSTEM; FUSION GENE; GENE DELETION; GENE EXPRESSION; GENE FUSION; GENE INACTIVATION; GENETIC REGULATION; GENETIC STRAIN; GLUCONEOGENESIS; METABOLITE; NONHUMAN; OPERON; PROMOTER REGION; PROTEIN METABOLISM; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ACRAB-TOLC; ACRR; GENE REGULATION; MARA; MULTIDRUG EFFLUX; SOXS;

CELLS, CULTURED; CELLULAR MICROENVIRONMENT; ENERGY METABOLISM; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; OPERON; SIGNAL TRANSDUCTION;

EID: 84892467971     PISSN: 03057453     EISSN: 14602091     Source Type: Journal    
DOI: 10.1093/jac/dkt352     Document Type: Article

References (34)

1. Li XZ, Nikaido H. Efflux-mediated drug resistance in bacteria. Drugs 2004; 64: 159-204.
2. Blair JM, Piddock LJ. Structure, function and inhibition of RND efflux pumps in Gram-negative bacteria: an update. Curr Opin Microbiol 2009; 12:512-9.
3. Warner DM, Levy SB. Different effects of transcriptional regulators MarA, SoxS and Rob on susceptibility of Escherichia coli to cationic antimicrobial peptides (CAMPs): Rob-dependent CAMP induction of the marRAB operon. Microbiology 2010; 156: 570-8.
4. Sulavik MC, Houseweart C, Cramer C et al. Antibiotic susceptibility profiles of Escherichia coli strains lacking multidrug efflux pump genes. Antimicrob Agents Chemother 2001; 45: 1126-36.
5. Nishino K, Yamaguchi A. Analysis of a complete library of putative drug transporter genes in Escherichia coli. J Bacteriol 2001; 183: 5803-12.
6. Ma D, Alberti M, Lynch Cet al. The local repressor AcrR plays a modulating role in the regulation of acrAB genes of Escherichia coli by global stress signals. Mol Microbiol 1996; 19: 101-12.
7. Webber MA, Bailey AM, Blair JM et al. The global consequence of disruption of the AcrAB-TolC efflux pump in Salmonella enterica includes reduced expression of SPI-1 and other attributes required to infect the host. J Bacteriol 2009; 191: 4276-85.
8. Aoki SK, Malinverni JC, Jacoby K et al. Contact-dependent growth inhibition requires the essential outer membrane protein BamA (YaeT) as the receptor and the inner membrane transport protein AcrB. Mol Microbiol 2008; 70: 323-40.
9. Dhamdhere G, Zgurskaya HI. Metabolic shutdown in Escherichia coli cells lacking the outer membrane channel TolC. Mol Microbiol 2010; 77: 743-54.
10. Zgurskaya HI, Krishnamoorthy G, Ntreh A et al. Mechanism and function of the outermembranechannel TolC in multidrug resistance and physiology of enterobacteria. Front Microbiol 2011; 2: 189.
11. Rosner JL, Martin RG. An excretory function for the Escherichia coli outer membrane pore TolC: upregulation of marA and soxS transcription and Rob activity due to metabolites accumulated in tolC mutants. J Bacteriol 2009; 191: 5283-92.
12. Sambrook J, Russell DW. Molecular Cloning: A Laboratory Manual. 3rd edn. Cold Spring Harbor: Cold Spring Harbor Laboratory Press, 2001.
13. Baba T, Ara T, Hasegawa M et al. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol 2006; 2: 2006.0008.
14. Datsenko KA, Wanner BL. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 2000; 97:6640-5.
15. Ruiz C, Levy SB. Many chromosomal genes modulate MarA-mediated multidrug resistance in Escherichia coli. Antimicrob Agents Chemother 2010; 54: 2125-34.
16. Viveiros M, Dupont M, Rodrigues L et al. Antibiotic stress, genetic response and altered permeability of E. coli. PLoS One 2007; 2: e365.
