Role of the acrAB locus in organic solvent tolerance mediated by expression of marA, soxS, or robA in Escherichia coli

Journal of Bacteriology

Volumn 179, Issue 19, 1997, Pages 6122-6126

  White, David G ^a,b   Goldman, John D ^a,d   Demple, Bruce ^c   Levy, Stuart B ^a  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NORTH DAKOTA STATE UNIVERSITY   (United States)

^c HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^d School of Medicine ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTIC AGENT; ORGANIC SOLVENT;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENE; BACTERIUM MUTANT; ESCHERICHIA COLI; GENE DELETION; GENE EXPRESSION; GENE LOCUS; MULTIDRUG RESISTANCE; NONHUMAN; PRIORITY JOURNAL;

BACTERIA (MICROORGANISMS); ESCHERICHIA; ESCHERICHIA COLI; ESCHERICHIA COLI K12;

EID: 0030983818     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/jb.179.19.6122-6126.1997     Document Type: Article

References (50)

1. Alekshun, M., and S. B. Levy. Unpublished data.
2. Amabile-Cuevas, C. F., and B. Demple. 1991. Molecular characterization of the soxRS genes of Escherichia coli: two genes control a superoxide stress regulon. Nucleic Acids Res. 19:4479-4484.
3. Aono, R., K. Aibe, A. Inoue, and K. Horikoshi. 1991. Preparation of organic solvent tolerant mutants from Escherichia coli. Agric. Biol. Chem. 55:1935-1938.
4. Aono, R., T. Negishi, and H. Nakajima. 1994. Cloning of organic solvent tolerance gene ostA that determines n-hexane tolerance level in Escherichia coli. Appl. Environ. Microbiol. 60:4624-4626.
5. Aono, R., M. Kobayashi, H. Nakajima, and H. Kobayashi. 1995. A close correlation between improvement of organic solvent tolerance levels and alteration of resistance toward low levels of multiple antibiotics. Biosci. Biotech. Biochem. 59:213-218.
6. Ariza, R. R., S. P. Cohen, N. Bachhawat, S. B. Levy, and B. Demple. 1994. Repressor mutations in the marRAB operon that activate oxidative stress genes and multiple antibiotic resistance in Escherichia coli. J. Bacteriol. 176:143-148.
7. Ariza, R. R., Z. Li, N. Ringstad, and B. Demple. 1995. Activation of multiple antibiotic resistance and binding of stress-inducible promoters by Escherichia coli Rob protein. J. Bacteriol. 177:1655-1661.
8. Asako, H., H. Nakajima, K. Kobayashi, M. Kobayashi, and R. Aono. 1997. Organic solvent tolerance and antibiotic resistance increased by overexpression of marA in Escherichia coli. Appl. Environ. Microbiol 63:1428-1433.
9. Cohen, S. P., H. H. Hachler, and S. B. Levy. 1993. Genetic and functional analysis of the multiple antibiotic resistance (mar) locus in Escherichia coli. J. Bacteriol. 175:1484-1492.
10. Cohen, S. P., L. M. McMurry, D. C. Hooper, J. S. Wolfson, and S. B. Levy. 1989. Cross-resistance to fluoroquinolones in multiple-antibiotic-resistant (Mar) Escherichia coli selected by tetracycline or chloramphenicol: decreased drug accumulation associated with membrane changes in addition to OmpF reduction. Antimicrob. Agents Chemother. 33:1318-1325.
11. Cohen, S. P., L. M. McMurry, and S. B. Levy. 1988. marA locus causes decreased expression of OmpF porin in multiple-antibiotic-resistant (Mar) mutants of Escherichia coli. J. Bacteriol. 170:5416-5422.
12. Corwin, H., and S. M. Anderson. 1967. The effect of intramolecular hydrophobic bonding on partition coefficients. J. Org. Chem. 32:2583-2586.
13. De Smet, M. J., J. Kingman, and B. Witholt. 1978. The effect of toluene on the structure and permeability of the outer and cytoplasmic membrane of Escherichia coli. Biochim. Biophys. Acta 506:64-80.
14. Fawcett, W. P., and R. E. Wolf, Jr. 1994. Purification of a MalE-SoxS fusion protein and identification of the control sites of Escherichia coli superoxide-inducible genes. Mol. Microbiol. 14:669-679.
