Indole induces the expression of multidrug exporter genes in Escherichia coli

Molecular Microbiology

Volumn 55, Issue 4, 2005, Pages 1113-1126

  Hirakawa, Hidetada ^a,b   Inazumi, Yoshihiko ^a,b   Masaki, Takeshi ^a,b   Hirata, Takahiro ^a,b   Yamaguchi, Akihito ^a,b  

^a OSAKA UNIVERSITY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CARBENICILLIN; CARRIER PROTEIN; DEOXYRIBONUCLEASE; DODECYL SULFATE SODIUM; INDOLE; MULTIDRUG EXPORTER PROTEIN; PROTEIN BAER; PROTEIN CPXR; RHODAMINE 6G; UNCLASSIFIED DRUG; XENOBIOTIC AGENT;

ACRD GENE; ARCE GENE; ARTICLE; BACTERIAL GENE; CONTROLLED STUDY; CUSB GENE; DELETION MUTANT; DNA FOOTPRINTING; EMRK GENE; ESCHERICHIA COLI; GEL MOBILITY SHIFT ASSAY; GENE DELETION; GENE EXPRESSION; GENE INDUCTION; MDTA GENE; MDTE GENE; MULTIDRUG RESISTANCE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN PHOSPHORYLATION; REGULATOR GENE; REPORTER GENE; SIGNAL TRANSDUCTION; YCEL GENE;

BASE SEQUENCE; CHROMOSOMES, BACTERIAL; DEOXYRIBONUCLEASE I; DNA FOOTPRINTING; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; INDOLES; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; MUTAGENESIS, SITE-DIRECTED; PLASMIDS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; XENOBIOTICS;

EID: 14544286364     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2004.04449.x     Document Type: Article

References (48)

