Investigating the Link Between Imipenem Resistance and Biofilm Formation by Pseudomonas aeruginosa

O’Toole G, Kaplan HB, Kolter R (2000) Biofilm formation as microbial development. Annu Rev Microbiol 54:49–79 Davies DG, Parsek MR, Pearson JP, Iglewski BH, Costerton JW, Greenberg EP (1998) The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 280:295–298 Sanchez-Romero I, Cercenado E, Cuevas O, Garcia-Escribano N, Garcia-Martinez J, Bouza E (2007) Evolution of the antimicrobial resistance of Pseudomonas aeruginosa in Spain: second national study (2003). Rev Esp Quimioterapia Publ Oficial Soc Esp Quimioterapia 20:222–229 Ruiz-Martinez L, Lopez-Jimenez L, Fuste E, Vinuesa T, Martinez JP, Vinas M (2011) Class 1 integrons in environmental and clinical isolates of Pseudomonas aeruginosa. Int J Antimicrob Agents 38:398–402 Riera E, Cabot G, Mulet X, Garcia-Castillo M, del Campo R, Juan C, Canton R, Oliver A (2011) Pseudomonas aeruginosa carbapenem resistance mechanisms in Spain: impact on the activity of Imipenem, meropenem and doripenem. J Antimicrob Chemother 66(9):2022–2027 Lynch MJ, Drusano GL, Mobley HL (1987) Emergence of resistance to imipenem in Pseudomonas aeruginosa. Antimicrob Agents Chemother 31:1892–1896 Wolter DJ, Hanson ND, Lister PD (2004) Insertional inactivation of oprD in clinical isolates of Pseudomonas aeruginosa leading to carbapenem resistance. FEMS Microbiol Lett 236:137–143 Wolter DJ, Khalaf N, Robledo IE, Vazquez GJ, Sante MI, Aquino EE, Goering RV, Hanson ND (2009) Surveillance of carbapenem-resistant Pseudomonas aeruginosa isolates from Puerto Rican Medical Center Hospitals: dissemination of KPC and IMP-18 beta-lactamases. Antimicrob Agents Chemother 53:1660–1664. doi:10.1128/AAC.01172-08 Wolter DJ, Acquazzino D, Goering RV, Sammut P, Khalaf N, Hanson ND (2008) Emergence of carbapenem resistance in Pseudomonas aeruginosa isolates from a patient with cystic fibrosis in the absence of carbapenem therapy. Clin Infect Dis 46:e137–e141 Evans JC, Segal H (2007) A novel insertion sequence, ISPA26, in oprD of Pseudomonas aeruginosa is associated with carbapenem resistance. Antimicrob Agents Chemother 51:3776–3777 Yoneyama H, Nakae T (1993) Mechanism of efficient elimination of protein D2 in outer membrane of imipenem-resistant Pseudomonas aeruginosa. Antimicrob Agents Chemother 37:2385–2390 Pirnay JP, De Vos D, Mossialos D, Vanderkelen A, Cornelis P, Zizi M (2002) Analysis of the Pseudomonas aeruginosa oprD gene from clinical and environmental isolates. Environ Microbiol 4:872–882 El Amin N, Giske CG, Jalal S, Keijser B, Kronvall G, Wretlind B (2005) Carbapenem resistance mechanisms in Pseudomonas aeruginosa: alterations of porin OprD and efflux proteins do not fully explain resistance patterns observed in clinical isolates. APMIS 113:187–196 Zanetti G, Bally F, Greub G, Garbino J, Kinge T, Lew D, Romand JA, Bille J, Aymon D, Stratchounski L, Krawczyk L, Rubinstein E, Schaller MD, Chiolero R, Glauser MP, Cometta A (2003) Cefepime versus Imipenem-cilastatin for treatment of nosocomial pneumonia in intensive care unit patients: a multicenter, evaluator-blind, prospective, randomized study. Antimicrob Agents Chemother 47:3442–3447 Sanbongi Y, Shimizu A, Suzuki T, Nagaso H, Ida T, Maebashi K, Gotoh N (2009) Classification of OprD sequence and correlation with antimicrobial activity of carbapenem agents in Pseudomonas aeruginosa clinical isolates collected in Japan. Microbiol Immunol 53:361–367 Fukuda H, Hosaka M, Iyobe S, Gotoh N, Nishino T, Hirai K (1995) nfxC-type quinolone resistance in a clinical isolate of Pseudomonas aeruginosa. Antimicrob Agents Chemother 39:790–792 Kohler T, Michea-Hamzehpour M, Henze U, Gotoh N, Curty LK, Pechere JC (1997) Characterization of MexE-MexF-OprN, a