Structural changes and differentially expressed genes in Pseudomonas aeruginosa exposed to meropenem-ciprofloxacin combination

Antimicrobial Agents and Chemotherapy

Volumn 58, Issue 7, 2014, Pages 3957-3967

  Siqueira, Vera Lućia Dias ^a   Cardoso, Rosilene Fressatti ^a   Caleffi Ferracioli, Katiany Rizzieri ^a   De Lima Scodro, Regiane Bertin ^a   Fernandez, Maria Aparecida ^a   Fiorini, Adriana ^a   Ueda Nakamura, Tania ^a   Dias Filho, Benedito Prado ^a   Nakamura, Celso Vataru ^a  

^a STATE UNIVERSITY OF MARINGÁ   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE RACEMASE; CELL WALL ASSOCIATED HYDROLASE; CIPROFLOXACIN; COMPLEMENTARY DNA; CONTIG; DNA FRAGMENT; HYDROLASE; HYPOTHETICAL PROTEIN I; HYPOTHETICAL PROTEIN II; HYPOTHETICAL PROTEIN III; MEROPENEM; PEPTIDES AND PROTEINS; SERINE ACETYLTRANSFERASE; UNCLASSIFIED DRUG; URACIL DNA GLYCOSIDASE; ANTIINFECTIVE AGENT; BACTERIAL DNA; BACTERIAL RNA; DRUG COMBINATION; THIENAMYCIN DERIVATIVE;

ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ANTIMICROBIAL THERAPY; ARTICLE; BACTERIAL CELL; BACTERIAL CELL WALL; BACTERIAL COUNT; BACTERIAL GROWTH; BACTERIAL OUTER MEMBRANE; BACTERICIDAL ACTIVITY; BACTERIUM COLONY; BACTERIUM ISOLATE; COLONY FORMING UNIT; CONTROLLED STUDY; DNA REPAIR; DRUG POTENTIATION; ELECTRON MICROSCOPY; EXPRESSED SEQUENCE TAG; GENE EXPRESSION; HOSPITAL SUBDIVISIONS AND COMPONENTS; HUMAN; INOCULATION; LIMIT OF QUANTITATION; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; REPRESSOR GENE; RNA ISOLATION; SCANNING ELECTRON MICROSCOPY; TRANSMISSION ELECTRON MICROSCOPY; BACTERIAL GENE; BIOSYNTHESIS; BRAZIL; DRUG COMBINATION; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; MICROBIAL SENSITIVITY TEST; MICROBIOLOGY; MULTIDRUG RESISTANCE; POLYMERASE CHAIN REACTION; PSEUDOMONAS INFECTION; ULTRASTRUCTURE;

ANTI-BACTERIAL AGENTS; BRAZIL; CIPROFLOXACIN; COLONY COUNT, MICROBIAL; DNA, BACTERIAL; DRUG COMBINATIONS; DRUG RESISTANCE, MULTIPLE, BACTERIAL; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; HUMANS; MICROBIAL SENSITIVITY TESTS; POLYMERASE CHAIN REACTION; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS; RNA, BACTERIAL; THIENAMYCINS;

EID: 84903158590     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.02584-13     Document Type: Article

References (56)

