A novel tryptophanyl-tRNA synthetase gene confers high-level resistance to indolmycin

Antimicrobial Agents and Chemotherapy

Volumn 53, Issue 9, 2009, Pages 3972-3980

  Vecchione, James J ^a   Sello, Jason K ^a  

^a BROWN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIINFECTIVE AGENT; CHUANGXINMYCIN; INDOLMYCIN; TRYPTOPHAN TRANSFER RNA LIGASE; UNCLASSIFIED DRUG;

ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; CONTROLLED STUDY; GENE LOCUS; GENE OVEREXPRESSION; GENETIC CODE; GENETIC TRANSCRIPTION; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; POINT MUTATION; PRIORITY JOURNAL; PROMOTER REGION; STREPTOMYCES GRISEUS;

AMINO ACID SEQUENCE; ANTI-BACTERIAL AGENTS; CHROMATOGRAPHY, LIQUID; DRUG RESISTANCE, MULTIPLE, BACTERIAL; INDOLES; ISOENZYMES; MASS SPECTROMETRY; MICROBIAL SENSITIVITY TESTS; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY, AMINO ACID; STREPTOMYCES; STREPTOMYCES COELICOLOR; STREPTOMYCES GRISEUS; TRYPTOPHAN; TRYPTOPHAN-TRNA LIGASE;

EID: 70349111449     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.00723-09     Document Type: Article

References (39)

