Identification of amino acids conferring high-level resistance to expanded-spectrum cephalosporins in the penA gene from Neisseria gonorrhoeae strain H041

Antimicrobial Agents and Chemotherapy

Volumn 57, Issue 7, 2013, Pages 3029-3036

  Tomberg, Joshua ^a   Unemo, Magnus ^b   Ohnishi, Makoto ^c   Davies, Christopher ^d   Nicholas, Robert A ^a  

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

^b ÖREBRO UNIVERSITY HOSPITAL   (Sweden)

^c NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

^d MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; BACTERIAL PROTEIN; BETA LACTAM ANTIBIOTIC; CEFIXIME; CEFTRIAXONE; CEPHALOSPORIN; NUCLEOPHILE; PROTEIN PENA; SERINE; UNCLASSIFIED DRUG;

ANTIBIOTIC RESISTANCE; ANTIMICROBIAL THERAPY; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIUM IDENTIFICATION; BACTERIUM ISOLATE; ENZYME ACTIVE SITE; GENE MUTATION; GONORRHEA; MINIMUM INHIBITORY CONCENTRATION; MONOTHERAPY; MOSAICISM; NEISSERIA GONORRHOEAE; NONHUMAN; PRIORITY JOURNAL; RESTRICTION FRAGMENT; SITE DIRECTED MUTAGENESIS; WILD TYPE;

AMINO ACID SEQUENCE; ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; CEFTRIAXONE; CEPHALOSPORIN RESISTANCE; CEPHALOSPORINS; GONORRHEA; MICROBIAL SENSITIVITY TESTS; MOLECULAR SEQUENCE DATA; MUTATION; NEISSERIA GONORRHOEAE; PENICILLIN-BINDING PROTEINS; PROTEIN STRUCTURE, SECONDARY; SEQUENCE ALIGNMENT;

EID: 84879012055     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.00093-13     Document Type: Article

References (38)

