Penicillin-binding protein transpeptidase signatures for tracking and predicting β-lactam resistance levels in Streptococcus pneumoniae

mBio

Volumn 7, Issue 3, 2016, Pages

  Li, Yuan ^a   Metcalf, Benjamin J ^a   Chochua, Sopio ^a   Li, Zhongya ^a   Gertz, Robert E ^a   Walker, Hollis ^a   Hawkins, Paulina A ^a   Tran, Theresa ^a   Whitney, Cynthia G ^a   McGee, Lesley ^a   Beall, Bernard W ^a  

^a NATIONAL CENTER FOR IMMUNIZATION AND RESPIRATORY DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMOXICILLIN; BETA LACTAM ANTIBIOTIC; CEFOTAXIME; CEFTRIAXONE; CEFUROXIME; DRUG BINDING PROTEIN; GAMMA GLUTAMYLTRANSFERASE; MEROPENEM; PENICILLIN BINDING PROTEIN; PENICILLIN BINDING PROTEIN 1A; PENICILLIN BINDING PROTEIN 2B; PENICILLIN BINDING PROTEIN 2X; PENICILLIN DERIVATIVE; UNCLASSIFIED DRUG; ANTIINFECTIVE AGENT; BETA LACTAM; PEPTIDYLTRANSFERASE;

AMINO ACID SEQUENCE; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIUM ISOLATE; BROTH DILUTION; DRUG PROTEIN BINDING; ELASTIC NET MODEL; ENZYME ACTIVE SITE; GENETIC BACKGROUND; GENETIC VARIABILITY; GENETIC VARIATION; MINIMUM INHIBITORY CONCENTRATION; MODE MIC MODEL; MULTILOCUS SEQUENCE TYPING; NONBIOLOGICAL MODEL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; RANDOM FOREST MODEL; SEQUENCE ANALYSIS; STREPTOCOCCUS PNEUMONIAE; CLASSIFICATION; DRUG EFFECTS; ENZYMOLOGY; GENETICS; GENOTYPE; HUMAN; MICROBIAL SENSITIVITY TEST; MICROBIOLOGY; PNEUMOCOCCAL INFECTION;

ANTI-BACTERIAL AGENTS; BETA-LACTAM RESISTANCE; BETA-LACTAMS; GENOTYPE; HUMANS; MICROBIAL SENSITIVITY TESTS; MULTILOCUS SEQUENCE TYPING; PENICILLIN-BINDING PROTEINS; PEPTIDYL TRANSFERASES; PNEUMOCOCCAL INFECTIONS; STREPTOCOCCUS PNEUMONIAE;

EID: 84979022762     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.00756-16     Document Type: Article

References (36)

