Cyclic-di-GMP levels affect Pseudomonas aeruginosa fitness in the presence of imipenem

Environmental Microbiology

Volumn 16, Issue 5, 2014, Pages 1321-1333

  Nicastro, Gianlucca G ^a   Kaihami, Gilberto H ^a   Pereira, Thays O ^a   Meireles, Diogo A ^a   Groleau, Marie Christine ^b   Déziel, Eric ^b   Baldini, Regina L ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b INRS INSTITUT ARMAND FRAPPIER   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA (MICROORGANISMS); PSEUDOMONAS AERUGINOSA;

ANTIINFECTIVE AGENT; BETA LACTAMASE; BIS(3',5')-CYCLIC DIGUANYLIC ACID; CYCLIC GMP; IMIPENEM; OPRD PROTEIN, PSEUDOMONAS AERUGINOSA; PORIN; BACTERIAL PROTEIN; BIS(3',5') CYCLIC DIGUANYLIC ACID; DRUG DERIVATIVE;

ANALOGS AND DERIVATIVES; BIOFILM; DRUG EFFECTS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOLECULAR GENETICS; PLANKTON; PSEUDOMONAS AERUGINOSA; REPRODUCTIVE FITNESS; ADAPTATION; ARTICLE; DRUG EFFECT;

ANTI-BACTERIAL AGENTS; BETA-LACTAMASES; BIOFILMS; CYCLIC GMP; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; GENETIC FITNESS; IMIPENEM; MOLECULAR SEQUENCE ANNOTATION; PLANKTON; PORINS; PSEUDOMONAS AERUGINOSA; ADAPTATION, BIOLOGICAL; BACTERIAL PROTEINS;

EID: 84898776343     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/1462-2920.12422     Document Type: Article

References (55)