1. Aguilar, P.S., Hernandez-Arriaga, A.M., Cybulski, L.E., Erazo, A.C., and de Mendoza, D. (2001) Molecular basis of thermosensing: a two-component signal transduction thermometer in Bacillus subtilis. EMBO J 20: 1681-1691.
2. Baca-DeLancey, R.R., South, M.M., Ding, X., and Rather, P.N. (1999) Escherichia coli genes regulated by cell-to-cell signaling. Proc Natl Acad Sci USA 96: 4610-4614.
3. Baranova, N., and Nikaido, H. (2002) The baeSR two-component regulatory system activates transcription of the yegMNOB (mdtABCD) transporter gene cluster in Escherichia coli, and increases its resistance to novobiocin and deoxycholate. J Bacteriol 184: 4168-4176.
4. Bassler, B.L. (2002) Small talk. Cell-to-cell communication in bacteria. Cell 109: 421-424.
5. Casadaban, M.J. (1976) Transposition and fusion of the lac genes to selected promoters in Escherichia coli using bacteriophage lambda and Mu. J Mol Biol 104: 541-555.
6. Chen, X., Schauder, S., Potier, N., Van Dorsselaer, A., Pelczer, I., and Bassler, B.L., and Hughson, P.M. (2002) Structural identification of a bacterial quorum-sensing signal containing boron. Nature 415: 545-549.
7. DeMoss, R.D., and Moser, K. (1969) Tryptophanase in diverse bacterial species. J Bacteriol 98: 167-171.
8. Elledge, S.J., and Davis, R.W. (1989) Position and density effects on repression by stationary and mobile DNA-binding proteins. Genes Dev 3: 185-197.
9. Fuqua, C., Parsek, M.R., and Greenberg, E.P. (2001) Regulation of gene expression by cell-to-cell communication: acyl-homoserine lactone quorum sensing. Annu Rev Genet 35: 439-468.
10. Garbe, T.R., Kobayashi, M., and Yukawa, H. (2000) Indole-inducible proteins in bacteria suggest membrane and oxidant toxicity. Arch Microbiol 173: 78-82.
11. Grkovic, S., Brown, M.H., and Skurray, R.A. (2002) Regulation of bacterial drug export systems. Microbiol Mol Biol Rev 66: 671-701.
12. Hashimoto-Gotoh, T., Yamaguchi, M., Yasojima, K., Tsujimura, A., Wakabayashi, Y., and Watanabe, Y. (2000) A set of temperature sensitive-replication/-segregation and temperature resistant plasmid vectors with different copy numbers and in an isogenic background (chloramphenicol, kanamycin, lacZ, repA, par, polA). Gene 241: 185-191.
13. Hirakawa, H., Nishino, K., Hirata, T., and Yamaguchi, A. (2003a) Comprehensive studies of drug resistance mediated by overexpression of response regulators of two-component signal transduction systems in Escherichia coli. J Bacteriol 185: 1851-1856.
14. Hirakawa, H., Nishino, K., Yamada, J., and Hirata, T., and Yamaguchi, A. (2003b) Beta-lactam resistance modulated by the overexpression of response regulators of two-component signal transduction systems in Escherichia coli. J Antimicrob Chemother 52: 576-582.
15. Hoch, J.A., and Varughese, K.I. (2001) Keeping signals straight in phosphorelay signal transduction. J Bacteriol 183: 4941-4949.
16. Kato, A., Ohnishi, H., Yamamoto, K., Furuta, E., Tanabe, H., and Utsumi, R. (2000) Transcription of emrKY is regulated by the EvgA-EvgS two-component system in Escherichia coli K-12. Biosci Biotechnol Biochem 64: 1203-1209.
17. Kawamura-Sato, K., Shibayama, K., Horii, T., Iimuma, Y., Arakawa, Y., and Ohta, M. (1999) Role of multiple efflux pumps in Escherichia coli in indole expulsion. FEMS Microbiol Lett 179: 345-352.
18. Kunkel, T.A. (1985) Rapid and efficient site-specific mutagenesis without phenotypic selection. Proc Natl Acad Sci USA 82: 488-492.
19. Link, A.J., Phillips, D., and Church, G.M. (1997) Methods for generating precise deletions and insertions in the genome of wild-type Escherichia coli: application to open reading frame characterization. J Bacteriol 179: 6228-6237.
20. Lomovskaya, O., Lewis, K., and Matin, A. (1995) EmrR is a negative regulator of the Escherichia coli multidrug resistance pump EmrAB. J Bacteriol 177: 2328-2334.
21. Ma, D., Alberti, M., Lynch, C., Nikaido, H., and Hearst, J.E. (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.
22. Ma, Z., Gong, S., Richard, H., Tucker, D.L., Conway, T., and Foster, J.W. (2003) GadE (YhiE) activates glutamate decarboxylase-dependent acid resistance in Escherichia coli K-12. Mol Microbiol 49: 1309-1320.
23. Martin, K., Morlin, G., Smith, A., Nordyke, A., Eisenstark, A., and Golomb, M. (1998) The tryptophanase gene cluster of Haemophilus influenzae type b: evidence for horizontal gene transfer. J Bacteriol 180: 107-118.
