A low-affinity penicillin-binding protein 2x variant is required for heteroresistance in Streptococcus pneumoniae

Antimicrobial Agents and Chemotherapy

Volumn 58, Issue 7, 2014, Pages 3934-3941

  Engel, Hansjürg ^a   Mika, Moana ^a   Denapaite, Dalia ^b   Hakenbeck, Regine ^b   Muḧlemann, Kathrin ^a   Heller, Manfred ^a   Hathaway, Lucy J ^a   Hilty, Markus ^a  

^a UNIVERSITY OF BERN   (Switzerland)

^b University of Koblenz Landau   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; BETA LACTAM; PENICILLIN BINDING PROTEIN 2B; PENICILLIN BINDING PROTEIN 2X; PENICILLIN DERIVATIVE; PHOU PROTEIN; PSTB PROTEIN; PSTC PROTEIN; PSTS PROTEIN; UNCLASSIFIED DRUG; BACTERIAL DNA; PBP 2X PROTEIN, STREPTOCOCCUS; PENICILLIN BINDING PROTEIN;

ANALYTIC METHOD; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BINDING AFFINITY; CONTROLLED STUDY; GENETIC VARIABILITY; HETERORESISTANCE; NONHUMAN; PHENOTYPE; POPULATION ANALYSIS PROFILING; PRIORITY JOURNAL; PROGENY; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPAIN; STREPTOCOCCUS PNEUMONIAE; UPREGULATION; BACTERIUM TRANSFORMATION; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; METABOLISM; MICROBIAL SENSITIVITY TEST; MICROBIOLOGY; MULTIDRUG RESISTANCE; PENICILLIN RESISTANCE; PNEUMOCOCCAL INFECTION; PROCEDURES; PROTEOMICS;

DNA, BACTERIAL; DRUG RESISTANCE, MULTIPLE, BACTERIAL; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; MICROBIAL SENSITIVITY TESTS; PENICILLIN RESISTANCE; PENICILLIN-BINDING PROTEINS; PNEUMOCOCCAL INFECTIONS; PROTEOMICS; REAL-TIME POLYMERASE CHAIN REACTION; STREPTOCOCCUS PNEUMONIAE; TRANSFORMATION, BACTERIAL;

EID: 84903164753     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.02547-14     Document Type: Article

References (48)