positively regulated multidrug efflux system of Pseudomonas aeruginosa. Mol Microbiol 23:345–354 Shanks RM, Caiazza NC, Hinsa SM, Toutain CM, O’Toole GA (2006) Saccharomyces cerevisiae-based molecular tool kit for manipulation of genes from gram-negative bacteria. Appl Environ Microbiol 72:5027–5036 CLSI (2013) Performance Standards for Antimicrobial Susceptibility Testing; Twenty-Third Informational Supplement. Clinical and Laboratory Standards Institute, Wayne, CLSI document M100-S23 Andrews JM (2001) Determination of minimum inhibitory concentrations. J Antimicrob Chemother 48(Suppl 1):5–16 Wiegand I, Hilpert K, Hancock RE (2008) Agar and broth dilution methods to determine the minimal inhibitory concentration (MIC) of antimicrobial substances. Nat Protoc 3:163–175 O'Toole GA, Pratt LA, Watnick PI, Newman DK, Weaver VB, Kolter R (1999) Genetic approaches to the study of biofilms. In: Doyle RJ (ed) Methods in Enzymology. Academic Press, San Diego, pp 91–109 Caetano-Annoles G (1993) Amplifying DNA with arbitrary oligonucleotide primers. PCR Methods Appl 3:85–92 O'Toole GA, Kolter R (1998) Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis. Mol Microbiol 28:449–461 Whitchurch CB, Hobbs M, Livingston SP, Krishnapillai V, Mattick JS (1990) Characterization of a Pseudomonas aeruginosa twitching motility gene and evidence for a specialized protein export system widespread in eubacteria. Gene 101:33–44 O'Toole GA, Kolter R (1998) Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol Microbiol 30:295–304 Caiazza NC, O'Toole GA (2004) SadB is required for the transition from reversible to irreversible attachment during biofilm formation by Pseudomonas aeruginosa PA14. J Bacteriol 186:4476–4485 Honko AN, Sriranganathan N, Lees CJ, Mizel SB (2006) Flagellin is an effective adjuvant for immunization against lethal respiratory challenge with Yersinia pestis. Infect Immun 74:1113–1120 Digiandomenico A, Warrener P, Hamilton M, Guillard S, Ravn P, Minter R, Camara MM, Venkatraman V, Macgill RS, Lin J, Wang Q, Keller AE, Bonnell JC, Tomich M, Jermutus L, McCarthy MP, Melnick DA, Suzich JA, Stover CK (2012) Identification of broadly protective human antibodies to Pseudomonas aeruginosa exopolysaccharide Psl by phenotypic screening. J Expl Med 209:1273–1287 Trias J, Nikaido H (1990) Protein D2 channel of the Pseudomonas aeruginosa outer membrane has a binding site for basic amino acids and peptides. J Biol Chem 265:15680–15684 Trias J, Nikaido H (1990) Outer membrane protein D2 catalyzes facilitated diffusion of carbapenems and penems through the outer membrane of Pseudomonas aeruginosa. Antimicrob Agents Chemother 34:52–57 Mah TF, O'Toole GA (2001) Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol 9:34–39 Friedman L, Kolter R (2004) Genes involved in matrix formation in Pseudomonas aeruginosa PA14 biofilms. Mol Microbiol 51:675–690 Kuchma SL, Griffin EF, O'Toole GA (2012) Minor pilins of the type IV pilus system participate in the negative regulation of swarming motility. J Bacteriol 194:5388–5403 Zegans ME, Wozniak D, Griffin E, Toutain-Kidd CM, Hammond JH, Garfoot A, Lam JS (2012) Pseudomonas aeruginosa exopolysaccharide Psl promotes resistance to the biofilm inhibitor polysorbate 80. Antimicrob Agents Chemother 56:4112–4122 Li Y, Hao G, Galvani CD, Meng Y, De La Fuente L, Hoch HC, Burr TJ (2007) Type I and type IV pili of Xylella fastidiosa affect twitching motility, biofilm formation and cell-cell aggregation. Microbiology 153:719–726 Kuchma SL, Ballok AE, Merritt JH, Hammond JH, Lu W, Rabinowitz JD, O'Toole GA (2010) Cyclic-di-GMP-mediated repression of swarming motility by Pseudomonas aeruginosa: the pilY1 gene and its impact on surface-associated behaviors. J Bacteriol 192:2950–2964 Goldberg JB, Hatano