1. Blanka, A., Schulz, S., Eckweiler, D., Franke, R., Bielecka, A., Nicolai, T., etal. (2014) Identification of the alternative sigma factor SigX regulon and its implications for Pseudomonas aeruginosa pathogenicity. J Bacteriol 196: 345-356.
2. Boyd, C.D., and O'Toole, G.A. (2012) Second messenger regulation of biofilm formation: breakthroughs in understanding c-di-GMP effector systems. Annu Rev Cell Dev Biol 28: 439-462.
3. Breidenstein, E.B., de la Fuente-Nunez, C., and Hancock, R.E. (2011) Pseudomonas aeruginosa: all roads lead to resistance. Trends Microbiol 19: 419-426.
4. Carmeli, Y., Troillet, N., Eliopoulos, G.M., and Samore, M.H. (1999) Emergence of antibiotic-resistant Pseudomonas aeruginosa: comparison of risks associated with different antipseudomonal agents. Antimicrob Agents Chemother 43: 1379-1382.
5. Choi, K.H., and Schweizer, H.P. (2006) mini-Tn7 insertion in bacteria with single attTn7 sites: example Pseudomonas aeruginosa. Nat Protoc 1: 153-161.
6. Choi, K.H., Gaynor, J.B., White, K.G., Lopez, C., Bosio, C.M., Karkhoff-Schweizer, R.R., and Schweizer, H.P. (2005) A Tn7-based broad-range bacterial cloning and expression system. Nat Methods 2: 443-448.
7. Choi, K.H., Kumar, A., and Schweizer, H.P. (2006) A 10-min method for preparation of highly electrocompetent Pseudomonas aeruginosa cells: application for DNA fragment transfer between chromosomes and plasmid transformation. J Microbiol Methods 64: 391-397.
8. Chua, S.L., Tan, S.Y., Rybtke, M.T., Chen, Y., Rice, S.A., Kjelleberg, S., etal. (2013) Bis-(3′-5′)-cyclic dimeric GMP regulates antimicrobial peptide resistance in Pseudomonas aeruginosa. Antimicrob Agents Chemother 57: 2066-2075.
9. Costerton, J.W., Lewandowski, Z., Caldwell, D.E., Korber, D.R., and Lappin-Scott, H.M. (1995) Microbial biofilms. Annu Rev Microbiol 49: 711-745.
10. Costerton, J.W., Stewart, P.S., and Greenberg, E.P. (1999) Bacterial biofilms: a common cause of persistent infections. Science 284: 1318-1322.
11. Drenkard, E. (2003) Antimicrobial resistance of Pseudomonas aeruginosa biofilms. Microbes Infect 5: 1213-1219.
12. Drenkard, E., and Ausubel, F.M. (2002) Pseudomonas biofilm formation and antibiotic resistance are linked to phenotypic variation. Nature 416: 740-743.
13. Fernandez, L., Breidenstein, E.B., Song, D., and Hancock, R.E. (2012) Role of intracellular proteases in the antibiotic resistance, motility, and biofilm formation of Pseudomonas aeruginosa. Antimicrob Agents Chemother 56: 1128-1132.
14. Gicquel, G., Bouffartigues, E., Bains, M., Oxaran, V., Rosay, T., Lesouhaitier, O., etal. (2013) The extra-cytoplasmic function sigma factor sigX modulates biofilm and virulence-related properties in Pseudomonas aeruginosa. PLoS ONE 8: e80407.
15. Govan, J.R., and Deretic, V. (1996) Microbial pathogenesis in cystic fibrosis: mucoid Pseudomonas aeruginosa and Burkholderia cepacia. Microbiol Rev 60: 539-574.
16. Hancock, R.E. (1997) The bacterial outer membrane as a drug barrier. Trends Microbiol 5: 37-42.
17. Hancock, R.E., and Brinkman, F.S. (2002) Function of Pseudomonas porins in uptake and efflux. Annu Rev Microbiol 56: 17-38.
18. Harmsen, M., Yang, L., Pamp, S.J., and Tolker-Nielsen, T. (2010) An update on Pseudomonas aeruginosa biofilm formation, tolerance, and dispersal. FEMS Immunol Med Microbiol 59: 253-268.
19. Hellman, U., Wernstedt, C., Gonez, J., and Heldin, C.H. (1995) Improvement of an 'In-Gel' digestion procedure for the micropreparation of internal protein fragments for amino acid sequencing. Anal Biochem 224: 451-455.
20. Hengge, R. (2009) Principles of c-di-GMP signalling in bacteria. Nat Rev Micro 7: 263-273.
21. Hengge, R. (2010) Cyclic-di-GMP reaches out into the bacterial RNA world. Sci Signal 3: pe44.
22. Hinz, A., Lee, S., Jacoby, K., and Manoil, C. (2011) Membrane proteases and aminoglycoside antibiotic resistance. J Bacteriol 193: 4790-4797.
23. Hoang, T.T., Karkhoff-Schweizer, R.R., Kutchma, A.J., and Schweizer, H.P. (1998) A broad-host-range Flp-FRT recombination system for site-specific excision of chromosomally-located DNA sequences: application for isolation of unmarked Pseudomonas aeruginosa mutants. Gene 212: 77-86.
24. Hoang, T.T., Kutchma, A.J., Becher, A., and Schweizer, H.P. (2000) Integration-proficient plasmids for Pseudomonas aeruginosa: site-specific integration and use for engineering of reporter and expression strains. Plasmid 43: 59-72.
25. Hoffman, L.R., D'Argenio, D.A., MacCoss, M.J., Zhang, Z., Jones, R.A., and Miller, S.I. (2005) Aminoglycoside antibiotics induce bacterial biofilm formation. Nature 436: 1171-1175.
26. Hoiby, N., Bjarnsholt, T., Givskov, M., Molin, S., and Ciofu, O. (2010) Antibiotic resistance of bacterial biofilms. Int J Antimicrob Agents 35: 322-332.
27. Jimenez, P.N., Koch, G., Thompson, J.A., Xavier, K.B., Cool, R.H., and Quax, W.J. (2012) The multiple signaling systems regulating virulence in Pseudomonas aeruginosa. Microbiol Mol Biol Rev: MMBR 76: 46-65.
28. Kohler, T., Michea-Hamzehpour, M., Epp, S.F., and Pechere, J.C. (1999) Carbapenem activities against Pseudomonas aeruginosa: respective contributions of OprD and efflux systems. Antimicrob Agents Chemother 43: 424-427.
29. Kulasakara, H., Lee, V., Brencic, A., Liberati, N., Urbach, J., Miyata, S., etal. (2006) Analysis of Pseudomonas aeruginosa diguanylate cyclases and phosphodiesterases reveals a role for bis-(3′-5′)-cyclic-GMP in virulence. Proc Natl Acad Sci U S A 103: 2839-2844.