1. O'Brien KL, Wolfson LJ, Watt JP, Henkle E, Deloria-Knoll M, McCall N, Lee E, Mulholland K, Levine OS, Cherian T, Hib Pneumococcal Global Burden of Disease Study. 2009. Burden of disease caused by Streptococcus pneumoniae in children younger than 5 years: global estimates. Lancet 374:893-902. http://dx.doi.org/10.1016/S0140-6736(09)61204-6.
2. Klugman KP. 2002. The successful clone: the vector of dissemination of resistance in Streptococcus pneumoniae. J. Antimicrob. Chemother. 50(Suppl. 2):1-5. http://dx.doi.org/10.1093/jac/dkf500. (Pubitemid 36175831)
3. McGee L, McDougal L, Zhou J, Spratt BG, Tenover FC, George R, Hakenbeck R, Hryniewicz W, Lefevre JC, Tomasz A, Klugman KP. 2001. Nomenclature of major antimicrobial-resistant clones of Streptococcus pneumoniae defined by the pneumococcal molecular epidemiology network. J. Clin. Microbiol. 39:2565-2571. http://dx.doi.org/10.1128/JCM.39.7.2565-2571.2001. (Pubitemid 32606233)
4. 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.
5. Martin C, Sibold C, Hakenbeck R. 1992. Relatedness of penicillin-binding protein 1a genes from different clones of penicillin-resistant Streptococcus pneumoniae isolated in South Africa and Spain. EMBO J. 11:3831-3836.
6. 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. (Pubitemid 23248774)
7. Dowson CG, Hutchison A, Brannigan JA, George RC, Hansman D, Linares J, Tomasz A, Smith JM, Spratt BG. 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. http://dx.doi.org/10. 1073/pnas.86.22.8842. (Pubitemid 20010321)
8. Reichmann P, Konig A, Linares J, Alcaide F, Tenover FC, McDougal L, Swidsinski S, Hakenbeck R. 1997. A global gene pool for high-level cephalosporin resistance in commensal Streptococcus species and Streptococcus pneumoniae. J. Infect. Dis. 176:1001-1012. http://dx.doi.org/10.1086/516532. (Pubitemid 27411043)
9. Munoz R, Coffey TJ, Daniels M, Dowson CG, Laible G, Casal J, Hakenbeck R, Jacobs M, Musser JM, Spratt BG, Tomasz A. 1991. Intercontinental spread of a multiresistant clone of serotype 23F Streptococcus pneumoniae. J. Infect. Dis. 164:302-306. http://dx.doi.org/10.1093/infdis/164.2.302.
10. Filipe SR, Tomasz A. 2000. Inhibition of the expression of penicillin resistance in Streptococcus pneumoniae by inactivation of cell wall muropeptide branching genes. Proc. Natl. Acad. Sci. U. S. A. 97:4891-4896. http://dx.doi.org/10.1073/pnas.080067697. (Pubitemid 30238653)
11. Smith AM, Klugman KP. 2001. Alterations in MurM, a cell wall muropeptide branching enzyme, increase high-level penicillin and cephalosporin resistance in Streptococcus pneumoniae. Antimicrob. Agents Chemother. 45: 2393-2396. http://dx.doi.org/10.1128/AAC.45.8.2393-2396.2001. (Pubitemid 32664488)
12. Guenzi E, Gasc AM, Sicard MA, Hakenbeck R. 1994. A two-component signal-transducing system is involved in competence and penicillin susceptibility in laboratory mutants of Streptococcus pneumoniae. Mol. Microbiol. 12:505-515. http://dx.doi.org/10.1111/j.1365-2958.1994.tb01038.x. (Pubitemid 24197505)
13. Halfmann A, Kovacs M, Hakenbeck R, Bruckner R. 2007. Identification of the genes directly controlled by the response regulator CiaR in Streptococcus pneumoniae: five out of 15 promoters drive expression of small non-coding RNAs. Mol. Microbiol. 66:110-126. http://dx.doi.org/10.1111/j.1365-2958.2007.05900.x. (Pubitemid 47414793)
14. Muller M, Marx P, Hakenbeck R, Bruckner R. 2011. Effect of new alleles of the histidine kinase gene ciaH on the activity of the response regulator CiaR in Streptococcus pneumoniae R6. Microbiology 157:3104-3112. http://dx.doi.org/ 10.1099/mic.0.053157-0.
15. Hakenbeck R, Bruckner 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.
16. Morand B, Mühlemann K. 2007. Heteroresistance to penicillin in Streptococcus pneumoniae. Proc. Natl. Acad. Sci. U. S. A. 104:14098-14103. http://dx.doi.org/10.1073/pnas.0702377104. (Pubitemid 350003341)