1. Fothergill JL, Winstanley C, James CE. 2012. Novel therapeutic strategies to counter Pseudomonas aeruginosa infections. Expert Rev. Anti Infect. Ther. 10:219-235. http://dx.doi.org/10.1586/eri.11.168.
2. Strateva T, Yordanov D. 2009. Pseudomonas aeruginosa - a phenomenon of bacterial resistance. J. Med. Microbiol. 58:1133-1148. http://dx.doi.org/10. 1099/jmm.0.009142-0.
3. McGowan JE, Jr. 2006. Resistance in nonfermenting Gram-negative bacteria: multidrug resistance to the maximum. Am. J. Med. 119(Suppl 1): S29-S36. http://dx.doi.org/10.1016/j.amjmed.2006.03.014.
4. Mangoni ML, Maisetta G, Di Luca M, Gaddi LM, Esin S, Florio W, Brancatisano FL, Barra D, Campa M, Batoni G. 2008. Comparative analysis of the bactericidal activities of amphibian peptide analogues against multidrug-resistant nosocomial bacterial strains. Antimicrob. Agents Chemother. 52:85-91. http://dx.doi.org/10.1128/AAC.00796-07.
5. Mesaros N, Nordmann P, Plesiat P, Roussel-Delvallez M, Van Eldere J, Glupczynski Y, Van Laethem Y, Jacobs F, Lebecque P, Malfroot A, Tulkens PM, Van Bambeke F. 2007. Pseudomonas aeruginosa: resistance and therapeutic options at the turn of the new millennium. Clin. Microbiol. Infect. 13:560-578. http://dx.doi.org/10.1111/j.1469-0691.2007.01681.x. (Pubitemid 46730662)
6. El Solh AA, Alhajhusain A. 2009. Update on the treatment of Pseudomonas aeruginosa pneumonia. J. Antimicrob. Chemother. 64:229-238. http://dx.doi.org/ 10.1093/jac/dkp201.
7. Cirioni O, Ghiselli R, Silvestri C, Kamysz W, Orlando F, Mocchegiani F, Di Matteo F, Riva A, Lukasiak J, Scalise G, Saba V, Giacometti A. 2007. Efficacy of tachyplesin III, colistin, and imipenem against a multiresistant Pseudomonas aeruginosa strain. Antimicrob. Agents Chemother. 51:2005-2010. http://dx.doi.org/10.1128/AAC.01576-06. (Pubitemid 46903087)
8. Kanellakopoulou K, Sarafis P, Galani I, Giamarellou H, Giamarellos-Bourboulis EJ. 2008. In vitro synergism of β-lactams with ciprofloxacin and moxifloxacin against genetically distinct multidrug-resistant isolates of Pseudomonas aeruginosa. Int. J. Antimicrob. Agents 32:33-39. http://dx.doi.org/10.1016/j.ijantimicag.2008.02.019.
9. Lim TP, Lee W, Tan TY, Sasikala S, Teo J, Hsu LY, Tan TT, Syahidah N, Kwa AL. 2011. Effective antibiotics in combination against extreme drug-resistant Pseudomonas aeruginosa with decreased susceptibility to polymyxin B. PLoS One 6:e28177. http://dx.doi.org/10.1371/journal.pone.0028177.
10. Louie A, Grasso C, Bahniuk N, Van Scoy B, Brown DL, Kulawy R, Drusano GL. 2010. The combination of meropenem and levofloxacin is synergistic with respect to both Pseudomonas aeruginosa kill rate and resistance suppression. Antimicrob. Agents Chemother. 54:2646-2654. http://dx.doi.org/10.1128/AAC.00065- 10.
11. Lister PD, Wolter DJ, Wickman PA, Reisbig MD. 2006. Levofloxacin/imipenem prevents the emergence of high-level resistance among Pseudomonas aeruginosa strains already lacking susceptibility to one or both drugs. J. Antimicrob. Chemother. 57:999-1003. http://dx.doi.org/10.1093/jac/dkl063.
12. Ermertcan S, Hosgor M, Tunger O, Cosar G. 2001. Investigation of synergism of meropenem and ciprofloxacin against Pseudomonas aeruginosa and Acinetobacter strains isolated from intensive care unit infections. Scand. J. Infect. Dis. 33:818-821. http://dx.doi.org/10.1080/00365540110027222. (Pubitemid 33069519)
13. Solak S, Willke A, Ergonul O, Tekeli E. 2005. In vitro activity of meropenem in combination with ciprofloxacin against clinical isolates of Pseudomonas aeruginosa. Int. J. Antimicrob. Agents 25:181-182. http://dx.doi.org/10.1016/j.ijantimicag.2004.11.005. (Pubitemid 40138959)