24. Martino, P.D., Fursy, R., Bret, L., Sundararaju, B., and Phillips, R.S. (2003) Indole can act as an extracellular signal to regulate biofilm formation of Escherichia coli and other indole-producing bacteria. Can J Microbiol 49: 443-449.
25. Masuda, N., and Church, G.M. (2003) Regulatory network of acid resistance genes in Escherichia coli. Mol Microbiol 48: 699-712.
26. Miller, J.H. (1992) A Short Course in Molecular Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
27. Mizuno, T. (1997) Compilation of all genes encoding two-component phosphotransfer signal transducers in the genome of Escherichia coli. DNA Res 4: 161-168.
28. Mizuno, T. (1998) His-Asp phosphotransfer signal transduction. J Biochem (Tokyo) 123: 555-563.
29. Nagasawa, S., Ishige, K., and Mizuno, T. (1993) Novel members of the two-component signal transduction genes in Escherichia coli. J Biochem (Tokyo) 114: 350-357.
30. Nagakubo, S., Nishino, K., Hirata, T., and Yamaguchi, A. (2002) The putative response regulator BaeR stimulates multidrug resistance of Escherichia coli via a novel multidrug exporter system, MdtABC. J Bacteriol 184: 4161-4167.
31. Nikaido, H. (1996) Multidrug efflux pumps of gram-negative bacteria. J Bacteriol 178: 5853-5859.
32. Nikaido, H. (1998) Antibiotic resistance caused by gram-negative multidrug efflux pumps. Clin Infect Dis 27: S32-S41.
33. Nishino, K., and Yamaguchi, A. (2001a) Analysis of a complete library of putative drug transporter genes in Escherichia coli. J Bacteriol 183: 5803-5812.
34. Nishino, K., and Yamaguchi, A. (2001b) Overexpression of the response regulator evgA of the two-component signal transduction system modulates multidrug resistance conferred by multidrug resistance transporters. J Bacteriol 183: 1455-1458.
35. Nishino, K., and Yamaguchi, A. (2002) EvgA of the two-component signal transduction system modulates production of the yhiUV multidrug transporter in Escherichia coli. J Bacteriol 184: 2319-2323.
36. Parkinson, J.S. (1993) Signal transduction schemes of bacteria. Cell 73: 857-871.
37. Poole, K. (2001) Multidrug efflux pumps and antimicrobial resistance in Pseudomonas aeruginosa and related organisms. J Mol Microbiol Biotechnol 3: 255-264.
38. Raffa, R.G., and Raivio, T.L. (2002) A third envelope stress signal transduction pathway in Escherichia coli. Mol Microbiol 45: 1599-1611.
39. Raivio, T.L., and Silhavy, T.J. (1999) The sigmaE and Cpx regulatory pathways: overlapping but distinct envelope stress responses. Curr Opin Microbiol 2: 159-165.
40. Rosenberg, E.Y., Bertenthal, D., Nilles, M.L., Bertrand, K.P., and Nikaido, H. (2003) Bile salts and fatty acids induce the expression of Escherichia coli AcrAB multidrug efflux pump through their interaction with Rob regulatory protein. Mol Microbiol 48: 1609-1619.
41. Snell, E.E. (1975) Tryptophanase: structure, catalytic activities, and mechanism of action. Adv Enzymol Relat Areas Mol Biol 42: 287-333.
42. Sulavik, M.C., Houseweart, C., Cramer, C., Jiwani, N., Murgolo, N., Greene, J., et al. (2001) Antibiotic susceptibility profiles of Escherichia constrains lacking multidrug efflux pump genes. Antimicrob Agents Chemother 45: 1126-1136.
43. Tucker, D.L., Tucker, N., Ma, Z., Foster, J.W., Miranda, R.L., Cohen, P.S., and Conway, T. (2003) Genes of the GadX-GadW regulon in Escherichia coli. J Bacteriol 185: 3190-3201.
44. Wang, D., Ding, X., and Rather, P.N. (2001) Indole can act as an extracellular signal in Escherichia coli. J Bacteriol 183: 4210-4216.
45. Wei, Y., Lee, J.M., Smulski, D.R., and LaRossa, R.A. (2001) Global impact of sdiA amplification revealed by comprehensive gene expression profiling of Escherichia coli. J Bacteriol 183: 2265-2272.
46. Wilson, D.O., Johnson, P., and McCord, B.R. (2001) Nonradiochemical DNasel footprinting by capillary electrophoresis. Electrophoresis 22: 1979-1986.
47. Wulf, P.D., McGuire, A.M., Liu, X., and Lin, E.C.C. (2002) Genome-wide profiling of promoter recognition by the two-component response regulator CpxR-P in Escherichia coli. J Biol Chem 277: 26652-26661.
48. Yamamoto, T., Tanaka, M., Nohara, C., Fukunaga, Y., and Yamagishi, S. (1981) Transposition of the oxacillin-hydrolyzing penicillinase gene. J Bacteriol 145: 808-813.