Mycobacterium tuberculosis efpA encodes an efflux protein of the QacA transporter family

Clinical and Diagnostic Laboratory Immunology

Volumn 4, Issue 1, 1997, Pages 23-32

  Doran, James L ^a,b   Pang, Yijun ^c,h   Mdluli, Khizimuzi E ^a,b,i   Moran, Alison J ^a,b   Victor, Tommie C ^d   Stokes, Richard W ^b,e,f   Mahenthiralingam, Eshwar ^b,e,f   Kreiswirth, Barry N ^g   Butt, Jennifer L ^d   Baron, Gerald S ^a   Treit, Janice D ^a,b   Kerr, Valerie J ^a,b   Van Helden, Paul D ^d   Roberts, Marilyn C ^c   Nano, Francis E ^a,b  

^a UNIVERSITY OF VICTORIA   (Canada)

^b Canadian Bacterial Diseases Network   (Canada)

^c UNIVERSITY OF WASHINGTON   (United States)

^d STELLENBOSCH UNIVERSITY   (South Africa)

^e BC CHILDREN S HOSPITAL   (Canada)

^f UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^g PUBLIC HEALTH RESEARCH INSTITUTE   (United States)

^h UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

ⁱ NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EFFLUX PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTIBIOTIC RESISTANCE; ARTICLE; DNA SEQUENCE; MACROPHAGE; MOUSE; MULTIDRUG RESISTANCE; MYCOBACTERIUM AVIUM; MYCOBACTERIUM BOVIS; MYCOBACTERIUM INTRACELLULARE; MYCOBACTERIUM LEPRAE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL;

EID: 12644298635     PISSN: 1071412X     EISSN: None     Source Type: Journal    
DOI: 10.1128/cdli.4.1.23-32.1997     Document Type: Article

References (70)

1. Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.
2. Anderson, S. G. E., and P. M. Sharp. 1996. Codon usage in the Mycobacterium tuberculosis complex. Microbiology 142:915-925.
3. Balasubramian, V., M. S. Pavelka, Jr., S. S. Bardarov, J. Martin, T. R. Weisbrod, R. A. McAdam, B. R. Bloom, and W. R. Jacobs, Jr. 1996. Allelic exchange in Mycobacterium tuberculosis with long linear recombination substrates. J. Bacteriol. 178:273-279.
4. Banerjee, A., E. Dubnau, A. Quémard, V. Balasubramian, K. S. Um, T. Wilson, D. Collins, G. de Lisle, and W. R. Jacobs, Jr. 1994. inhA, a gene encoding a target for isoniazid and ethionamide in Mycobacterium tuberculosis. Science 263:227-230.
5. Bergh, S., and S. T. Cole. 1994. MycDB: an integrated mycobacterial database. Mol. Microbiol. 5:517-534.
6. Bibb, M. J., P. R. Findlay, and M. W. Johnson. 1984. The relationship between base composition and codon usage in bacterial genes and its use in the simple and reliable identification of protein coding sequences. Gene 30:157-166.
7. Bifani, P. J., B. B. Plikaytis, V. Kapur, K. Stockbauer, X. Pan, M. L. Lutfey, S. L. Moghazeh, W. Eisner, T. M. Daniel, M. H. Kaplan, J. T. Crawford, J. M. Musser, and B. N. Kreiswirth. 1996. Origin and interstate spread of a New York City multidrug-resistant Mycobacterium tuberculosis clone family. JAMA 275:487-489.
8. Bloch, A. B., G. M. Cauthen, I. M. Onorato, K. G. Dansbury, G. D. Kelly, C. R. Driver, and D. E. Snider. 1994. Nationwide survey of drug-resistant tuberculosis in the United States. JAMA 271:665-671.
9. Coque, J. J. R., P. Liras, and J. F. Martin. 1993. Genes for a beta-lactamase, a penicillin binding protein and a transmembrane protein are clustered with cephamycin biosynthetic genes in Nocardia lactamdurans. EMBO J. 12:631-639.
10. Dessen, A., A. Quémard, J. S. Blanchard, W. R. Jacobs, Jr., and J. C. Sacchettini. 1995. Crystal structure and function of the isoniazid target of Mycobacterium tuberculosis. Science 267:1638-1641.
11. Elhai, J., and C. P. Wolk. 1988. A versatile class of positive-selection vectors based on the nonviability of palindrome-containing plasmids that allows cloning into long polylinkers. Gene 68:119-138.
12. Fernandez-Moreno, M. A., J. L. Caballero, D. A. Hopwood, and F. Malpartida. 1991. The act cluster contains regulatory and antibiotic export genes, directs targets for translational control by the bldA tRNA gene of Streptomyces. Cell 66:769-780.
13. Friedman, C. R., M. Y. Stoeckle, B. N. Kreiswirth, W. D. Johnson, S. M. Manoach, J. Berger, K. Sathianathan, A. Hafner, and L. W. Riley. 1995. Transmission of multi-drug-resistant tuberculosis in a large urban setting. Am. J. Respir. Crit. Care Med. 152:355-359.
14. Giladi, M., C. I. Champion, D. A. Haake, D. R. Blanco, J. N. Miller, and M. A. Lovett. 1993. Use of the "blue halo" assay in the identification of genes encoding exported proteins with eleavable signal peptides: cloning of a Borrelia burgdorferi plasmid gene with a signal peptide. J. Bacteriol. 175:4129-4136.
15. Griffith, J. K., M. E. Baker, D. A. Rouch, M. G. P. Page, R. A. Skurray, I. T. Paulsen, K. F. Chater, S. A. Baldwin, and P. J. F. Hendersen. 1992. Membrane transport proteins: implications of sequence comparisons. Curr. Opin. Cell Biol. 4:684-695.
16. Guilfoile, P. G., and C. R. Hutchinson. 1992. Sequence and transcriptional analysis of the Streptomyces glaucescens tcmAR tetracenomycin C resistance and repressor gene loci. J. Bacteriol. 174:3651-3658.
17. Guilfoile, P. G., and C. R. Hutchinson. 1992. The Streptomyces glaucescens TcmR protein represses transcription of divergently oriented tcmR and tcmA genes by binding to an intergenic operator region. J. Bacteriol. 174:3659-3666.
18. Henderson, P. J. F. 1993. The 12-transmembrane helix transporters. Curr. Opin. Cell Biol. 5:708-721.
19. Heym, B., P. M. Alzari, N. Honoré, and S. T. Cole. 1995. Missense mutations in the catalase-peroxidase gene, katG, are associated with isoniazid resistance in Mycobacterium tuberculosis. Mol. Microbiol. 15:235-245.
20. Honoré, N., and S. T. Cole. 1994. Streptomycin resistance in mycobacteria. Antimicrob. Agents Chemother. 38:238-242.
21. Hopwood, D. A., M. J. Bibb, K. F. Chater, T. Keiser, C. J. Bruton, H. M. Keiser, D. J. Lydiate, C. P. Smith, J. M. Ward, and H. Schrempf. 1985. Genetic manipulation of Streptomyces: a laboratory manual. The John Innes Foundation, Norwich, United Kingdom.
22. Jacobs, W. R., Jr., G. V. Kalpana, J. D. Cirillo, L. Pascopella, S. B. Snapper, R. A. Udani, W. Jones, R. G. Baretta, and B. R. Bloom. 1991. Genetic systems for Mycobacteria. Methods Enzymol. 204:537-555.