15. Ferrante, A. A., J. Augliera, K. Lewis, and A. M. Klibanov. 1995. Cloning of an organic solvent-resistance gene in Escherichia coli: the unexpected role of alkylhydroperoxide reductase. Proc. Natl. Acad. Sci. USA 92:7617-7621.
16. Gambino, L., S. J. Gracheck, and P. F. Miller. 1993. Overexpression of the MarA positive regulator is sufficient to confer multiple antibiotic resistance in Escherichia coli. J. Bacteriol. 175:2888-2894.
17. George, A. M., and S. B. Levy. 1983. Amplifiable resistance to tetracycline, chloramphenicol, and other antibiotics in Escherichia coli: involvement of a non-plasmid-determined efflux of tetracycline. J. Bacteriol. 155:531-540.
18. Goldman, J. D., D. G. White, and S. B. Levy. 1996. The multiple antibiotic resistance (mar) locus protects Escherichia coli from rapid cell killing by fluoroquinolones. Antimicrob. Agents Chemother. 40:1266-1269.
19. Goldman, J. D., D. G. White, and S. B. Levy. 1996. A central role for the multiple antibiotic resistance (mar) locus in E. coli in organic solvent tolerance abstr. A115, p. 153. In Abstracts of the 96th General Meeting of the American Society for Microbiology 1996. American Society for Microbiology, Washington, D.C.
20. Greenberg, J. T., J. H. Chou, P. Monach, and B. Demple. 1991. Activation of oxidative stress genes by mutations at the soxQ/cfxB/marA locus of Escherichia coli. J. Bacteriol. 173:4433-4439.
21. Greenberg, J. T., P. Monach, J. H. Chou, P. D. Josephy, and B. Demple. 1990. Positive control of global antioxidant defense regulon activated by superoxide-generating agents in Escherichia coli. Proc. Natl. Acad. Sci. USA 87:6181-6185.
22. Gustafson, J., and S. B. Levy. Unpublished data.
23. Hamilton, C. M., M. Aldema, B. K. Washburn, P. Babizke, and S. Kushner. 1989. New method for generating deletions and gene replacement in Escherichia coli. J. Bacteriol. 173:2888-2894.
24. Hansch, C., M. R. Muir, T. Fujita, P. P. Maloney, F. Geiger, and M. Streich 1963. The correlation of biological activity of plant growth regulators and chloromycetin derivatives with Hammett constants and partition coefficients. J. Am. Chem. Soc. 85:2817-2824.
25. Hansch, C., and T. Fujita. 1964. p-r-π analysis. A method for correlation of biological activity and chemical structure. J. Am. Chem. Soc. 86:1616-1626.
26. ow shake-flask values and capacity factors derived from reversed-phase high performance liquid chromatography for n-alkylbenzeds and some OECD reference substances. J. Chromatogr. 282:315-332.
27. Heipieper, H. J., F. J. Weber, J. Sikkema, H. Keweloh, and J. A. M. de Bont. 1994. Mechanisms of resistance of whole cells to toxic organic solvents. Trends Biotechnol. 12:409-415.
28. Inoue, A., and K. Horikoshi. 1989. A pseudomonas thrives in high concentrations of toluene. Nature (London) 338:264-265.
29. Isken, S., and J. A. M. de Bont. 1996. Active efflux of toluene in a solvent-resistant bacterium. J. Bacteriol. 178:6056-6058.
30. Jackson, R. W., and J. A. Demoss. 1965. Effects of toluene on Escherichia coli. J. Bacteriol. 90:1420-1425.
31. Jair, K.-W., X. Yu, K. Skarstad, B. Thony, N. Fujita, A. Ishihama, and R. E. Wolf, Jr. 1996. Transcriptional activation of promoters of the superoxide and multiple antibiotic resistance regulons by Rob, a binding protein of the Escherichia coli origin of chromosomal replication. J. Bacteriol. 178:2507-2513.
32. Li, Z. Y., and B. Demple. 1994. SoxS, an activator of superoxide stress genes in Escherichia coli: purification and interaction with DNA. J. Biol. Chem. 269:18371-18377.
33. Ma, D., D. N. Cook, M. Alberti, N. G. Pon, H. Nikaido, and J. E. Hearst. 1995. Genes acrA and acrB encode a stress induced efflux system of Escherichia coli. Mol. Microbiol. 16:45-55.
