PBP 4 mediates high-level resistance to new-generation cephalosporins in Staphylococcus aureus

Antimicrobial Agents and Chemotherapy

Volumn 60, Issue 7, 2016, Pages 3934-3941

  Chan, Liana C ^a,c   Gilbert, Aubre ^a   Basuino, Li ^a   Da Costa, Thaina M ^a,b   Hamilton, Stephanie M ^a   Dos Santos, Katia R ^b   Chambers, Henry F ^a   Chatterjee, Som S ^a  

^a SAN FRANCISCO GENERAL HOSPITAL   (United States)

^b FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^c HARBOR UCLA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPICILLIN; BETA LACTAM; CEFAZOLIN; CEFOXITIN; CEFTAROLINE; CEFTOBIPROLE; CEFTRIAXONE; CEPHALOSPORIN DERIVATIVE; NAFCILLIN; PENICILLIN BINDING PROTEIN; PENICILLIN BINDING PROTEIN 4; UNCLASSIFIED DRUG; ANTIINFECTIVE AGENT; BACTERIAL PROTEIN;

ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ARTICLE; CROSS LINKING; ENZYME ACTIVITY; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PHENOTYPE; POINT MUTATION; PRIORITY JOURNAL; STAPHYLOCOCCUS AUREUS; DRUG EFFECTS; GENETICS; METABOLISM; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MICROBIAL SENSITIVITY TEST;

ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; BETA-LACTAM RESISTANCE; BETA-LACTAMS; CEPHALOSPORINS; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS; MICROBIAL SENSITIVITY TESTS; PENICILLIN-BINDING PROTEINS; STAPHYLOCOCCUS AUREUS;

EID: 84976910665     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.00358-16     Document Type: Article

References (45)

