High-level chromosomally mediated tetracycline resistance in Neisseria gonorrhoeae results from a point mutation in the rpsJ gene encoding ribosomal protein S10 in combination with the mtrR and penB resistance determinants

Antimicrobial Agents and Chemotherapy

Volumn 49, Issue 10, 2005, Pages 4327-4334

  Hu, Mei ^a,c   Nandi, Sobhan ^a   Davies, Christopher ^b   Nicholas, Robert A ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^c Serenex Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINOACYL TRANSFER RNA; ERYTHROMYCIN; GLUTAMINE; LEUCINE; METHIONINE; PENICILLIN G; PROTEIN S10; RIBOSOME PROTEIN; RIBOSOME RNA; TETRACYCLINE; UNCLASSIFIED DRUG; VALINE;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENE; BINDING AFFINITY; CODON; CONTROLLED STUDY; DRUG BINDING SITE; GENE IDENTIFICATION; MINIMUM INHIBITORY CONCENTRATION; MOLECULAR CLONING; MTRR GENE; NEISSERIA GONORRHOEAE; NONHUMAN; NUCLEOTIDE SEQUENCE; PENB GENE; POINT MUTATION; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RIBOSOME SUBUNIT; RPSJ GENE; TET 2 GENE; THERMUS THERMOPHILUS;

ALLELES; AMINO ACID SEQUENCE; GENES, BACTERIAL; MICROBIAL SENSITIVITY TESTS; MODELS, GENETIC; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NEISSERIA GONORRHOEAE; POINT MUTATION; RIBOSOMAL PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; TETRACYCLINE RESISTANCE;

EID: 25844478583     PISSN: 00664804     EISSN: None     Source Type: Journal    
DOI: 10.1128/AAC.49.10.4327-4334.2005     Document Type: Article

References (39)