23. Kanazawa, S., M. Driscoll, and K. Struhl. 1988. ATR1, a Saccharomyces cerevisiae gene encoding a transmembrane protein for aminotriazole resistance. Mol. Cell. Biol. 8:664-673.
24. Kneller, D. G., F. E. Cohen, and R. Langridge. 1990. Improvements in protein secondary structure prediction by an enhanced neural network. J. Mol. Biol. 214:171-182.
25. Kremer, L., A. Baulard, J. Estaquler, J. Content, A. Capron, and C. Locht. 1995. Analysis of the Mycobacterium tuberculosis 85A antigen promoter region. J. Bacteriol. 177:642-653.
26. Kreiswith, B. N., and A. R. Moss. 1996. Genotyping multidrug-resistant M. tuberculosis in New York City. In W. N. Rom and S. M. Garay (ed.), Tuberculosis. Little, Brown & Co., New York, N.Y.
27. Kyte, J., and R. F. Doolittle. 1982. A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157:105-132.
28. Levy, S. B. 1992. Active efflux mechanisms for antimicrobial resistance. Antimicrob. Agents Chemother. 36:695-703.
29. Littlejohn, T. G., I. T. Paulsen, M. T. Gillespie, J. M. Tennent, M. Midgley, I. G. Jones, A. S. Purewal, and R. A. Skurray. 1992. Substrate specificity and energetics of antiseptic and disinfectant resistance in Staphyloccus aureus. FEMS Microbiol. Lett. 95:259-266.
30. Liu, J., H. E. Takiff, and H. Nikaido. 1996. Active efflux of fluoroquinolones in Mycobacterium smegmatis mediated by LfrA, a multidrug efllux pump. J. Bacteriol. 178:3791-3795.
31. Lomovskaya, O., and K. Lewis. 1992. emr, an Escherichia coli locus for multidrug resistance. Proc. Natl. Acad. Sci. USA 89:8938-8942.
32. Marger, M. D., and M. H. Saier, Jr. 1993. A major superfamily of transmembrane facilitators that catalyse uniport, symport and antiport. Trends Biochem. Sci. 18:13-20.
33. Mdluli, K. E., J. D. Treit, V. J. Kerr, and F. E. Nano. 1995. New vectors for the in vitro generation of alkaline phosphatase fusions to proteins encoded by G+C-rich DNA. Gene 155:133-134.
34. Mikusova, K., R. A. Slayden, G. S. Besra, and P. J. Brennan. 1995. Biogenesis of the mycobacterial cell wall and the site of action of ethambutol. Antimicrob. Agents Chemother. 39:2484-2489.
35. Moran, A. J. 1994. Ph.D. thesis. University of Glasgow, Glasgow, United Kingdom.
36. Morris, S., G. H. Bai, P. Suffys, L. Portillogomez, M. Fairchok, and D. Rouse. 1995. Molecular mechanisms of multiple drug resistance in clinical isolates of Mycobacterium tuberculosis. J. Infect. Dis. 171:954-960.
37. Neal, R. J., and K. F. Chater. 1987. Nucleotide sequence analysis reveals similarities between proteins determining methylenomycin A resistance in Streptomyces and tetracycline resistance in eubacteria. Gene 58:229-241.
38. Neyfakh, A. A., V. E. Bidnenko, and L. B. Chen. 1991. Efflux-mediated multidrug resistance in Bacillus subtilis: similarities and dissimilarities with the mammalian system. Proc. Natl. Acad. Sci. USA 88:4781-4785.
39. Nikaido, H. 1994. Prevention of drug access to bacterial targets: permeability barriers and active efflux. Science 264:382-388.
40. Pang, Y., T. Bosch, and M. C. Roberts. 1994. Single polymerase chain reaction for the detection of tetracycline-resistant determinants Tet K and Tet L. Mol. Cell. Probes 8:417-422.
41. Pang, Y., B. A. Brown, V. A. Steingrube, R. J. Wallace, Jr., and M. C. Roberts. 1994. Tetracycline resistance determinants in Mycobacterium and Streptomyces species. Antimicrob. Agents Chemother. 38:1403-1412.
42. Paulsen, I. T., and R. A. Skurray. 1993. Topology, structure and evolution of two families of proteins involved in antibiotic and antiseptic resistance in eukaryotes and prokaryotes - an analysis. Gene 124:1-11.
43. Persson, B., and P. Argos. 1994. Prediction of transmembrane segments in proteins utilizing multiple sequence alignments. J. Mol. Biol. 237:182-192.
44. Pretorius, G. S., F. A. Sirgel, H. S. Schaaf, P. D. Van Helden, and T. C. Victor. 1996. Rifampicin resistance in Mycobacterium tuberculosis - rapid detection and implications in chemotherapy. S. Afr. Med. J. 86:50-55.
45. Pretorius, G. S., P. D. Van Helden, F. A. Sirgel, K. D. Eisenach, and T. C. Victor. 1995. Mutations in katG gene sequences in isoniazid-resistant clinical isolates of Mycobacterium tuberculosis are rare. Antimicrob. Agents Chemother. 39:2276-2281.
46. Putzer, H., N. Gendron, and M. Grunberg-Manago. 1992. Co-ordinate expression of the two threonyl-tRNA synthetase genes in Bacillus subtilis: control by transcriptional antitermination involving a conserved regulatory sequence. EMBO J. 11:3117-3127.
