Compensatory evolution of pbp mutations restores the fitness cost imposed by β-lactam resistance in streptococcus pneumoniae

PLoS Pathogens

Volumn 7, Issue 2, 2011, Pages

  Albarracín Orio, Andrea G ^a   Piñas, Germán E ^a   Cortes, Paulo R ^a   Cian, Melina B ^a   Echenique, José ^a  

^a UNIVERSIDAD NACIONAL DE CÓRDOBA   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

BETA LACTAM ANTIBIOTIC; PENICILLIN BINDING PROTEIN; PENICILLIN BINDING PROTEIN 1A; PENICILLIN BINDING PROTEIN 2B; PENICILLIN BINDING PROTEIN 2X; UNCLASSIFIED DRUG; AMINOACYLTRANSFERASE; BACTERIAL DNA; BACTERIAL PROTEIN; BETA LACTAM; PBP 2X PROTEIN, STREPTOCOCCUS; PBP1A PROTEIN, STREPTOCOCCUS PNEUMONIAE; PENICILLIN BINDING PROTEIN 2B, STREPTOCOCCUS; PENICILLIN-BINDING PROTEIN 2B, STREPTOCOCCUS; PEPTIDYLTRANSFERASE;

ALLELE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBIOTIC RESISTANCE; ARTICLE; CELL DIVISION; CELL WALL; CONTROLLED STUDY; DISEASE TRANSMISSION; FLUORESCENCE MICROSCOPY; GENE MUTATION; IN VITRO STUDY; IN VIVO STUDY; MALE; MOLECULAR EVOLUTION; MOUSE; NONHUMAN; PROTEIN LOCALIZATION; PROTEIN STABILITY; STREPTOCOCCUS PNEUMONIAE; CHEMISTRY; DRUG EFFECT; FLOW CYTOMETRY; GENETICS; HUMAN; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; MUTATION; NASOPHARYNX; PNEUMOCOCCAL INFECTION; POLYMERASE CHAIN REACTION;

STREPTOCOCCUS PNEUMONIAE;

AMINOACYLTRANSFERASES; BACTERIAL PROTEINS; BETA-LACTAM RESISTANCE; BETA-LACTAMS; CELL DIVISION; DNA, BACTERIAL; EVOLUTION, MOLECULAR; FLOW CYTOMETRY; HUMANS; MUTATION; NASOPHARYNX; PENICILLIN-BINDING PROTEINS; PEPTIDYL TRANSFERASES; PNEUMOCOCCAL INFECTIONS; POLYMERASE CHAIN REACTION; PROTEIN STABILITY; STREPTOCOCCUS PNEUMONIAE;

EID: 79952221144     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002000     Document Type: Article

References (45)