14. Pankuch GA, Lin G, Seifert H, Appelbaum PC. 2008. Activity of meropenem with and without ciprofloxacin and colistin against Pseudomonas aeruginosa and Acinetobacter baumannii. Antimicrob. Agents Chemother. 52:333-336. http://dx.doi.org/10.1128/AAC.00689-07.
15. Erdem I, Kucukercan M, Ceran N. 2003. In vitro activity of combination therapy with cefepime, piperacillin-tazobactam, or meropenem with ciprofloxacin against multidrug-resistant Pseudomonas aeruginosa strains. Chemotherapy 49:294-297. http://dx.doi.org/10.1159/000074529. (Pubitemid 37524131)
16. Rossi F. 2011. The challenges of antimicrobial resistance in Brazil. Clin. Infect. Dis. 52:1138-1143. http://dx.doi.org/10.1093/cid/cir120.
17. Zavascki AP, Carvalhaes CG, Picao RC, Gales AC. 2010. Multidrugresistant Pseudomonas aeruginosa and Acinetobacter baumannii: resistance mechanisms and implications for therapy. Expert Rev. Anti Infect. Ther. 8:71-93. http://dx.doi.org/10.1586/eri.09.108.
18. Siqueira VLD, Cardoso RF, Pádua RAF, Caleffi-Ferracioli KR, Helbel C, Santos ACB, Aoki EE, Nakamura CV. 2013. High genetic diversity among Pseudomonas aeruginosa and Acinetobacter spp. isolated in a public hospital in Brazil. Braz. J. Pharm. Sci. 49:49-56. http://dx.doi.org/10.1590/S1984- 82502013000100006.
19. Clinical and Laboratory Standards Institute. 2012. Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically; approved standard. Clinical and Laboratory Standards Institute, Wayne, PA.
20. Clinical and Laboratory Standards Institute. 2012. Performance standards for antimicrobial susceptibility testing; 22nd informational supplement. Clinical and Laboratory Standards Institute, Wayne, PA.
21. Pillai SK, Moellering RC, Eliopoulos GM. 2005. Antimicrobial combinations, p 365-440. In Lorian V (ed), Antibiotics in laboratory medicine, 5th ed. Lippincott Williams & Wilkins, New York, NY.
22. Odds FC. 2003. Synergy, antagonism, and what the chequerboard puts between them. J. Antimicrob. Chemother. 52:1. http://dx.doi.org/10.1093/jac/ dkg301. (Pubitemid 36850074)
23. Leite GGS, Baeza LC, Batista AA, Barbosa MFI, Pavan FL, Leite CQF, Silva JL, Hirata RDC, Hirata MH, Cardoso RF. 2013. Genes differentially expressed by Mycobacterium tuberculosis after exposure to ruthenium phosphinic compound and isoniazid. Intern. J. Microbiol. Res. 5:356-361. http://dx.doi.org/10.9735/0975- 5276.5.1.357-362.
24. Del Sal G, Manfioletti G, Schneider C. 1989. The CTAB-DNA precipitation method: a common mini-scale preparation of template DNA from phagemids, phages or plasmids suitable for sequencing. Biotechniques 7:514-520.
25. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402. http://dx.doi.org/10.1093/nar/ 25.17.3389. (Pubitemid 27359211)
26. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402-408. http://dx.doi.org/10.1006/meth.2001.1262. (Pubitemid 34164012)
27. Ocampo-Sosa AA, Cabot G, Rodriguez C, Roman E, Tubau F, Macia MD, Moya B, Zamorano L, Suarez C, Pena C, Dominguez MA, Moncalian G, Oliver A, Martinez-Martinez L. 2012. Alterations of OprD in carbapenem-intermediate and -susceptible strains of Pseudomonas aeruginosa isolated from patients with bacteremia in a Spanish multicenter study. Antimicrob. Agents Chemother. 56:1703-1713. http://dx.doi.org/10.1128/AAC.05451-11.
28. Bodí M, Garnacho J. 2007. Pseudomonas aeruginosa: combined treatment vs. monotherapy. Med. Intensiva 31:83-87. (In Spanish.) doi:http://dx.doi.org/10.1016/S0210-5691(07)74780-0.