1. Bentley, S. D., K. F. Chater, A. M. Cerdeño-Tarraga, G. L. Challis, N. R. Thomson, K. D. James, et al. 2002. Complete genome sequence of the model actinomycete Streptomyces coelicolor. Nature 417:141-147.
2. Brown, J. R., D. Gentry, J. A. Becker, K. Ingraham, D. J. Holmes, and M. J. Stanhope. 2003. Horizontal transfer of drug-resistant aminoacyl-transfer- RNA synthetases of anthrax and gram-positive pathogens. EMBO Rep. 4:692-698.
3. Brown, M. J., P. S. Carter, A. E. Fenwick, A. P. Fosberry, D. W. Hamprecht, M. J. Hibbs, et al. 2002. The antimicrobial natural product chuangxinmycin and some synthetic analogues are potent and selective inhibitors of bacterial tryptophanyl-tRNA synthetase. Bioorg. Med. Chem. Lett. 12:3171-3174.
4. Casewell, M. W., and R. L. Hill. 1987. Mupirocin (pseudomonic acid) - a promising new topical antimicrobial agent. J. Antimicrob. Chemother. 19:1-5.
5. Davies, J. 2008. Resistance redux. Infectious diseases, antibiotic resistance and the future of mankind. EMBO Rep. 9:S18-S21.
6. D'Costa, V. M., K. M. McGrann, D. W. Hughes, and G. D. Wright. 2006. Sampling the antibiotic resistome. Science 311:374-377.
7. El-Sayed, A. K., J. Hothersall, S. M. Cooper, E. Stephens, T. J. Simpson, and C. M. Thomas. 2003. Characterization of the mupirocin biosynthesis gene cluster from Pseudomonas fluorescens NCIMB 10586. Chem. Biol. 10:419-430.
8. Fuller, A. T., G. Mellows, M. Woolford, G. T. Banks, K. D. Barrow, and E. B. Chain. 1971. Pseudomonic acid: an antibiotic produced by Pseudomonas fluorescens. Nature 234:416-417.
9. Gentry, D. R., K. A. Ingraham, M. J. Stanhope, S. Rittenhouse, R. L. Jarvest, P. J. O'Hanlon, et al. 2003. Variable sensitivity to bacterial methionyl-tRNA synthetase inhibitors reveals subpopulations of Streptococcus pneumoniae with two distinct methionyl-tRNA synthetase genes. Antimicrob. Agents Chemother. 47:1784-1789.
10. Gregory, M. A., R. Till, and M. C. M. Smith. 2003. Integration site for Streptomyces phage BT1 and development of site-specific integrating vectors. J. Bacteriol. 185:5320-5323.
11. Hasuoka, A., Y. Nakayama, M. Adachi, H. Kamiguchi, and K. Kamiyama. 2001. Development of a stereoselective practical synthetic route to indolmycin, a candidate anti-H. pylori agent. Chem. Pharm. Bull. 49:1604-1608. (Pubitemid 33126589)
12. Hong, H. J., M. I. Hutchings, L. M. Hill, and M. J. Buttner. 2005. The role of the novel Fem protein VanK in vancomycin resistance in. Streptomyces coelicolor. J. Biol. Chem. 280:13055-13061.
13. Hopwood, D. A. 2007. How do antibiotic-producing bacteria ensure their self-resistance before antibiotic biosynthesis incapacitates them? Mol. Microbiol. 63:937-940.
14. Hopwood, D. A. 2007. Streptomyces in nature and medicine. Oxford University Press, New York, NY.
15. Hughes, J., and G. Mellows. 1978. Inhibition of isoleucyl-transfer ribonucleic acid synthetase in Escherichia coli by pseudomonic acid. Biochem. J. 176:305-318.
16. Hurdle, J. G., A. J. O' Neill, and I. Chopra. 2004. Anti-staphylococcal activity of indolmycin, a potential topical agent for control of staphylococcal infections. J. Antimicrob. Chemother. 54:549-552.
17. Hurdle, J. G., A. J. O'Neill, and I. Chopra. 2005. Prospects for aminoacyl-tRNA synthetase inhibitors as new antimicrobial agents. Antimicrob. Agents Chemother. 49:4821-4833.
18. Ikeda, H., J. Ishikawa, A. Hanamoto, M. Shinose, H. Kikuchi, T. Shiba, Y. Sakaki, M. Hattori, and S. Omura. 2003. Complete genome sequence and comparative analysis of the industrial microorganism Streptomyces avermitilis. Nat. Biotechnol. 21:526-531.
19. Kanamaru, T., Y. Nakano, Y. Toyoda, K. I. Miyagawa, M. Tada, T. Kaisho, and M. Nakao. 2001. In vitro and in vivo antibacterial activities of TAK-083, an agent for treatment of Helicobacter pylori infection. Antimicrob. Agents Chemother. 45:2455-2459.
20. Kieser, T., M. J. Bibb, M. J. Buttner, K. F. Chater, and D. A. Hopwood. 2000. Practical Streptomyces genetics. John Innes Foundation, Norwich, CT.
21. Kim, S., S. W. Lee, E. C. Choi, and S. Y. Choi. 2003. Aminoacyl-tRNA synthetases and their inhibitors as a novel family of antibiotics. Appl. Microbiol. Biotechnol. 61:278-288.
22. Kitabatake, M., K. Ali, A. Demain, K. Sakamoto, S. Yokoyama, and D. Söll. 2002. Indolmycin resistance of Streptomyces coelicolor A3(2) by induced expression of one of its two tryptophanyl-tRNA synthetases. J. Biol. Chem. 277:23882-23887.
23. Marsh, W. S., A. L. Garretson, and E. M. Wesel. 1960. PA 155 A, B, and X antibiotics produced by a strain of Streptomyces albus. Antibiot. Chemother. 10:316-320.
24. Martínez, J. L., F. Baquero, and D. I. Andersson. 2007. Predicting antibiotic resistance. Nat. Rev. Microbiol. 5:958-965.
25. Ochsner, U. A., X. Sun, T. Jarvis, I. Critchley, and N. Janjic. 2007. Aminoacyl- tRNA synthetases: essential and still promising targets for new antiinfective agents. Expert Opin. Investig. Drugs 16:573-593.
26. Ohnishi, Y., J. Ishikawa, H. Hara, H. Suzuki, M. Ikenoya, H. Ikeda, A. Yamashita, M. Hattori, and S. Horinouchi. 2008. Genome sequence of the streptomycin-producing microorganism Streptomyces griseus IFO 13350. J. Bacteriol. 190:4050-4060.
27. Omura, S., H. Ikeda, J. Ishikawa, A. Hanamoto, C. Takahashi, M. Shinose, Y. Takahashi, H. Horikawa, H. Nakazawa, T. Osonoe, H. Kikuchi, T. Shiba, Y. Sakaki, and M. Hattori. 2001. Genome sequence of an industrial microorganism Streptomyces avermitilis: deducing the ability of producing secondary metabolites. Proc. Natl. Acad. Sci. USA 98:12215-12220.
28. Pohlmann, J., and H. Broetz-Oesterhelt. 2004. New aminoacyl-tRNA synthetase inhibitors as antibacterial agents. Curr. Drug. Targets 4:261-272.
29. Routien, J. B. 1966. Identity of streptomycete producing antibiotic PA155A. J. Bacteriol. 91:1663.
30. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
31. Strohl, W. R. 1992. Compilation and analysis of DNA sequences associated with apparent streptomycete promoters. Nucleic Acids Res. 20:961-974.
32. Sutherland, R., R. J. Boon, K. E. Griffin, P. J. Masters, B. Slocombe, and A. R. White. 1985. Antibacterial activity of mupirocin (pseudomonic acid), a new antibiotic for topical use. Antimicrob. Agents Chemother. 27:495-498.
33. Tahlan, K., S. K. Ahn, A. Sing, T. D. Bodnaruk, A. R. Willems, A. R. Davidson, and J. R. Nodwell. 2007. Initiation of actinorhodin export in Streptomyces coelicolor. Mol. Microbiol. 63:951-961.
34. Tao, J., and P. Schimmel. 2000. Inhibitors of aminoacyl-tRNA synthetases as novel anti-infectives. Expert Opin. Investig. Drugs 9:1767-1775.
35. Udo, E. E., L. E. Jacob, and E. M. Mokadas. 1997. Conjugative transfer of high-level mupirocin resistance from Staphylococcus haemolyticus to other staphylococci. Antimicrob. Agents Chemother. 41:693-695.
36. Vecchione, J. J., and J. K. Sello. 2008. Characterization of an inducible, antibiotic-resistant aminoacyl-tRNA synthetase gene in Streptomyces coelicolor. J. Bacteriol. 190:6253-6257.
37. Werner, R. G., and A. L. Demain. 1981. Directed biosynthesis of new indolmycins. J. Antibiot. 34:551-554.
38. Werner, R. G., L. F. Thorpe, W. Reuter, and K. H. Nierhaus. 1976. Indolmycin inhibits prokaryotic tryptophanyl-tRNA ligase. Eur. J. Biochem. 68:1-3.
39. Yanagisawa, T., and M. Kawakami. 2003. How does Pseudomonas fluorescens avoid suicide from its antibiotic pseudomonic acid? Evidence for two evolutionarily distinct isoleucyl-tRNA synthetases conferring self-defense. J. Biol. Chem. 278:25887-25894.