17. Ruiz C, McMurry LM, Levy SB. Role of the multidrug resistance regulator MarA in global regulation of the hdeAB acid resistance operon in Escherichia coli. J Bacteriol 2008; 190: 1290-7.
18. Helling RB, Janes BK, Kimball H et al. Toxic waste disposal in Escherichia coli. J Bacteriol 2002; 184: 3699-703.
19. Chubiz LM, Rao CV. Aromatic acid metabolites of Escherichia coli K-12 can induce the marRAB operon. J Bacteriol 2010; 192: 4786-9.
20. Lomovskaya O, Warren MS, Lee A et al. Identificationandcharacterization of inhibitors of multidrug resistance efflux pumps in Pseudomonas aeruginosa: novel agents for combination therapy. Antimicrob Agents Chemother 2001; 45: 105-16.
21. Kern WV, Steinke P, Schumacher A et al. Effect of 1-(1-naphthylmethyl)- piperazine, a novel putative efflux pump inhibitor, on antimicrobial drug susceptibility in clinical isolates of Escherichia coli. J Antimicrob Chemother 2006; 57: 339-43.
22. Coldham NG, Webber M, Woodward MJ et al. A 96-well plate fluorescence assay for assessment of cellular permeability and active efflux in Salmonella enterica serovar Typhimurium and Escherichia coli. J Antimicrob Chemother 2010; 65: 1655-63.
23. Khalil S, Pawelek PD. Enzymatic adenylation of 2,3-dihydroxybenzoate is enhanced by a protein-protein interaction between Escherichia coli 2,3-dihydro-2,3-dihydroxybenzoate dehydrogenase (EntA) and 2,3-dihydroxybenzoate-AMP ligase (EntE). Biochemistry 2011; 50: 533-45.
24. Donahue JL, Bownas JL, Niehaus WG et al. Purification and characterization of glpX-encoded fructose 1,6-bisphosphatase, a new enzyme of the glycerol3-phosphateregulon of Escherichia coli. J Bacteriol 2000;182:5624-7.
25. Roberts IZ, Wolffe EL. Utilization of labeled fructose-6-phosphate and fructose-1,6-diphosphate by Escherichia coli. Arch Biochem Biophys 1951;33: 165-6.
26. Hall JA, Maloney PC. Transmembrane segment 11 of UhpT, the sugar phosphate carrier of Escherichia coli, is an a-helix that carries determinants of substrate selectivity. J Biol Chem2001; 276: 25107-13.
27. Singh R, Swick MC, Ledesma KR et al. Temporal interplay between efflux pumps and target mutations in development of antibiotic resistance in Escherichia coli. Antimicrob Agents Chemother 2012; 56: 1680-5.
28. Rosner JL, Martin RG. Reduction of cellular stress by TolC-dependent efflux pumps in Escherichia coli indicated by BaeSR and CpxARP activation of spy in efflux mutants. J Bacteriol 2013; 195: 1042-50.
29. Lee JH, Yeo WS, Roe JH. Induction of the sufA operon encoding Fe-S assembly proteins by superoxide generators and hydrogen peroxide: involvement of OxyR, IHF and an unidentified oxidant-responsive factor. Mol Microbiol 2004; 51: 1745-55.
30. Cohen SP, Levy SB, Foulds J et al. Salicylate induction of antibiotic resistance in Escherichia coli: activation of the mar operon and a mar-independent pathway. J Bacteriol 1993; 175: 7856-62.
31. Su CC, Rutherford DJ, Yu EW. Characterization of the multidrug efflux regulator AcrR from Escherichia coli. Biochem Biophys Res Commun 2007; 361: 85-90.
32. Gu M, Imlay JA. The SoxRS response of Escherichia coli is directly activated by redox-cycling drugs rather than by superoxide. Mol Microbiol 2011; 79: 1136-50.
33. Ruiz C, Levy SB. Use of functional interactions with MarA to discover chromosomal genes affecting antibiotic susceptibility in Escherichia coli. Int J Antimicrob Agents 2011; 37: 177-8.
34. Smith TG, Hoover TR. Deciphering bacterial flagellar gene regulatory networks in the genomic era. Adv Appl Microbiol 2009; 67: 257-95.