29. Isenberg HD, Alperstein P, France K. 1999. In vitro activity of ciprofloxacin, levofloxacin, and trovafloxacin, alone and in combination with beta-lactams, against clinical isolates of Pseudomonas aeruginosa, Stenotrophomonas maltophilia, and Burkholderia cepacia. Diagn. Microbiol. Infect. Dis. 33:81-86. http://dx.doi.org/10.1016/S0732-8893(98)00126-6. (Pubitemid 29115035)
30. Campana S, Taccetti G, Farina S, Ravenni N, de Martino M. 2003. Antimicrobial susceptibility and synergistic activity of meropenem against Gram-negative non-fermentative bacteria isolated from cystic fibrosis patients. J. Chemother. 15: 551-554. http://dx.doi.org/10.1179/joc.2003.15.6.551. (Pubitemid 38241402)
31. Cappelletty DM, Rybak MJ. 1996. Comparison of methodologies for synergism testing of drug combinations against resistant strains of Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 40:677-683. (Pubitemid 26071535)
32. Bonapace CR, White RL, Friedrich LV, Bosso JA. 2000. Evaluation of antibiotic synergy against Acinetobacter baumannii: a comparison with Etest, time-kill, and checkerboard methods. Diagn. Microbiol. Infect. Dis. 38:43-50. http://dx.doi.org/10.1016/S0732-8893(00)00163-2.
33. Beveridge TJ. 1999. Structures of gram-negative cell walls and their derived membrane vesicles. J. Bacteriol. 181:4725-4733. (Pubitemid 29383496)
34. Bomberger JM, Maceachran DP, Coutermarsh BA, Ye S, O'Toole GA, Stanton BA. 2009. Long-distance delivery of bacterial virulence factors by Pseudomonas aeruginosa outer membrane vesicles. PLoS Pathog. 5:e1000382. http://dx.doi.org/10.1371/journal.ppat.1000382.
35. Tashiro Y, Uchiyama H, Nomura N. 2012. Multifunctional membrane vesicles in Pseudomonas aeruginosa. Environ. Microbiol. 14:1349-1362. http://dx.doi.org/10.1111/j.1462-2920.2011.02632.x.
36. Maredia R, Devineni N, Lentz P, Dallo SF, Yu J, Guentzel N, Chambers J, Arulanandam B, Haskins WE, Weitao T. 2012. Vesiculation from Pseudomonas aeruginosa under SOS. ScientificWorldJournal 2012:402919. http://dx.doi.org/10. 1100/2012/402919.
37. Cirz RT, O'Neill BM, Hammond JA, Head SR, Romesberg FE. 2006. Defining the Pseudomonas aeruginosa SOS response and its role in the global response to the antibiotic ciprofloxacin. J. Bacteriol. 188:7101-7110. http://dx.doi.org/10. 1128/JB.00807-06. (Pubitemid 44547615)
38. Waisbren SJ, Hurley DJ, Waisbren BA. 1980. Morphological expressions of antibiotic synergism against Pseudomonas aeruginosa as observed by scanning electron microscopy. Antimicrob. Agents Chemother. 18:969-975. http://dx.doi.org/10.1128/AAC.18.6.969. (Pubitemid 11183003)
39. Hayami H, Goto T, Kawahara M, Ohi Y. 1999. Activities of beta-lactams, fluoroquinolones, amikacin and fosfomycin alone and in combination against Pseudomonas aeruginosa isolated from complicated urinary tract infections. J. Infect. Chemother. 5:130-138. http://dx.doi.org/10.1007/s101560050022. (Pubitemid 29484858)
40. Kolayli F, Karadenizli A, Savli H, Ergen K, Hatirnaz O, Balikci E, Budak F, Vahaboglu H. 2004. Effect of carbapenems on the transcriptional expression of the oprD, oprM and oprN genes in Pseudomonas aeruginosa. J. Med. Microbiol. 53:915-920. http://dx.doi.org/10.1099/jmm.0.45692-0. (Pubitemid 39238399)
41. Juan C, Macia MD, Gutierrez O, Vidal C, Perez JL, Oliver A. 2005. Molecular mechanisms of beta-lactam resistance mediated by AmpC hyperproduction in Pseudomonas aeruginosa clinical strains. Antimicrob. Agents Chemother. 49:4733-4738. http://dx.doi.org/10.1128/AAC.49.11.4733-4738.2005. (Pubitemid 41552606)