1. Jacobs MR, (2008) Antimicrobial-resistant Streptococcus pneumoniae: trends and management. Expert Rev Anti Infect Ther 6: 619-635.
2. Zapun A, Contreras-Martel C, Vernet T, (2008) Penicillin-binding proteins and beta-lactam resistance. FEMS Microbiol Rev 32: 361-385.
3. Claverys JP, Prudhomme M, Martin B, (2006) Induction of competence regulons as a general response to stress in gram-positive bacteria. Annu Rev Microbiol 60: 451-475.
4. 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.
5. Maisnier-Patin S, Andersson DI, (2004) Adaptation to the deleterious effects of antimicrobial drug resistance mutations by compensatory evolution. Res Microbiol 155: 360-369.
6. Andersson DI, (2006) The biological cost of mutational antibiotic resistance: any practical conclusions? Curr Opin Microbiol 9: 461-465.
7. Balsalobre L, de la Campa AG, (2008) Fitness of Streptococcus pneumoniae fluoroquinolone-resistant strains with topoisomerase IV recombinant genes. Antimicrob Agents Chemother 52: 822-830.
8. Rozen DE, McGee L, Levin BR, Klugman KP, (2007) Fitness costs of fluoroquinolone resistance in Streptococcus pneumoniae. Antimicrob Agents Chemother 51: 412-416.
9. Briles DE, Crain MJ, Gray BM, Forman C, Yother J, (1992) Strong association between capsular type and virulence for mice among human isolates of Streptococcus pneumoniae. Infect Immun 60: 111-116.
10. Azoulay-Dupuis E, Rieux V, Muffat-Joly M, Bedos JP, Vallee E, et al. (2000) Relationship between capsular type, penicillin susceptibility, and virulence of human Streptococcus pneumoniae isolates in mice. Antimicrob Agents Chemother 44: 1575-1577.
11. Rieux V, Carbon C, Azoulay-Dupuis E, (2001) Complex relationship between acquisition of beta-lactam resistance and loss of virulence in Streptococcus pneumoniae. J Infect Dis 184: 66-72.
12. Trzcinski K, Thompson CM, Gilbey AM, Dowson CG, Lipsitch M, (2006) Incremental increase in fitness cost with increased beta-lactam resistance in pneumococci evaluated by competition in an infant rat nasal colonization model. J Infect Dis 193: 1296-1303.
13. Albarracin Orio AG, Cortes PR, Tregnaghi M, Pinas GE, Echenique JR, (2008) A new serotype 14 variant of the pneumococcal Spain9V-3 international clone detected in the central region of Argentina. J Med Microbiol 57: 992-999.
14. Cortes PR, Albarracín Orio AG, Regueira M, Piñas GE, Echenique J, (2008) Characterization of in vitro-generated and clinical optochin-resistant strains of Streptococcus pneumoniae isolated from Argentina. J Clin Microbiol 46: 1930-1934.
15. Di Guilmi AM, Mouz N, Andrieu JP, Hoskins J, Jaskunas SR, et al. (1998) Identification, purification, and characterization of transpeptidase and glycosyltransferase domains of Streptococcus pneumoniae penicillin-binding protein 1a. J Bacteriol 180: 5652-5659.
16. Morlot C, Zapun A, Dideberg O, Vernet T, (2003) Growth and division of Streptococcus pneumoniae: localization of the high molecular weight penicillin-binding proteins during the cell cycle. Mol Microbiol 50: 845-855.
17. Daniel RA, Errington J, (2003) Control of cell morphogenesis in bacteria: two distinct ways to make a rod-shaped cell. Cell 113: 767-776.
18. Desai BV, Morrison DA, (2006) An unstable competence-induced protein, CoiA, promotes processing of donor DNA after uptake during genetic transformation in Streptococcus pneumoniae. J Bacteriol 188: 5177-5186.
19. Lan G, Wolgemuth CW, Sun SX, (2007) Z-ring force and cell shape during division in rod-like bacteria. Proc Natl Acad Sci U S A 104: 16110-16115.
20. Lutkenhaus J, Addinall SG, (1997) Bacterial cell division and the Z ring. Annu Rev Biochem 66: 93-116.
21. Andersson DI, Levin BR, (1999) The biological cost of antibiotic resistance. Curr Opin Microbiol 2: 489-493.
22. Bjorkman J, Andersson DI, (2000) The cost of antibiotic resistance from a bacterial perspective. Drug Resist Updat 3: 237-245.
23. Dowson CG, Hutchison A, Brannigan JA, George RC, Hansman D, et al. (1989) Horizontal transfer of penicillin-binding protein genes in penicillin-resistant clinical isolates of Streptococcus pneumoniae. Proc Natl Acad Sci U S A 86: 8842-8846.