17. de Lencastre H, Figueiredo AM, Tomasz A. 1993. Genetic control of population structure in heterogeneous strains of methicillin resistant Staphylococcus aureus. Eur. J. Clin. Microbiol. Infect. Dis. 12(Suppl. 1):S13-S18. http://dx.doi.org/10.1007/BF02389872. (Pubitemid 23104604)
18. Ender M, Berger-Bachi B, McCallum N. 2009. A novel DNA-binding protein modulating methicillin resistance in Staphylococcus aureus. BMC Microbiol. 9:15. http://dx.doi.org/10.1186/1471-2180-9-15.
19. Finan JE, Rosato AE, Dickinson TM, Ko D, Archer GL. 2002. Conversion of oxacillin-resistant staphylococci from heterotypic to homotypic resistance expression. Antimicrob. Agents Chemother. 46:24-30. http://dx.doi.org/10.1128/ AAC.46.1.24-30.2002. (Pubitemid 34031597)
20. Hartman BJ, Tomasz A. 1986. Expression of methicillin resistance in heterogeneous strains of Staphylococcus aureus. Antimicrob. Agents Chemother. 29:85-92. http://dx.doi.org/10.1128/AAC.29.1.85. (Pubitemid 16155227)
21. Murakami K, Tomasz A. 1989. Involvement of multiple genetic determinants in high-level methicillin resistance in Staphylococcus aureus. J. Bacteriol. 171:874-879. (Pubitemid 19053483)
22. Ryffel C, Strassle A, Kayser FH, Berger-Bachi B. 1994. Mechanisms of heteroresistance in methicillin-resistant Staphylococcus aureus. Antimicrob. Agents Chemother. 38:724-728. http://dx.doi.org/10.1128/AAC.38.4.724. (Pubitemid 24114008)
23. Tomasz A, Nachman S, Leaf H. 1991. Stable classes of phenotypic expression in methicillin-resistant clinical isolates of staphylococci. Antimicrob. Agents Chemother. 35:124-129. http://dx.doi.org/10.1128/AAC.35.1. 124.
24. Hung KH, Wang MC, Huang AH, Yan JJ, Wu JJ. 2012. Heteroresistance to cephalosporins and penicillins in Acinetobacter baumannii. J. Clin. Microbiol. 50:721-726. http://dx.doi.org/10.1128/JCM.05085-11.
25. Li J, Rayner CR, Nation RL, Owen RJ, Spelman D, Tan KE, Liolios L. 2006. Heteroresistance to colistin in multidrug-resistant Acinetobacter baumannii. Antimicrob. Agents Chemother. 50:2946-2950. http://dx.doi.org/10.1128/AAC.00103- 06. (Pubitemid 44396396)
26. Pournaras S, Ikonomidis A, Markogiannakis A, Spanakis N, Maniatis AN, Tsakris A. 2007. Characterization of clinical isolates of Pseudomonas aeruginosa heterogeneously resistant to carbapenems. J. Med. Microbiol. 56:66-70. http://dx.doi.org/10.1099/jmm.0.46816-0. (Pubitemid 46036277)
27. Pournaras S, Ikonomidis A, Neou E, Kantzanou M, Maniatis AN, Tsakris A. 2008. Piperacillin/tazobactam-heteroresistant Pseudomonas aeruginosa from urinary infection, successfully treated by piperacillin/tazobactam. J. Antimicrob. Chemother. 61:757-758. http://dx.doi.org/10.1093/jac/dkm528. (Pubitemid 351321163)
28. Alam MR, Donabedian S, Brown W, Gordon J, Chow JW, Zervos MJ, Hershberger E. 2001. Heteroresistance to vancomycin in Enterococcus faecium. J. Clin. Microbiol. 39:3379-3381. http://dx.doi.org/10.1128/JCM.39.9.3379-3381.2001. (Pubitemid 32830347)
29. Rinder H, Mieskes KT, Loscher T. 2001. Heteroresistance in Mycobacterium tuberculosis. Int. J. Tuberc. Lung Dis. 5:339-345. (Pubitemid 32397584)
30. Varma A, Kwon-Chung KJ. 2010. Heteroresistance of Cryptococcus gattii to fluconazole. Antimicrob. Agents Chemother. 54:2303-2311. http://dx.doi.org/10. 1128/AAC.00153-10.
31. Yamazumi T, Pfaller MA, Messer SA, Houston AK, Boyken L, Hollis RJ, Furuta I, Jones RN. 2003. Characterization of heteroresistance to fluconazole among clinical isolates of Cryptococcus neoformans. J. Clin. Microbiol. 41:267-272. http://dx.doi.org/10.1128/JCM.41.1.267-272.2003.
32. Engel H, Gutierrez-Fernandez J, Fluckiger C, Martinez-Ripoll M, Muhlemann K, Hermoso JA, Hilty M, Hathaway LJ. 2013. Heteroresistance to fosfomycin is predominant in Streptococcus pneumoniae and depends on the murA1 gene. Antimicrob. Agents Chemother. 57:2801-2808. http://dx.doi.org/10.1128/AAC.00223- 13.
33. Avery SV. 2006. Microbial cell individuality and the underlying sources of heterogeneity. Nat. Rev. Microbiol. 4:577-587. http://dx.doi.org/10.1038/ nrmicro1460. (Pubitemid 44317020)