1. Ban, N., P. Nissen, J. Hansen, P. B. Moore, and T. A. Steitz. 2000. The complete atomic structure of the large ribosomal subunit at 2.4 Å resolution. Science 289:905-920.
2. Bowler, L. D., Q. Y. Zhang, J. Y. Riou, and B. G. Spratt. 1994. Interspecies recombination between the penA genes of Neisseria meningitidis and commensal Neisseria species during the emergence of penicillin resistance in N. meningitidis: natural events and laboratory simulation. J. Bacteriol. 176:333-337.
3. Brodersen, D. E., W. M. Clemons, Jr., A. P. Carter, R. J. Morgan-Warren, B. T. Wimberly, and V. Ramakrishnan. 2000. The structural basis for the action of the antibiotics tetracycline, pactamycin, and hygromycin B on the 30S ribosomal subunit. Cell 103:1143-1154.
4. Carter, A. P., W. M. Clemons, D. E. Brodersen, R. J. Morgan-Warren, B. T. Wimberly, and V. Ramakrishnan. 2000. Functional insights from the structure of the 30S ribosomal subunit and its interactions with antibiotics. Nature 407:340-348.
5. Centers for Disease Control and Prevention. 2004. Increases in fluoroquinolone-resistant Neisseria gonorrhoeae among men who have sex with men-United States, 2003, and revised recommendations for gonorrhea treatment, 2004. Morb. Mortal. Wkly. Rep. 53:335-338.
6. Centers for Disease Control and Prevention. 2002. Increases in fluoroquinolone-resistant Neisseria gonorrhoeae-Hawaii and California, 2001. Morb. Mortal. Wkly. Rep. 51:1041-1044.
7. Centers for Disease Control and Prevention. 2004. Sexually transmitted disease surveillance 2003 supplement: Gonococcal Isolate Surveillance Project (GISP) annual report-2003. Centers for Disease Control and Prevention, Atlanta, Ga.
8. Centers for Disease Control and Prevention. 2002. Sexually transmitted disease treatment guidelines 2002. Morb. Mortal. Wkly. Rep. 51:36-41.
9. Chang, A. C., and S. N. Cohen. 1978. Construction and characterization of amplifiable multicopy DNA cloning vehicles derived from the P15A cryptic miniplasmid. J. Bacteriol. 134:1141-1156.
10. Danielsson, D., H. Faruki, D. Dyer, and P. F. Sparling. 1986. Recombination near the antibiotic resistance locus penB results in antigenic variation of gonococcal outer membrane protein I. Infect. Immun. 52:529-533.
11. Elkins, C., C. E. Thomas, H. S. Seifert, and P. F. Sparling. 1991. Species-specific uptake of DNA by gonococci is mediated by a 10-base-pair sequence. J. Bacteriol. 173:3911-3913.
12. Fox, K. K., J. C. Thomas, D. H. Weiner, R. H. Davis, P. F. Sparling, and M. S. Cohen. 1999. Longitudinal evaluation of serovar-specific immunity to Neisseria gonorrhoeae. Am. J. Epidemiol. 149:353-358.
13. Gill, M. J., S. Simjee, K. Al-Hattawi, B. D. Robertson, C. S. Easmon, and C. A. Ison. 1998. Gonococcal resistance to beta-lactams and tetracycline involves mutation in loop 3 of the porin encoded at the penB locus. Antimicrob. Agents Chemother. 42:2799-2803.
14. Hagman, K. E., W. Pan, B. G. Spratt, J. T. Balthazar, R. C. Judd, and W. M. Shafer. 1995. Resistance of Neisseria gonorrhoeae to antimicrobial hydrophobic agents is modulated by the mtrRCDE efflux system. Microbiology 141: 611-622.
15. Ho, S. N., H. D. Hunt, R. M. Horton, J. K. Pullen, and L. R. Pease. 1989. Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77:51-59.
16. Hobbs, M. M., T. M. Alcorn, R. H. Davis, W. Fischer, J. C. Thomas, I. Martin, C. Ison, P. F. Sparling, and M. S. Cohen. 1999. Molecular typing of Neisseria gonorrhoeae causing repeated infections: evolution of porin during passage within a community. J. Infect. Dis. 179:371-381.
17. Ito, M., T. Deguchi, K. S. Mizutani, M. Yasuda, S. Yokoi, S. Ito, Y. Takahashi, S. Ishihara, Y. Kawamura, and T. Ezaki. 2005. Emergence and spread of Neisseria gonorrhoeae clinical isolates harboring mosaic-like structure of penicillin-binding protein 2 in central Japan. Antimicrob. Agents Chemother. 49:137-143.
18. Jeanmougin, F., J. D. Thompson, M. Gouy, D. G. Higgins, and T. J. Gibson. 1998. Multiple sequence alignment with Clustal X. Trends Biochem. Sci. 23:403-405.
19. Kellogg, D. S., W. L. Peacock, W. E. Deacon, L. Browh, and C. I. Perkle. 1963. Neisseria gonorrhoeae. I. Virulence genetically linked to colonial variation. J. Bacteriol. 85:1274-1279.
20. Kraulis, P. J. 1991. MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr. 24:946-950.
21. Maness, M. J., and P. F. Sparling. 1973. Multiple antibiotic resistance due to a single mutation in Neisseria gonorrhoeae. J. Infect. Dis. 128:321-330.
22. Merritt, E. A., and M. E. P. Murphy. 1994. Raster3D Version 2.0: a program for photorealistic molecular graphics. Acta Crystallogr. D 50:869-873.
23. Morse, S. A., S. R. Johnson, J. W. Biddle, and M. C. Roberts. 1986. High-level tetracycline resistance in Neisseria gonorrhoeae is result of acquisition of streptococcal tetM determinant. Antimicrob. Agents Chemother. 30:664-670.
24. Olesky, M., M. Hobbs, and R. A. Nicholas. 2002. Identification and analysis of amino acid mutations in porin IB that mediate intermediate-level resistance to penicillin and tetracycline in Neisseria gonorrhoeae. Antimicrob. Agents Chemother. 46:2811-2820.
25. Olesky, M., R. L. Rosenberg, and R. A. Nicholas. Submitted for publication.
26. Pan, W., and B. G. Spratt. 1994. Regulation of the permeability of the gonococcal cell envelope by the mtr system. Mol. Microbiol. 11:769-775.
27. Phillips, I. 1976. Beta-lactamase producing penicillin-resistant gonococcus. Lancet ii:656-657.
28. Ropp, P. A., M. Hu, M. Olesky, and R. A. Nicholas. 2002. Mutations in ponA, the gene encoding penicillin-binding protein 1, and a novel locus, penC, are required for high-level chromosomally mediated penicillin resistance in Neisseria gonorrhoeae. Antimicrob. Agents Chemother. 46:769-777.
29. Scholar, E., and W. B. Pratt. 2000. The antimicrobial drugs, 2nd ed. Oxford University Press, Inc., New York, N.Y.
30. Sparling, P. F., F. A. J. Sarubbi, and E. Blackman. 1975. Inheritance of low-level resistance to penicillin, tetracycline, and chloramphenicol in Neisseria gonorrhoeae. J. Bacteriol. 124:740-749.
31. Spratt, B. G. 1988. Hybrid penicillin-binding proteins in penicillin-resistant strains of Neisseria gonorrhoeae. Nature 332:173-176.
32. Spratt, B. G., Q. Y. Zhang, D. M. Jones, A. Hutchison, J. A. Brannigan, and C. G. Dowson. 1989. Recruitment of a penicillin-binding protein gene from Neisseria flavescens during the emergence of penicillin resistance in Neisseria meningitidis. Proc. Natl. Acad. Sci. USA 86:8988-8992.
33. Swanson, J. 1973. Studies on gonococcus infection. IV. Pili: their role in attachment of gonococci to tissue culture cells. J. Exp. Med. 137:571-589.
34. Veal, W. L., R. A. Nicholas, and W. M. Shafer. 2002. Overexpression of the MtrC-MtrD-MtrE efflux pump due to an mtrR mutation is required for chromosomally mediated penicillin resistance in Neisseria gonorrhoeae. J. Bacteriol. 184:5619-5624.
35. Wei, Y., and D. H. Bechhofer. 2002. Tetracycline induces stabilization of mRNA in Bacillus subtilis. J. Bacteriol. 184:889-894.
36. Williams, G., and I. Smith. 1979. Chromosomal mutations causing resistance to tetracycline in Bacillus subtilis. Mol. Gen. Genet. 177:23-29.
37. Wimberly, B. T., D. E. Brodersen, W. M. J. Clemons, R. J. Morgan-Warren, A. P. Carter, C. Vonrhein, T. Hartsch, and V. Ramakrishnan. 2000. Structure of the 30S ribosomal subunit. Nature 407:327-339.
38. Yusupov, M. M., G. Z. Yusupova, A. Baucom, K. Lieberman, T. N. Earnest, J. H. Cate, and H. F. Noller. 2001. Crystal structure of the ribosome at 5.5 Å resolution. Science 292:883-896.
39. Zhao, S., D. M. Tobiason, M. Hu, H. S. Seifert, and R. A. Nicholas. 2005. The penC mutation conferring antibiotic resistance in Neisseria gonorrhoeae arises from a mutation in the PilQ secretin that interferes with multimer stability. Mol. Microbiol. 57:1238-1251.