1. Chambers HF, Deleo FR. 2009. Waves of resistance: Staphylococcus aureus in the antibiotic era. Nat Rev Microbiol 7:629-641. http://dx.doi.org/10.1038/nrmicro2200.
2. Chatterjee SS, Otto M. 2013. Improved understanding of factors driving methicillin-resistant Staphylococcus aureus epidemic waves. Clin Epidemiol 5:205-217. http://dx.doi.org/10.2147/CLEP.S37071.
3. Lowy FD. 1998. Staphylococcus aureus infections. N Engl J Med 339:520-532. http://dx.doi.org/10.1056/NEJM199808203390806.
4. Bush K. 2012. Antimicrobial agents targeting bacterial cell walls and cell membranes. Rev Sci Tech 31:43-56.
5. Miller EL. 2002. The penicillins: a review and update. J Midwifery Womens Health 47:426-434. http://dx.doi.org/10.1016/S1526-9523(02)00330-6.
6. Frere JM, Page MG. 2014. Penicillin-binding proteins: evergreen drug targets. Curr Opin Pharmacol 18:112-119. http://dx.doi.org/10.1016/j.coph.2014.09.012.
7. Macheboeuf P, Contreras-Martel C, Job V, Dideberg O, Dessen A. 2006. Penicillin binding proteins: key players in bacterial cell cycle and drug resistance processes. FEMS Microbiol Rev 30:673-691. http://dx.doi.org/10.1111/j.1574-6976.2006.00024.x.
8. Sauvage E, Kerff F, Terrak M, Ayala JA, Charlier P. 2008. The penicillin-binding proteins: structure and role in peptidoglycan biosynthesis. FEMS Microbiol Rev 32:234-258. http://dx.doi.org/10.1111/j.1574-6976.2008.00105.x.
9. Zapun A, Contreras-Martel C, Vernet T. 2008. Penicillin-binding proteins and β-lactam resistance. FEMS Microbiol Rev 32:361-385. http://dx.doi.org/10.1111/j.1574-6976.2007.00095.x.
10. Berger-Bachi B. 1999. Genetic basis of methicillin resistance in Staphylococcus aureus. Cell Mol Life Sci 56:764-770. http://dx.doi.org/10.1007/s000180050023.
11. Laurent F, Chardon H, Haenni M, Bes M, Reverdy ME, Madec JY, Lagier E, Vandenesch F, Tristan A. 2012. MRSA harboring mecA variant gene mecC, France. Emerg Infect Dis 18:1465-1467. http://dx.doi.org/10.3201/eid1809.111920.
12. Livermore DM. 2006. Can β-lactams be re-engineered to beat MRSA? Clin Microbiol Infect 12(Suppl 2):S11-S16.
13. Chan LC, Basuino L, Diep B, Hamilton S, Chatterjee SS, Chambers HF. 2015. Ceftobiprole- and ceftaroline-resistant methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 59:2960-2963. http://dx.doi.org/10.1128/AAC.05004-14.
14. Leski TA, Tomasz A. 2005. Role of penicillin-binding protein 2 (PBP2) in the antibiotic susceptibility and cell wall cross-linking of Staphylococcus aureus: evidence for the cooperative functioning of PBP2, PBP4, and PBP2A. J Bacteriol 187:1815-1824. http://dx.doi.org/10.1128/JB.187.5.1815-1824.2005.
15. Anderson SD, Gums JG. 2008. Ceftobiprole: an extended-spectrum anti-methicillin-resistant Staphylococcus aureus cephalosporin. Ann Pharmacother 42:806-816. http://dx.doi.org/10.1345/aph.1L016.
16. Barbour A, Derendorf H. 2010. Resistance and the management of complicated skin and skin structure infections: the role of ceftobiprole. Ther Clin Risk Manag 6:485-495. http://dx.doi.org/10.2147/TCRM.S5823.
17. Chambers HF. 2006. Ceftobiprole: in vivo profile of a bactericidal cephalosporin. Clin Microbiol Infect 12(Suppl 2):S17-S22.
18. File TM, Jr, Wilcox MH, Stein GE. 2012. Summary of ceftaroline fosamil clinical trial studies and clinical safety. Clin Infect Dis 55(Suppl 3):S173-S180. http://dx.doi.org/10.1093/cid/cis559.
19. Casapao AM, Davis SL, Barr VO, Klinker KP, Goff DA, Barber KE, Kaye KS, Mynatt RP, Molloy LM, Pogue JM, Rybak MJ. 2014. Large retrospective evaluation of the effectiveness and safety of ceftaroline fosamil therapy. Antimicrob Agents Chemother 58:2541-2546. http://dx.doi.org/10.1128/AAC.02371-13.
20. Otero LH, Rojas-Altuve A, Llarrull LI, Carrasco-Lopez C, Kumarasiri M, Lastochkin E, Fishovitz J, Dawley M, Hesek D, Lee M, Johnson JW, Fisher JF, Chang M, Mobashery S, Hermoso JA. 2013. How allosteric control of Staphylococcus aureus penicillin binding protein 2a enables methicillin resistance and physiological function. Proc Natl Acad Sci U S A 110:16808-16813. http://dx.doi.org/10.1073/pnas.1300118110.
21. Lovering AL, Gretes MC, Safadi SS, Danel F, de Castro L, Page MG, Strynadka NC. 2012. Structural insights into the anti-methicillin-resistant Staphylococcus aureus (MRSA) activity of ceftobiprole. J Biol Chem 287:32096-32102. http://dx.doi.org/10.1074/jbc.M112.355644.
22. Fernandez R, Paz LI, Rosato RR, Rosato AE. 2014. Ceftaroline is active against heteroresistant methicillin-resistant Staphylococcus aureus clinical strains despite associated mutational mechanisms and intermediate levels of resistance. Antimicrob Agents Chemother 58:5736-5746. http://dx.doi.org/10.1128/AAC.03019-14.
23. Kelley WL, Jousselin A, Barras C, Lelong E, Renzoni A. 2015. Missense mutations in PBP2A affecting ceftaroline susceptibility detected in epidemic hospital-acquired methicillin-resistant Staphylococcus aureus clonotypes ST228 and ST247 in Western Switzerland archived since 1998. Antimicrob Agents Chemother 59:1922-1930. http://dx.doi.org/10.1128/AAC.04068-14.
24. Long SW, Olsen RJ, Mehta SC, Palzkill T, Cernoch PL, Perez KK, Musick WL, Rosato AE, Musser JM. 2014. PBP2a mutations causing high-level ceftaroline resistance in clinical methicillin-resistant Staphylococcus aureus isolates. Antimicrob Agents Chemother 58:6668-6674. http://dx.doi.org/10.1128/AAC.03622-14.