34. Zerfass I, Hakenbeck R, Denapaite D. 2009. An important site in PBP2x of penicillin-resistant clinical isolates of Streptococcus pneumoniae: mutational analysis of Thr338. Antimicrob. Agents Chemother. 53:1107-1115. http://dx.doi.org/10.1128/AAC.01107-08.
35. Shevchuk NA, Bryksin AV, Nusinovich YA, Cabello FC, Sutherland M, Ladisch S. 2004. Construction of long DNA molecules using long PCR-based fusion of several fragments simultaneously. Nucleic Acids Res. 32:e19. http://dx.doi.org/10.1093/nar/gnh014.
36. Brugger SD, Hathaway LJ, Muhlemann K. 2009. Detection of Streptococcus pneumoniae strain cocolonization in the nasopharynx. J. Clin. Microbiol. 47:1750-1756. http://dx.doi.org/10.1128/JCM.01877-08.
37. Mascher T, Heintz M, Zahner D, Merai M, Hakenbeck R. 2006. The CiaRH system of Streptococcus pneumoniae prevents lysis during stress induced by treatment with cell wall inhibitors and by mutations in pbp2x involved in beta-lactam resistance. J. Bacteriol. 188:1959-1968. http://dx.doi.org/10.1128/ JB.188.5.1959-1968.2006. (Pubitemid 43346876)
38. Meier PS, Utz S, Aebi S, Muhlemann K. 2003. Low-level resistance to rifampin in Streptococcus pneumoniae. Antimicrob. Agents Chemother. 47:863-868. http://dx.doi.org/10.1128/AAC.47.3.863-868.2003. (Pubitemid 36254207)
39. Hathaway LJ, Battig P, Muhlemann K. 2007. In vitro expression of the first capsule gene of Streptococcus pneumoniae, cpsA, is associated with serotype-specific colonization prevalence and invasiveness. Microbiology 153:2465-2471. http://dx.doi.org/10.1099/mic.0.2006/005066-0. (Pubitemid 47262036)
40. Haenni M, Moreillon P. 2006. Mutations in penicillin-binding protein (PBP) genes and in non-PBP genes during selection of penicillin-resistant Streptococcus gordonii. Antimicrob. Agents Chemother. 50:4053-4061. http://dx.doi.org/10.1128/AAC.00676-06. (Pubitemid 44865149)
41. Haenni M, Moreillon P, Lazarevic V. 2007. Promoter and transcription analysis of penicillin-binding protein genes in Streptococcus gordonii. Antimicrob. Agents Chemother. 51:2774-2783. http://dx.doi.org/10.1128/AAC.01127- 06. (Pubitemid 47206212)
42. 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. http://dx.doi.org/10.1046/j.1365-2958.2003.03767.x. (Pubitemid 37372248)
43. Paik J, Kern I, Lurz R, Hakenbeck R. 1999. Mutational analysis of the Streptococcus pneumoniae bimodular classApenicillin-binding proteins. J. Bacteriol. 181:3852-3856. (Pubitemid 29283819)
44. Smith AM, Klugman KP. 1998. Alterations in PBP 1A essential-for highlevel penicillin resistance in Streptococcus pneumoniae. Antimicrob. Agents Chemother. 42:1329-1333. (Pubitemid 28257625)
45. Zhao G, Yeh WK, Carnahan RH, Flokowitsch J, Meier TI, Alborn WE, Jr, Becker GW, Jaskunas SR. 1997. Biochemical characterization of penicillin-resistant and -sensitive penicillin-binding protein 2x transpeptidase activities of Streptococcus pneumoniae and mechanistic implications in bacterial resistance to beta-lactam antibiotics. J. Bacteriol. 179:4901-4908. (Pubitemid 27339739)
46. Soualhine H, Brochu V, Menard F, Papadopoulou B, Weiss K, Bergeron MG, Legare D, Drummelsmith J, Ouellette M. 2005. A proteomic analysis of penicillin resistance in Streptococcus pneumoniae reveals a novel role for PstS, a subunit of the phosphate ABC transporter. Mol. Microbiol. 58:1430-1440. http://dx.doi.org/10.1111/j.1365-2958.2005.04914.x. (Pubitemid 41705420)
47. Avery OT, Macleod CM, McCarty M. 1944. Studies on the chemical nature of the substance inducing transformation of pneumococcal types: induction of transformation by a desoxyribonucleic acid fraction isolated from pneumococcus type III. J. Exp. Med. 79:137-158. http://dx.doi.org/10.1084/jem.79.2.137.
48. Mascher T, Zahner D, Merai M, Balmelle N, de Saizieu AB, Hakenbeck R. 2003. The Streptococcus pneumoniae cia regulon: CiaR target sites and transcription profile analysis. J. Bacteriol. 185:60-70. http://dx.doi.org/10. 1128/JB.185.1.60-70.2003. (Pubitemid 36008822)