1. World Health Organization. 2008. Global incidence and prevalence of selected curable sexually transmitted infections-2008. World Health Organization, Geneva, Switzerland. http://www.who.int/reproductivehealth/ publications/rtis/2008-STI-estimates.pdf.
2. Unemo M, Shafer WM. 2011. Antibiotic resistance in Neisseria gonorrhoeae: origin, evolution, and lessons learned for the future. Ann. N. Y. Acad. Sci. 1230:E19-E28. doi:10.1111/j.1749-6632.2011.06215.x.
3. Unemo M, Nicholas RA. 2012. Emergence of multidrug-resistant, extensively drug-resistant and untreatable gonorrhea. Future Microbiol. 7:1401-1422.
4. Phillips I. 1976. β-Lactamase producing penicillin-resistant gonococcus. Lancet ii:656-657.
5. CDC. 2007. Update to CDC's sexually transmitted diseases treatment guidelines, 2006: fluoroquinolones no longer recommended for treatment of gonococcal infections. MMWRMorb. Mortal. Wkly. Rep. 56:332-336.
6. Golparian D, Hellmark B, Fredlund H, Unemo M. 2010. Emergence, spread and characteristics of Neisseria gonorrhoeae isolates with in vitro decreased susceptibility and resistance to extended-spectrum cephalosporins in Sweden. Sex. Transm. Infect. 86:454-460.
7. Allen VG, Mitterni L, Seah C, Rebbapragada A, Martin IE, Lee C, Siebert H, Towns L, Melano RG, Low DE. 2013. Neisseria gonorrhoeae treatment failure and susceptibility to cefixime in Toronto, Canada. JAMA 309:163-170.
8. CDC. 2012. Update to CDC's sexually transmitted diseases treatment guidelines, 2010: oral cephalosporins no longer a recommended treatment for gonococcal infections. MMWR Morb. Mortal. Wkly. Rep. 61: 590-594.
9. Bignell C, Unemo M. 2012 European guideline on the diagnosis and treatment of gonorrhoea in adults. Int. J. STD AIDS, in press.
10. Hagman KE, Pan W, Spratt BG, Balthazar JT, Judd RC, Shafer WM. 1995. Resistance of Neisseria gonorrhoeae to antimicrobial hydrophobic agents is modulated by the mtrRCDE efflux system. Microbiology 141: 611-622.
11. Veal WL, Nicholas RA, Shafer WM. 2002. Overexpression of the MtrCMtrD-MtrE efflux pump due to an mtrR mutation is required for chromosomally mediated penicillin resistance in Neisseria gonorrhoeae. J. Bacteriol. 184:5619-5624.
12. Gill MJ, Simjee S, Al-Hattawi K, Robertson BD, Easmon CS, Ison CA. 1998. Gonococcal resistance to β-lactams and tetracycline involves mutation in loop 3 of the porin encoded at the penB locus. Antimicrob. Agents Chemother. 42:2799-2803. (Pubitemid 28501206)
13. Olesky M, Hobbs M, Nicholas RA. 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.
14. Olesky M, Zhao S, Rosenberg RL, Nicholas RA. 2006. Porin-mediated antibiotic resistance in Neisseria gonorrhoeae: ion, solute, and antibiotic permeation through PIB proteins with penB mutations. J. Bacteriol. 188: 2300-2308.
15. Ropp PA, Hu M, Olesky M, Nicholas RA. 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. (Pubitemid 34162507)
16. Zhao S, Duncan M, Tomberg J, Davies C, Unemo M, Nicholas RA. 2009. Genetics of chromosomally mediated intermediate resistance to ceftriaxone and cefixime in Neisseria gonorrhoeae. Antimicrob. Agents Chemother. 53:3744-3751.
17. Spratt BG. 1988. Hybrid penicillin-binding proteins in penicillinresistant strains of Neisseria gonorrhoeae. Nature 332:173-176. (Pubitemid 18083565)
18. Ameyama S, Onodera S, Takahata M, Minami S, Maki N, Endo K, Goto H, Suzuki H, Oishi Y. 2002. Mosaic-like structure of penicillin-binding protein 2 gene (penA) in clinical isolates of Neisseria gonorrhoeae with reduced susceptibility to cefixime. Antimicrob. Agents Chemother. 46: 3744-3749. (Pubitemid 35403246)
19. Ito M, Deguchi T, Mizutani KS, Yasuda M, Yokoi S, Ito S, Takahashi Y, Ishihara S, Kawamura Y, Ezaki T. 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. (Pubitemid 40065784)
20. Tanaka M, Nakayama H, Tunoe H, Egashira T, Kanayama A, Saika T, Kobayashi I, Naito S. 2002. A remarkable reduction in the susceptibility of Neisseria gonorrhoeae isolates to cephems and the selection of antibiotic regimens for the single-dose treatment of gonococcal infection in Japan. J. Infect. Chemother. 8:81-86. (Pubitemid 34456585)