47. Roberts, M. C. 1994. Epidemiology of tetracyclinc-resistance determinants. Trends Microbiol. 2:353-357.
48. Rouch, D. A., D. S. Cram, D. DiBerardino, T. G. Littlejohn, and R. A. Skurray. 1990. Efflux-mediated antiseptic resistance gene qacA from Staphylococcus aureus: common ancestry with tetracycline- and sugar-transport proteins. Mol. Microbiol. 4:2051-2062.
49. Rouse, D. A., Z. M. Li, G. H. Bai, and S. L. Morris. 1995. Characterization of the katG and inhA genes of isoniazid-resistant clinical isolates of Mycobacterium tuberculosis. Antimicrob. Agents Chemother. 39:2276-2281.
50. Rouse, D. A., and S. L. Morris. 1995. Molecular mechanisms of isoniazid resistance in Mycobacterium tuberculosis and Mycobacterium bovis. Infect. Immun. 63:1427-1433.
51. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
52. Smith, P. G., and A. R. Moss. 1994. Epidemiology of tuberculosis, p. 47-59. In B. R. Bloom (ed.), Tuberculosis: pathogenesis, protection, and control. American Society for Microbiology, Washington, D.C.
53. Snider, D. E., Jr., M. Raviglione, and A. Kochi. 1994. Global burden of tuberculosis, p. 3-11. In B. R. Bloom (ed.), Tuberculosis: pathogenesis, protection, and control. American Society for Microbiology, Washington, D.C.
54. Stokes, R. W., I. M. Orme, and F. M. Collins. 1986. Role of mononuclear phagocytes in expression of resistance and susceptibility to Mycobacterium avium infections in mice. Infect. Immun. 54:811-819.
55. Strauch, K. L., and J. Beckwith. 1988. An Escherichia coli mutation preventing degradation of abnormal proteins. Proc. Natl. Acad. Sci. USA 85:1576-1580.
56. Strohl, W. R. 1992. Compilation and analysis of DNA sequences associated with apparent strcptomycete promoters. Nucleic Acids Res. 20:961-974.
57. Sturrock, S. S., and J. F. Collins. 1993. Unpublished BLITZ Program: MPsrch version 1.3. Available at http://vww.ebi.ac.uk/searches/blitz_input .html. Biocomputing Research Unit University of Edinburgh, Edinburgh, United Kingdom.
58. Takiff, H. E., M. Cimino, M. C. Musso, T. Weisbrod, R. Martinez, M. B. Delgado, L. Salazar, B. R. Bloom, and W. R. Jacobs, Jr. 1996. Efflux pump of the proton antiporter family confers low-level fluoroquinolone resistance in Mycobacterium smegmatis. Proc. Natl. Acad. Sci. USA 93:362-366.
59. Tercero, J. A., R. A. Lacalle, and A. Jimenez. 1993. The pur8 gene from the pur cluster of Streptomyces alboniger encodes a highly hydrophobic polypeptide which confers resistance to puromycin. Eur. J. Biochem. 218:963-971.
60. Tinoco, I., Jr., P. N. Borer, B. Dengler, M. D. Levine, O. C. Uhlenbeck, D. M. Crothers, and J. Gralla. 1973. Improved estimation of secondary structure in ribonucleic acids. Nature 246:40-41.
61. Victor, T. C., G. S. Pretorius, J. V. Felix, A. M. Jordaan, P. D. Van Helden, and K. D. Eisenach. 1996. Letter to the editor: katG mutations in isoniazid-resistant strains of Mycobacterium tuberculosis are not infrequent. Antimicrob. Agents Chemother. 40:1572.
62. von Heinje, G. 1986. The distribution of positively charged residues in bacterial inner membrane proteins correlates with trans-membrane topology. EMBO J. 5:3021-3027.
63. Warren, R., J. Hauman, N. Beyers, M. Richardson, H. S. Schaaf, P. Donald, and P. D. van Helden. 1996. Unexpectedly high strain diversity of Mycobacterium tuberculosis in a high-incidence community. S. Afr. Med. J. 86:45-49.
64. + antiporter of E. coli encoded by a transposon, Tn10: roles of the aspartyl residues located in the putative transmembrane helices. J. Biol. Chem. 267:7490-7498.
65. + antiporter encoded by transposon Tn10 of Escherichia coli. Biochemistry 31:8344-8348.
66. + antiporter of E. coli encoded by a transposon, Tn10; the role of a conserved sequence motif, GXXXXRXGRR, in a putative cytoplasmic loop between helices 2 and 3. J. Biol. Chem. 267:19155-19162.
67. Yamaguchi, A., T. Udagawa, and T. Sawai. 1990. Transport of divalent cations with tetracycline as mediated by the transposon, Tn10-encoded tetracycline resistance protein. J. Biol. Chem. 265:4809-4813.
68. Yanisch-Perron, C., J. Vieira, and J. Messing. 1985. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33:103-119.
69. Zhang, H.-Z., H. Schmidt, and W. Piepersberg. 1992. Molecular cloning and characterization of two lincomycin-resistance genes, ImrA and ImrB, from Streptomyces lincolnensis 78-11. Mol. Microbiol. 6:2147-2157.
70. Zhang, Y., and D. Young. 1994. Strain variation in the katG region of Mycobacterium tuberculosis. Mol. Microbiol. 14:301-308.