K, Pier GB (1993) Synthesis of lipopolysaccharide O side chains by Pseudomonas aeruginosa PAO1 requires the enzyme phosphomannomutase. J Bacteriol 175:1605–1611 Olvera C, Goldberg JB, Sanchez R, Soberon-Chavez G (1999) The Pseudomonas aeruginosa algC gene product participates in rhamnolipid biosynthesis. FEMS Microbiol Lett 179:85–90 Friedman L, Kolter R (2004) Two genetic loci produce distinct carbohydrate-rich structural components of the Pseudomonas aeruginosa biofilm matrix. J Bacteriol 186:4457–4465 Davies DG, Geesey GG (1995) Regulation of the alginate biosynthesis gene algC in Pseudomonas aeruginosa during biofilm development in continuous culture. Appl Environ Microbiol 61:860–867 Davies DG, Chakabarty AM, Geesey GG (1993) Exopolysaccharide production in biofilms: substratum activation of alginate gene expression by Pseudomonas aeruginosa. Appl Environ Microbiol 59:1181–1186 Jackson KD, Starkey M, Kremer S, Parsek MR, Wozniak DJ (2004) Identification of psl, a locus encoding a potential exopolysaccharide that Is essential for Pseudomonas aeruginosa PAO1 biofilm formation. J Bacteriol 186:4466–4475 Matsukawa M, Greenberg EP (2004) Putative exopolysaccharide synthesis genes influence Pseudomonas aeruginosa biofilm development. J Bacteriol 186:4449–4456 Costerton JW, Stewart PS, Greenberg EP (1999) Bacterial biofilms: a common cause of persistent infections. Science 284:1318–1322 Hoiby N, Bjarnsholt T, Givskov M, Molin S, Ciofu O (2010) Antibiotic resistance of bacterial biofilms. Int J Antimicrob Agents 35:322–332 Alm RA, Bodero AJ, Free PD, Mattick JS (1996) Identification of a novel gene, pilZ, essential for type 4 fimbrial biogenesis in Pseudomonas aeruginosa. J Bacteriol 178:46–53 Alm RA, Hallinan JP, Watson AA, Mattick JS (1996) Fimbrial biogenesis genes of Pseudomonas aeruginosa: pilW and pilX increase the similarity of type 4 fimbriae to the GSP protein-secretion systems and pilY1 encodes a gonococcal PilC homologue. Mol Microbiol 22:161–173 Bohn YS, Brandes G, Rakhimova E, Horatzek S, Salunkhe P, Munder A, van Barneveld A, Jordan D, Bredenbruch F, Haussler S, Riedel K, Eberl L, Jensen PO, Bjarnsholt T, Moser C, Hoiby N, Tummler B, Wiehlmann L (2009) Multiple roles of Pseudomonas aeruginosa TBCF10839 PilY1 in motility, transport and infection. Mol Microbiol 71:730–747 Giltner CL, Habash M, Burrows LL (2010) Pseudomonas aeruginosa minor pilins are incorporated into type IV pili. J Mol Biol 398:444–461 Dheepa M, Rashme VL, Appalaraju B (2011) Comparision of biofilm production and multiple drug resistance in clinical isolates of Acinetobacter baumanii from a tertiary care hospital in South India. Int J Pharm Biomed Sci 2:103–107 Rao RS, Karthika RU, Singh SP, Shashikala P, Kanungo R, Jayachandran S, Prashanth K (2008) Correlation between biofilm production and multiple drug resistance in imipenem resistant clinical isolates of Acinetobacter baumannii. Indian Journal Med Microbiol 26:333–337 Ibrahim NH, Somily AM, Bassyouni RH, El-Aabedien AZ (2012) Comparative study assessing the effect of tigecycline and moxifloxacin in prevention of Acinetobacter baumannii biofilm. Life Sci 9:1016–1024 Jacobs MA, Alwood A, Thaipisuttikul I, Spencer D, Haugen E, Ernst S, Will O, Kaul R, Raymond C, Levy R, Chun-Rong L, Guenthner D, Bovee D, Olson MV, Manoil C (2003) Comprehensive transposon mutant library of Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 100:14339–14344 Simon R, Priefer U, Pühler A (1983) A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in gram negative bacteria. Nat Biotechnol 1:784–791 Kulasekara HD, Ventre I, Kulasekara BR, Lazdunski A, Filloux A, Lory S (2005) A novel two-component system controls the expression of Pseudomonas aeruginosa fimbrial cup genes. Mol Microbiol 55:368–380