21. Wang SA, Lee MV, O'Connor N, Iverson CJ, Ohye RG, Whiticar PM, Hale JA, Trees DL, Knapp JS, Effler PV, Weinstock HS. 2003. Multidrug-resistant Neisseria gonorrhoeae with decreased susceptibility to cefixime-Hawaii, 2001. Clin. Infect. Dis. 37:849-852. (Pubitemid 37153668)
22. Lindberg R, Fredlund H, Nicholas RA, Unemo M. 2007. Neisseria gonorrhoeae isolates with reduced susceptibility to cefixime and ceftriaxone: association with genetic polymorphisms in penA, mtrR, porB1b, and ponA. Antimicrob. Agents Chemother. 51:2117-2122. (Pubitemid 46903103)
23. Ohnishi M, Saika T, Hoshina S, Iwasaku K, Nakayama S, Watanabe H, Kitawaki J. 2011. Ceftriaxone-resistant Neisseria gonorrhoeae, Japan. Emerg. Infect. Dis. 17:148-149.
24. Ohnishi M, Golparian D, Shimuta K, Saika T, Hoshina S, Iwasaku K, Nakayama SI, Kitawaki J, Unemo M. 2011. Is Neisseria gonorrhoeae initiating a future era of untreatable gonorrhea? Detailed characterization of the first high-level ceftriaxone resistant strain. Antimicrob. Agents Chemother. 55:3538-3545.
25. Tomberg J, Unemo M, Davies C, Nicholas RA. 2010. Molecular and structural analysis of mosaic variants of penicillin-binding protein 2 conferring decreased susceptibility to expanded-spectrum cephalosporins in Neisseria gonorrhoeae: role of epistatic mutations. Biochemistry 49:8062-8070.
26. Maness MJ, Sparling PF. 1973. Multiple antibiotic resistance due to a single mutation in Neisseria gonorrhoeae. J. Infect. Dis. 128:321-330.
27. Danielsson D, Faruki H, Dyer D, Sparling PF. 1986. Recombination near the antibiotic resistance locus penB results in antigenic variation of gonococcal outer membrane protein I. Infect. Immun. 52:529-533. (Pubitemid 16117811)
28. Kellogg DS, Peacock WL, Deacon WE, Browh L, Perkle CI. 1963. Neisseria gonorrhoeae. I. Virulence genetically linked to colonial variation. J. Bacteriol. 85:1274-1279.
29. Unemo M, Golparian D, Nicholas R, Ohnishi M, Gallay A, Sednaoui P. 2012. High-level cefixime- and ceftriaxone-resistant N. gonorrhoeae in France: novel penA mosaic allele in a successful international clone causes treatment failure. Antimicrob. Agents Chemother. 56:1273-1280.
30. Ho SN, Hunt HD, Horton RM, Pullen JK, Pease LR. 1989. Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77:51-59. (Pubitemid 19125653)
31. Powell AJ, Tomberg J, Deacon AM, Nicholas RA, Davies C. 2009. Crystal structures of penicillin-binding protein 2 from penicillin-susceptible and -resistant strains of Neisseria gonorrhoeae reveal an unexpectedly subtle mechanism for antibiotic resistance. J. Biol. Chem. 284: 1202-1212.
32. Frere JM, Nguyen-Disteche M, Coyette J, Joris B. 1992. Mode of action: interaction with the penicillin binding proteins, p 148-196. In Page MI (ed), The chemistry of β-lactams. Chapman & Hall, Glasgow, United Kingdom.
33. Stefanova ME, Tomberg J, Olesky M, Holtje JV, Gutheil WG, Nicholas RA. 2003. Neisseria gonorrhoeae penicillin-binding protein 3 exhibits exceptionally high carboxypeptidase and β-lactam binding activities. Biochemistry 42:14614-14625. (Pubitemid 37532008)
34. Camara J, Serra J, Ayats J, Bastida T, Carnicer-Pont D, Andreu A, Ardanuy C. 2012. Molecular characterization of two high-level ceftriaxone-resistant Neisseria gonorrhoeae isolates detected in Catalonia, Spain. J. Antimicrob. Chemother. 67:1858-1860.
35. Fermer C, Swedberg G. 1997. Adaptation to sulfonamide resistance in Neisseria meningitidis may have required compensatory changes to retain enzyme function: kinetic analysis of dihydropteroate synthases from N. meningitidis expressed in a knockout mutant of Escherichia coli. J. Bacteriol. 179:831-837. (Pubitemid 27051840)
36. Kunz AN, Begum AA, Wu H, D'Ambrozio JA, Robinson JM, Shafer WM, Bash MC, Jerse AE. 2012. Impact of fluoroquinolone resistance mutations on gonococcal fitness and in vivo selection for compensatory mutations. J. Infect. Dis. 205:1821-1829.
37. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG. 2007. Clustal W and Clustal X version 2.0. Bioinformatics 23:2947-2948. (Pubitemid 350162903)
38. Gordon E, Mouz N, Duee E, Dideberg O. 2000. The crystal structure of the penicillin-binding protein 2x from Streptococcus pneumoniae and its acyl-enzyme form: implication in drug resistance. J. Mol. Biol. 299:477-485.