25. Biedenbach DJ, Alm RA, Lahiri SD, Reiszner E, Hoban DJ, Sahm DF, Bouchillon SK, Ambler JE. 2015. In vitro activity of ceftaroline against Staphylococcus aureus isolated in 2012 from Asia-Pacific countries as part of the AWARE Surveillance Program. Antimicrob Agents Chemother 60: 343-347. http://dx.doi.org/10.1128/AAC.01867-15.
26. Banerjee R, Gretes M, Basuino L, Strynadka N, Chambers HF. 2008. In vitro selection and characterization of ceftobiprole-resistant methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 52:2089-2096. http://dx.doi.org/10.1128/AAC.01403-07.
27. Long SW, Beres SB, Olsen RJ, Musser JM. 2014. Absence of patient-to-patient intrahospital transmission of Staphylococcus aureus as determined by whole-genome sequencing. mBio 5:e01692-01614. http://dx.doi.org/10.1128/mBio.01692-14.
28. Banerjee R, Gretes M, Harlem C, Basuino L, Chambers HF. 2010. A mecA-negative strain of methicillin-resistant Staphylococcus aureus with high-level β-lactam resistance contains mutations in three genes. Antimicrob Agents Chemother 54:4900-4902. http://dx.doi.org/10.1128/AAC.00594-10.
29. Henze UU, Berger-Bachi B. 1995. Staphylococcus aureus penicillin-binding protein 4 and intrinsic β-lactam resistance. Antimicrob Agents Chemother 39:2415-2422. http://dx.doi.org/10.1128/AAC.39.11.2415.
30. Katayama Y, Zhang HZ, Chambers HF. 2003. Effect of disruption of Staphylococcus aureus PBP4 gene on resistance to β-lactam antibiotics. Microb Drug Resist 9:329-336. http://dx.doi.org/10.1089/107662903322762752.
31. Talan DA, Krishnadasan A, Gorwitz RJ, Fosheim GE, Limbago B, Albrecht V, Moran GJ, EMERGEncy ID Net Study Group. 2011. Comparison of Staphylococcus aureus from skin and soft-tissue infections in US emergency department patients, 2004 and 2008. Clin Infect Dis 53:144-149. http://dx.doi.org/10.1093/cid/cir308.
32. Memmi G, Filipe SR, Pinho MG, Fu Z, Cheung A. 2008. Staphylococcus aureus PBP4 is essential for β-lactam resistance in community-acquired methicillin-resistant strains. Antimicrob Agents Chemother 52:3955-3966. http://dx.doi.org/10.1128/AAC.00049-08.
33. Bae T, Schneewind O. 2006. Allelic replacement in Staphylococcus aureus with inducible counter-selection. Plasmid 55:58-63. http://dx.doi.org/10.1016/j.plasmid.2005.05.005.
34. Wang R, Braughton KR, Kretschmer D, Bach TH, Queck SY, Li M, Kennedy AD, Dorward DW, Klebanoff SJ, Peschel A, DeLeo FR, Otto M. 2007. Identification of novel cytolytic peptides as key virulence determinants for community-associated MRSA. Nat Med 13:1510-1514. http://dx.doi.org/10.1038/nm1656.
35. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE. 2004. UCSF Chimera - a visualization system for exploratory research and analysis. J Comput Chem 25:1605-1612. http://dx.doi.org/10.1002/jcc.20084.
36. Diep BA, Stone GG, Basuino L, Graber CJ, Miller A, des Etages SA, Jones A, Palazzolo-Ballance AM, Perdreau-Remington F, Sensabaugh GF, DeLeo FR, Chambers HF. 2008. The arginine catabolic mobile element and staphylococcal chromosomal cassette mec linkage: convergence of virulence and resistance in the USA300 clone of methicillin-resistant Staphylococcus aureus. J Infect Dis 197:1523-1530. http://dx.doi.org/10.1086/587907.
37. Pereira SF, Henriques AO, Pinho MG, de Lencastre H, Tomasz A. 2007. Role of PBP1 in cell division of Staphylococcus aureus. J Bacteriol 189: 3525-3531. http://dx.doi.org/10.1128/JB.00044-07.
38. Yoshida H, Kawai F, Obayashi E, Akashi S, Roper DI, Tame JR, Park SY. 2012. Crystal structures of penicillin-binding protein 3 (PBP3) from methicillin-resistant Staphylococcus aureus in the apo and cefotaxime-bound forms. J Mol Biol 423:351-364. http://dx.doi.org/10.1016/j.jmb.2012.07.012.
39. Navratna V, Nadig S, Sood V, Prasad K, Arakere G, Gopal B. 2010. Molecular basis for the role of Staphylococcus aureus penicillin binding protein 4 in antimicrobial resistance. J Bacteriol 192:134-144. http://dx.doi.org/10.1128/JB.00822-09.
40. Corrigan RM, Abbott JC, Burhenne H, Kaever V, Grundling A. 2011. c-di-AMP is a new second messenger in Staphylococcus aureus with a role in controlling cell size and envelope stress. PLoS Pathog 7:e1002217. http://dx.doi.org/10.1371/journal.ppat.1002217.
41. Corrigan RM, Grundling A. 2013. Cyclic di-AMP: another second messenger enters the fray. Nat Rev Microbiol 11:513-524. http://dx.doi.org/10.1038/nrmicro3069.
42. Wyke AW, Ward JB, Hayes MV, Curtis NA. 1981. A role in vivo for penicillin-binding protein-4 of Staphylococcus aureus. Eur J Biochem 119: 389-393. http://dx.doi.org/10.1111/j.1432-1033.1981.tb05620.x.
43. WHO. 2014. Antimicrobial resistance: global report on surveillance. WHO, Geneva, Switzerland. http://apps.who.int/iris/bitstream/10665/112647/1/WHO-HSE-PED-AIP-2014.2-eng.pdf?ua=1.
44. Corrigan RM, Bowman L, Willis AR, Kaever V, Grundling A. 2015. Cross-talk between two nucleotide-signaling pathways in Staphylococcus aureus. J Biol Chem 290:5826-5839. http://dx.doi.org/10.1074/jbc.M114.598300.
45. CLSI. 2013. Performance standards for antimicrobial susceptibility testing; 23rd informational supplement; CLSI document M100-S23. CLSI, Wayne, PA.