30. Kumagai, Y., Matsuo, J., Cheng, Z., Hayakawa, Y., and Rikihisa, Y. (2011) Cyclic dimeric GMP signaling regulates intracellular aggregation, sessility, and growth of Ehrlichia chaffeensis. Infect Immun 79: 3905-3912.
31. Lai, S., Tremblay, J., and Deziel, E. (2009) Swarming motility: a multicellular behaviour conferring antimicrobial resistance. Environ Microbiol 11: 126-136.
32. Lautenbach, E., Synnestvedt, M., Weiner, M.G., Bilker, W.B., Vo, L., Schein, J., and Kim, M. (2010) Imipenem resistance in Pseudomonas aeruginosa: emergence, epidemiology, and impact on clinical and economic outcomes. Infect Control Hosp Epidemiol 31: 47-53.
33. Lee, D.G., Urbach, J.M., Wu, G., Liberati, N.T., Feinbaum, R.L., Miyata, S., etal. (2006) Genomic analysis reveals that Pseudomonas aeruginosa virulence is combinatorial. Genome Biol 7: R90.
34. Lequette, Y., Lee, J.H., Ledgham, F., Lazdunski, A., and Greenberg, E.P. (2006) A distinct QscR regulon in the Pseudomonas aeruginosa quorum-sensing circuit. J Bacteriol 188: 3365-3370.
35. Liberati, N.T., Urbach, J.M., Miyata, S., Lee, D.G., Drenkard, E., Wu, G., etal. (2006) An ordered, nonredundant library of Pseudomonas aeruginosa strain PA14 transposon insertion mutants. Proc Natl Acad Sci U S A 103: 2833-2838.
36. ΔΔCt Method. Methods 25: 402-408.
37. Lyczak, J.B., Cannon, C.L., and Pier, G.B. (2000) Establishment of Pseudomonas aeruginosa infection: lessons from a versatile opportunist. Microbes Infect 2: 1051-1060.
38. Mah, T.F., and O'Toole, G.A. (2001) Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol 9: 34-39.
39. Masuda, N., Sakagawa, E., and Ohya, S. (1995) Outer membrane proteins responsible for multiple drug resistance in Pseudomonas aeruginosa. Antimicrob Agents Chemother 39: 645-649.
40. Meireles, D.A. (2011) Estudo da função do gene kerV de Pseudomonas aeruginosa. PhD Thesis. São Paulo: Instituto de Química, Universidade de São Paulo, pp. 1-187. [WWW document]. URL http://www.teses.usp.br/teses/disponiveis/46/46131/tde-05122011-150318/
41. Miliani, K., L'Heriteau, F., Lacave, L., Carbonne, A., and Astagneau, P. (2011) Imipenem and ciprofloxacin consumption as factors associated with high incidence rates of resistant Pseudomonas aeruginosa in hospitals in northern France. J Hosp Infect 77: 343-347.
42. Navarro, M.V., Newell, P.D., Krasteva, P.V., Chatterjee, D., Madden, D.R., O'Toole, G.A., and Sondermann, H. (2011) Structural basis for c-di-GMP-mediated inside-out signaling controlling periplasmic proteolysis. PLoS Biol 9: e1000588.
43. Newman, J.R., and Fuqua, C. (1999) Broad-host-range expression vectors that carry the L-arabinose-inducible Escherichia coli araBAD promoter and the araC regulator. Gene 227: 197-203.
44. Ochs, M.M., McCusker, M.P., Bains, M., and Hancock, R.E. (1999) Negative regulation of the Pseudomonas aeruginosa outer membrane porin OprD selective for imipenem and basic amino acids. Antimicrob Agents Chemother 43: 1085-1090.
45. O'Toole, G.A., Pratt, L.A., Watnick, P.I., Newman, D.K., Weaver, V.B., and Kolter, R. (1999) Genetic approaches to study of biofilms. Methods Enzymol 310: 91-109.
46. Rahme, L.G., Stevens, E.J., Wolfort, S.F., Shao, J., Tompkins, R.G., and Ausubel, F.M. (1995) Common virulence factors for bacterial pathogenicity in plants and animals. Science 268: 1899-1902.
47. Romling, U., Galperin, M.Y., and Gomelsky, M. (2013) Cyclic di-GMP: the first 25 years of a universal bacterial second messenger. Microbiol Mol Biol Rev 77: 1-52.
48. dos Santos, V.T., Bisson-Filho, A.W., and Gueiros-Filho, F.J. (2012) DivIVA-mediated polar localization of ComN, a posttranscriptional regulator of Bacillus subtilis. J Bacteriol 194: 3661-3669.
49. Simm, R., Morr, M., Kader, A., Nimtz, M., and Romling, U. (2004) GGDEF and EAL domains inversely regulate cyclic di-GMP levels and transition from sessility to motility. Mol Microbiol 53: 1123-1134.
50. de Souza, A.A., Ionescu, M., Baccari, C., da Silva, A.M., and Lindow, S.E. (2013) Phenotype overlap in Xylella fastidiosa is controlled by the cyclic di-GMP phosphodiesterase Eal in response to antibiotic exposure and diffusible signal factor-mediated cell-cell signaling. Appl Environ Microbiol 79: 3444-3454.
51. Spangler, C., Bohm, A., Jenal, U., Seifert, R., and Kaever, V. (2010) A liquid chromatography-coupled tandem mass spectrometry method for quantitation of cyclic di-guanosine monophosphate. J Microbiol Methods 81: 226-231.
52. Torres, A. (2006) The new American Thoracic Society/Infectious Disease Society of North America guidelines for the management of hospital-acquired, ventilator-associated and healthcare-associated pneumonia: a current view and new complementary information. Curr Opin Crit Care 12: 444-445.
53. Tremblay, J., and Déziel, E. (2008) Improving the reproducibility of Pseudomonas aeruginosa swarming motility assays. J Basic Microb 48: 509-515.
54. Ueda, A., and Wood, T.K. (2009) Connecting quorum sensing, c-di-GMP, pel polysaccharide, and biofilm formation in Pseudomonas aeruginosa through tyrosine phosphatase TpbA (PA3885). PLoS Pathog 5: e1000483.
55. Wiegand, I., Hilpert, K., and Hancock, R.E. (2008) Agar and broth dilution methods to determine the minimal inhibitory concentration (MIC) of antimicrobial substances. Nat Protoc 3: 163-175.