1. Hansman D, Bullen MM. 1967. A resistant pneumococcus. Lancet i:264-265.
2. Jacobs MR, Koornhof HJ, Robins-Browne RM, Stevenson CM, Vermaak ZA, Freiman I, Miller GB, Witcomb MA, Isaacson M, Ward JI, Austrian R. 1978. Emergence of multiply resistant pneumococci. N Engl J Med 299:735-740.
3. Michel J, Dickman D, Greenberg Z, Bergner-Rabinowitz S. 1983. Serotype distribution of penicillin-resistant pneumococci and their susceptibilities to seven antimicrobial agents. Antimicrob Agents Chemother 23: 397-401. http://dx.doi.org/10.1128/AAC.23.3.397.
4. Spika JS, Facklam RR, Plikaytis BD, Oxtoby MJ. 1991. Antimicrobial resistance of Streptococcus pneumoniae in the United States, 1979-1987. The Pneumococcal Surveillance Working Group. J Infect Dis 163: 1273-1278. http://dx.doi.org/10.1093/infdis/163.6.1273.
5. Liñares J, Pallares R, Alonso T, Perez JL, Ayats J, Gudiol F, Viladrich PF, Martin R. 1992. Trends in antimicrobial resistance of clinical isolates of Streptococcus pneumoniae in Bellvitge Hospital, Barcelona, Spain (1979-1990). Clin Infect Dis 15:99-105. http://dx.doi.org/10.1093/clinids/15.1.99.
6. Butler JC, Hofmann J, Cetron MS, Elliott JA, Facklam RR, Breiman RF. 1996. The continued emergence of drug-resistant Streptococcus pneu-moniae in the United States: an update from the Centers for Disease Control and Prevention’s Pneumococcal Sentinel Surveillance System. J Infect Dis 174:986-993. http://dx.doi.org/10.1093/infdis/174.5.986.
7. Hofmann J, Cetron MS, Farley MM, Baughman WS, Facklam RR, Elliott JA, Deaver KA, Breiman RF. 1995. The prevalence of drugresistant Streptococcus pneumoniae in Atlanta. N Engl J Med 333: 481-486. http://dx.doi.org/10.1056/NEJM199508243330803.
8. Hampton LM, Farley MM, Schaffner W, Thomas A, Reingold A, Harrison LH, Lynfield R, Bennett NM, Petit S, Gershman K, Baumbach J, Beall B, Jorgensen J, Glennen A, Zell ER, Moore M. 2012. Prevention of antibiotic-nonsusceptible Streptococcus pneumoniae with conjugate vaccines. J Infect Dis 205:401-411. http://dx.doi.org/10.1093/infdis/jir755.
9. Desai AP, Sharma D, Crispell EK, Baughman W, Thomas S, Tunali A, Sherwood L, Zmitrovich A, Jerris R, Satola SW, Beall B, Moore MR, Jain S, Farley MM. 2015. Decline in pneumococcal nasopharyngeal carriage of vaccine serotypes after the introduction of the 13-valent pneumococcal conjugate vaccine in children in Atlanta, Georgia. Pediatr Infect Dis J 34:1168-1174. http://dx.doi.org/10.1097/INF.0000000000000849.
10. Kyaw MH, Lynfield R, Schaffner W, Craig AS, Hadler J, Reingold A, Thomas AR, Harrison LH, Bennett NM, Farley MM, Facklam RR, Jorgensen JH, Besser J, Zell ER, Schuchat A, Whitney CG, Active Bacterial Core Surveillance of the Emerging Infections Program Network. 2006. Effect of introduction of the pneumococcal conjugate vaccine on drug-resistant Streptococcus pneumoniae. N Engl J Med 354: 1455-1463. http://dx.doi.org/10.1056/NEJMoa051642.
11. Kocaoglu O, Tsui HC, Winkler ME, Carlson EE. 2015. Profiling of beta-lactam selectivity for penicillin-binding proteins in Streptococcus pneumoniae D39. Antimicrob Agents Chemother 59:3548-3555. http://dx.doi.org/10.1128/AAC.05142-14.
12. Barcus VA, Ghanekar K, Yeo M, Coffey TJ, Dowson CG. 1995. Genetics of high level penicillin resistance in clinical isolates of Streptococcus pneumoniae. FEMS Microbiol Lett 126:299-303. http://dx.doi.org/10.1111/j.1574-6968.1995.tb07433.x.
13. Dowson CG, Johnson AP, Cercenado E, George RC. 1994. Genetics of oxacillin resistance in clinical isolates of Streptococcus pneumoniae that are oxacillin resistant and penicillin susceptible. Antimicrob Agents Chemother 38:49-53. http://dx.doi.org/10.1128/AAC.38.1.49.
14. Grebe T, Hakenbeck R. 1996. Penicillin-binding proteins 2b and 2x of Streptococcus pneumoniae are primary resistance determinants for different classes of beta-lactam antibiotics. Antimicrob Agents Chemother 40:829-834.
15. Hakenbeck R, Kaminski K, König A, van der Linden M, Paik J, Reichmann P, Zähner D. 1999. Penicillin-binding proteins in beta-lactamresistant Streptococcus pneumoniae. Microb Drug Resist 5:91-99. http://dx.doi.org/10.1089/mdr.1999.5.91.
16. Smith AM, Klugman KP. 1998. Alterations in PBP 1A essential for highlevel penicillin resistance in Streptococcus pneumoniae. Antimicrob Agents Chemother 42:1329-1333.
17. Muñoz R, Dowson CG, Daniels M, Coffey TJ, Martin C, Hakenbeck R, Spratt BG. 1992. Genetics of resistance to third-generation cephalosporins in clinical isolates of Streptococcus pneumoniae. Mol Microbiol 6:2461-2465.
18. Laible G, Spratt BG, Hakenbeck R. 1991. Interspecies recombinational events during the evolution of altered PBP 2x genes in penicillin-resistant clinical isolates of Streptococcus pneumoniae. Mol Microbiol 5:1993-2002. http://dx.doi.org/10.1111/j.1365-2958.1991.tb00821.x.
19. Albarracín Orio AG, Piñas GE, Cortes PR, Cian MB, Echenique J. 2011. Compensatory evolution of pbp mutations restores the fitness cost imposed by beta-lactam resistance in Streptococcus pneumoniae. PLoS Pathog 7:e1002000. http://dx.doi.org/10.1371/journal.ppat.1002000.