34. Ma, D., M. Alberti, C. Lynch, H. Nikaido, and J. E. Hearst. 1996. The local repressor AcrR plays a modulating role in the regulation of acrAB genes of Escherichia coli by global stress signals. Mol. Microbiol. 19:101-112.
35. Maneewannakul, K., and S. B. Levy. 1996. Identification of mar mutants among quinolone-resistant clinical isolates of Escherichia coli. Antimicrob. Agents Chemother. 40:1695-1698.
36. Martin, R. G., and J. L. Rosner. 1995. Binding of purified multiple antibiotic resistance repressor protein (MarR) to mar operator sequences. Proc. Natl. Acad. Sci. USA 92:5456-5460.
37. McMurry, L. M., A. M. George, and S. B. Levy. 1994. Active efflux of chloramphenicol in susceptible Escherichia coli strains and in multiple-antibiotic-resistant (Mar) mutants. Antimicrob. Agents Chemother. 38:542-546.
38. Miller, P. F., L. F. Gambino, M. C. Sulavik, and S. J. Gracheck. 1994. Genetic relationship between soxRS and mar loci in promoting multiple antibiotic resistance in Escherichia coli. Antimicrob. Agents Chemother. 38:1773-1779.
39. Nakajima, H., K. Kobayashi, M. Kobayashi, H. Asako, and R. Aono. 1995. Overexpression of the robA gene increases organic solvent tolerance and multiple antibiotic and heavy metal ion resistance in Escherichia coli. Appl. Environ. Microbiol. 61:2302-2307.
40. Nakajima, H. K., H. Kobayashi, R. Aono, and K. Horikoshi. 1995. soxRS gene increased the level of organic solvent tolerance in Escherichia coli. Biosci. Biotechnol. Biochem. 59:1323-1325.
41. Nunoshiba, T., E. Hidalgo, C. F. Amabile-Cuevas, and B. Demple 1992. Two-stage control of an oxidative stress regulon: the Escherichia coli SoxR protein triggers redox-inducible expression of the soxS regulatory gene. J. Bacteriol. 174:6054-6060.
42. Okusu, H., D. Ma, and H. Nikaido. 1996. AcrAB efflux pump plays a major role in the antibiotic resistance phenotype of Escherichia coli multiple-antibiotic-resistance (Mar) mutants. J. Bacteriol. 178:306-308.
43. Rosner, J. L., and J. L. Slonczewski. 1994. Dual regulation of inaA by the multiple antibiotic resistance (Mar) and superoxide stress response (SoxRS) systems of Escherichia coli. J. Bacteriol. 176:6262-6269.
44. Seoane, A. S., and S. B. Levy. 1995. Characterization of MarR, the repressor of the multiple antibiotic resistance (mar) operon in Escherichia coli. J. Bacteriol. 177:3414-3419.
45. Skarstad, K., B. Thony, D. Hwang, and A. Kornberg. 1993. A novel binding protein of the origin of Escherichia coli chromosome. J. Biol. Chem. 268: 5365-5370.
46. Touati, D. 1983. Cloning and mapping of the manganese superoxide dismutase gene (sodA) of Escherichia coli RDEC-1 and DNA sequence of the major structural subunit. Infect. Immun. 58:1124-1128.
47. White, D. G., W. Yan, and S. B. Levy. 1994. Functional characterization of the chromosomal multiple antibiotic resistance (mar) locus in Escherichia coli, abstr. A-104, p. 20. In Abstracts of the 94th General Meeting of the American Society for Microbiology 1994. American Society for Microbiology, Washington, D.C.
48. Woodringh, C. L. 1973. Effects of toluene and phenylethyl alcohol on the ultrastructure of Escherichia coli. J. Bacteriol. 114:1359-1361.
49. Wu, J., and B. Weiss. 1991. Two divergently transcribed genes, soxR and soxS, control a superoxide response regulon of Escherichia coli. J. Bacteriol. 173:2864-2871.
50. Yan, W., S. P. Cohen, and S. B. Levy. 1992. Three putative proteins in the mar operon mediate intrinsic multidrug resistance in Escherichia coli, abstr. A-26, p. 5. In Abstracts of the 92nd General Meeting of the American Society for Microbiology 1992. American Society for Microbiology, Wasnington, D.C.