42. Hay T, Fraud S, Lau CH, Gilmour C, Poole K. 2013. Antibiotic inducibility of the mexXY multidrug efflux operon of Pseudomonas aeruginosa: involvement of the MexZ anti-repressor ArmZ. PLoS One 8:e56858. http://dx.doi.org/10.1371/ journal.pone.0056858.
43. Saravanamuthu SS, von Gotz F, Salunkhe P, Chozhavendan R, Geffers R, Buer J, Tummler B, Steinmetz I. 2004. Evidence for polyadenylated mRNA in Pseudomonas aeruginosa. J. Bacteriol. 186:7015-7018. http://dx.doi.org/10.1128/ JB.186.20.7015-7018.2004. (Pubitemid 39332140)
44. Olsen LR, Huang B, Vetting MW, Roderick SL. 2004. Structure of serine acetyltransferase in complexes with CoA and its cysteine feedback inhibitor. Biochemistry 43:6013-6019. http://dx.doi.org/10.1021/bi0358521. (Pubitemid 38669469)
45. Sugawara E, Steiert M, Rouhani S, Nikaido H. 1996. Secondary structure of the outer membrane proteins OmpA of Escherichia coli and OprF of Pseudomonas aeruginosa. J. Bacteriol. 178:6067-6069. (Pubitemid 26337797)
46. Bratu S, Landman D, Gupta J, Quale J. 2007. Role of AmpD, OprF and penicillin-binding proteins in beta-lactam resistance in clinical isolates of Pseudomonas aeruginosa. J. Med. Microbiol. 56(Pt 6):809-814. http://dx.doi.org/10.1099/jmm.0.47019-0. (Pubitemid 46911237)
47. Rawling EG, Brinkman FS, Hancock RE. 1998. Roles of the carboxyterminal half of Pseudomonas aeruginosa major outer membrane protein OprF in cell shape, growth in low-osmolarity medium, and peptidoglycan association. J. Bacteriol. 180:3556-3562. (Pubitemid 29115083)
48. Fito-Boncompte L, Chapalain A, Bouffartigues E, Chaker H, Lesouhaitier O, Gicquel G, Bazire A, Madi A, Connil N, Veron W, Taupin L, Toussaint B, Cornelis P, Wei Q, Shioya K, Deziel E, Feuilloley MG, Orange N, Dufour A, Chevalier S. 2011. Full virulence of Pseudomonas aeruginosa requires OprF. Infect. Immun. 79:1176-1186. http://dx.doi.org/10.1128/IAI.00850-10.
49. Wessel AK, Liew J, Kwon T, Marcotte EM, Whiteley M. 2013. Role of Pseudomonas aeruginosa peptidoglycan-associated outer membrane proteins in vesicle formation. J. Bacteriol. 195:213-219. http://dx.doi.org/10.1128/JB. 01253-12.
50. Johnson JW, Fisher JF, Mobashery S. 2013. Bacterial cell-wall recycling. Ann. N. Y. Acad. Sci. 1277:54-75. http://dx.doi.org/10.1111/j.1749-6632.2012. 06813.x.
51. Lambert MP, Neuhaus FC. 1972. Factors affecting the level of alanine racemase in Escherichia coli. J. Bacteriol. 109:1156-1161.
52. Bryskier A. 1993. Fluoroquinolones: mechanisms of action and resistance. Int.J.Antimicrob.Agents2:151-183.http://dx.doi.org/10.1016/0924-8579(93)90052-7.
53. Pearl LH. 2000. Structure and function in the uracil-DNA glycosylase superfamily. Mutat. Res. 460:165-181. http://dx.doi.org/10.1016/S0921-8777(00) 00025-2. (Pubitemid 30628589)
54. Hocquet D, Llanes C, Thouverez M, Kulasekara HD, Bertrand X, Plesiat P, Mazel D, Miller SI. 2012. Evidence for induction of integronbased antibiotic resistance by the SOS response in a clinical setting. PLoS Pathog. 8:e1002778. http://dx.doi.org/10.1371/journal.ppat.1002778.
55. Dumas JL, van Delden C, Perron K, Kohler T. 2006. Analysis of antibiotic resistance gene expression in Pseudomonas aeruginosa by quantitative real-time-PCR. FEMS Microbiol. Lett. 254:217-225. http://dx.doi.org/10.1111/j. 1574-6968.2005.00008.x.
56. Liu X, Li J, Wang Y, Li T, Zhao J, Zhang C. 2013. Green tea polyphenols function as prooxidants to inhibit Pseudomonas aeruginosa and induce the expression of oxidative stress-related genes. Folia Microbiol. (Praha) 58: 211-217. http://dx.doi.org/10.1007/s12223-012-0198-2.