24. Reynolds MG, (2000) Compensatory Evolution in Rifampin-Resistant Escherichia coli. Genetics 156: 1471-1481.
25. Gagneux S, Long CD, Small PM, Van T, Schoolnik GK, et al. (2006) The competitive cost of antibiotic resistance in Mycobacterium tuberculosis. Science 312: 1944-1946.
26. Bjorkholm B, Sjolund M, Falk PG, Berg OG, Engstrand L, et al. (2001) Mutation frequency and biological cost of antibiotic resistance in Helicobacter pylori. Proc Natl Acad Sci U S A 98: 14607-14612.
27. Bottger EC, Springer B, Pletschette M, Sander P, (1998) Fitness of antibiotic-resistant microorganisms and compensatory mutations. Nat Med 4: 1343-1344.
28. Marcusson LL, Frimodt-Moller N, Hughes D, (2009) Interplay in the selection of fluoroquinolone resistance and bacterial fitness. PLoS Pathog 5: e1000541.
29. Zapun A, Vernet T, Pinho MG, (2008) The different shapes of cocci. FEMS Microbiol Rev 32: 345-360.
30. Morlot C, Noirclerc-Savoye M, Zapun A, Dideberg O, Vernet T, (2004) The D,D-carboxypeptidase PBP3 organizes the division process of Streptococcus pneumoniae. Mol Microbiol 51: 1641-1648.
31. Popham DL, Young KD, (2003) Role of penicillin-binding proteins in bacterial cell morphogenesis. Curr Opin Microbiol 6: 594-599.
32. Varma A, Young KD, (2004) FtsZ collaborates with penicillin binding proteins to generate bacterial cell shape in Escherichia coli. J Bacteriol 186: 6768-6774.
33. Vinella D, Joseleau-Petit D, Thevenet D, Bouloc P, D'Ari R, (1993) Penicillin-binding protein 2 inactivation in Escherichia coli results in cell division inhibition, which is relieved by FtsZ overexpression. J Bacteriol 175: 6704-6710.
34. Pernot L, Chesnel L, Le Gouellec A, Croize J, Vernet T, et al. (2004) A PBP2x from a clinical isolate of Streptococcus pneumoniae exhibits an alternative mechanism for reduction of susceptibility to beta-lactam antibiotics. J Biol Chem 279: 16463-16470.
35. Lu WP, Kincaid E, Sun Y, Bauer MD, (2001) Kinetics of beta-lactam interactions with penicillin-susceptible and-resistant penicillin-binding protein 2x proteins from Streptococcus pneumoniae. Involvement of acylation and deacylation in beta-lactam resistance. J Biol Chem 276: 31494-31501.
36. Lefevre JC, Bertrand MA, Faucon G, (1995) Molecular analysis by pulsed-field gel electrophoresis of penicillin-resistant Streptococcus pneumoniae from Toulouse, France. Eur J Clin Microbiol Infect Dis 14: 491-497.
37. CLSI CaLSI (2007) Performance Standards for Antimicrobial Susceptibility Testing; Seventeenth edition Information Supplement. CLSI document M100-S17 [ISBN1-56238-625-5]. Wayne, Pennsylvania Clinical and Laboratory Standards Institute.
38. Pinas GE, Cortes PR, Orio AG, Echenique J, (2008) Acidic stress induces autolysis by a CSP-independent ComE pathway in Streptococcus pneumoniae. Microbiology 154: 1300-1308.
39. Lenski RE, (1991) Quantifying fitness and gene stability in microorganisms. Biotechnology 15: 173-192.
40. Bjorkman J, Nagaev I, Berg OG, Hughes D, Andersson DI, (2000) Effects of environment on compensatory mutations to ameliorate costs of antibiotic resistance. Science 287: 1479-1482.
41. Lara B, Rico AI, Petruzzelli S, Santona A, Dumas J, et al. (2005) Cell division in cocci: localization and properties of the Streptococcus pneumoniae FtsA protein. Mol Microbiol 55: 699-711.
42. Hansen MC, Palmer RJ Jr, Udsen C, White DC, Molin S, (2001) Assessment of GFP fluorescence in cells of Streptococcus gordonii under conditions of low pH and low oxygen concentration. Microbiology 147: 1383-1391.
43. Claverys JP, Dintilhac A, Pestova EV, Martin B, Morrison DA, (1995) Construction and evaluation of new drug-resistance cassettes for gene disruption mutagenesis in Streptococcus pneumoniae, using an ami test platform. Gene 164: 123-128.
44. Trieu-Cuot P, Carlier C, Poyart-Salmeron C, Courvalin P, (1991) Shuttle vectors containing a multiple cloning site and a lacZ alpha gene for conjugal transfer of DNA from Escherichia coli to gram-positive bacteria. Gene 102: 99-104.
45. Noble JE, Bailey MJ, (2009) Quantitation of protein. Methods Enzymol 463: 73-95.