20. Hakenbeck R, Brückner R, Denapaite D, Maurer P. 2012. Molecular mechanisms of beta-lactam resistance in Streptococcus pneumoniae. Future Microbiol 7:395-410. http://dx.doi.org/10.2217/fmb.12.2.
21. Coffey TJ, Dowson CG, Daniels M, Spratt BG. 1993. Horizontal spread of an altered penicillin-binding protein 2B gene between Streptococcus pneumoniae and Streptococcus oralis. FEMS Microbiol Lett 110:335-339. http://dx.doi.org/10.1111/j.1574-6968.1993.tb06345.x.
22. Dowson CG, Coffey TJ, Kell C, Whiley RA. 1993. Evolution of penicillin resistance in Streptococcus pneumoniae; the role of Streptococcus mitis in the formation of a low affinity PBP2B in S. pneumoniae. Mol Microbiol 9:635-643. http://dx.doi.org/10.1111/j.1365-2958.1993.tb01723.x.
23. Dowson CG, Coffey TJ, Spratt BG. 1994. Origin and molecular epidemiology of penicillin-binding-protein-mediated resistance to beta-lactam antibiotics. Trends Microbiol 2:361-366. http://dx.doi.org/10.1016/0966-842X(94)90612-2.
24. Contreras-Martel C, Job V, Di Guilmi AM, Vernet T, Dideberg O, Dessen A. 2006. Crystal structure of penicillin-binding protein 1a (PBP1a) reveals a mutational hotspot implicated in beta-lactam resistance in Streptococcus pneumoniae. J Mol Biol 355:684-696. http://dx.doi.org/10.1016/j.jmb.2005.10.030.
25. Contreras-Martel C, Dahout-Gonzalez C, Martins Ados S, Kotnik M, Dessen A. 2009. PBP active site flexibility as the key mechanism for betalactam resistance in pneumococci. J Mol Biol 387:899-909. http://dx.doi.org/10.1016/j.jmb.2009.02.024.
26. Gordon E, Mouz N, Duée 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. http://dx.doi.org/10.1006/jmbi.2000.3740.
27. Chewapreecha C, Marttinen P, Croucher NJ, Salter SJ, Harris SR, Mather AE, Hanage WP, Goldblatt D, Nosten FH, Turner C, Turner P, Bentley SD, Parkhill J. 2014. Comprehensive identification of single nucleotide polymorphisms associated with beta-lactam resistance within pneumococcal mosaic genes. PLoS Genet 10:e1004547. http://dx.doi.org/10.1371/journal.pgen.1004547.
28. Sauerbier J, Maurer P, Rieger M, Hakenbeck R. 2012. Streptococcus pneumoniae R6 interspecies transformation: genetic analysis of penicillin resistance determinants and genome-wide recombination events. Mol Microbiol 86:692-706. http://dx.doi.org/10.1111/mmi.12009.
29. Whitney CG, Farley MM, Hadler J, Harrison LH, Bennett NM, Lynfield R, Reingold A, Cieslak PR, Pilishvili T, Jackson D, Facklam RR, Jorgensen JH, Schuchat A, Active Bacterial Core Surveillance of the Emerging Infections Program Network. 2003. Decline in invasive pneumococcal disease after the introduction of protein-polysaccharide conjugate vaccine. N Engl J Med 348:1737-1746. http://dx.doi.org/10.1056/NEJMoa022823.
30. Moore MR, Link-Gelles R, Schaffner W, Lynfield R, Lexau C, Bennett NM, Petit S, Zansky SM, Harrison LH, Reingold A, Miller L, Scherzinger K, Thomas A, Farley MM, Zell ER, Taylor TH, Jr, Pondo T, Rodgers L, McGee L, Beall B, Jorgensen JH, Whitney CG. 2015. Effect of use of 13-valent pneumococcal conjugate vaccine in children on invasive pneumococcal disease in children and adults in the USA: analysis of multisite, population-based surveillance. Lancet Infect Dis 15:301-309. http://dx.doi.org/10.1016/S1473-3099(14)71081-3.
31. Pilishvili T, Lexau C, Farley MM, Hadler J, Harrison LH, Bennett NM, Reingold A, Thomas A, Schaffner W, Craig AS, Smith PJ, Beall BW, Whitney CG, Moore MR, Active Bacterial Core Surveillance/Emerging Infections Program Network. 2010. Sustained reductions in invasive pneumococcal disease in the era of conjugate vaccine. J Infect Dis 201: 32-41. http://dx.doi.org/10.1086/648593.
32. Beall BW, Gertz RE, Hulkower RL, Whitney CG, Moore MR, Brueggemann AB. 2011. Shifting genetic structure of invasive serotype 19A pneumococci in the United States. J Infect Dis 203:1360-1368. http://dx.doi.org/10.1093/infdis/jir052.
33. Clinical and Laboratory Standards Institute. 2013. Performance standards for antimicrobial susceptibility testing; twenty-third informational supplement. M100-S23. Clinical and Laboratory Standards Institute, Wayne, PA.
34. Metcalf BJ, Gertz RE, Jr, Gladstone RA, Walker H, Sherwood LK, Jackson D, Li Z, Law C, Hawkins PA, Chochua S, Sheth M, Rayamajhi N, Bentley SD, Kim L, Whitney CG, McGee L, Beall B, Active Bacterial Core surveillance Team. 2016. Strain features and distributions in pneumococci from children with invasive disease before and after 13-valent conjugate vaccine implementation in the USA. Clin Microbiol Infect 22: e9-60.e29. http://dx.doi.org/10.1016/j.cmi.2015.08.027.
35. US Food and Drug Administration. 2009. Guidance for industry and FDA class II special controls guidance Document: antimicrobial susceptibility test (AST) systems. US Food and Drug Administration, Silver Spring,MD. http://www.fda.gov/MedicalDevices/DeviceRegulationandGuidance/GuidanceDocuments/ucm080564.htm.
36. R Development Core Team. 2015. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org.