Clearance of pseudomonas aeruginosa foreign-body biofilm infections through reduction of the cyclic di-gmp level in the bacteria

Infection and Immunity

Volumn 81, Issue 8, 2013, Pages 2705-2713

  Christensen, Louise D ^a   Gennip, Maria van ^a   Rybtke, Morten T ^a   Wu, Hong ^a,d   Chiang, Wen Chi ^a   Alhede, Morten ^a   Høiby, Niels ^a,b   Nielsen, Thomas E ^c,d   Givskov, Michael ^a,d   Tolker Nielsena, Tim ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b Rigshospitalet   (Denmark)

^c TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^d NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CYCLIC GMP; PHOSPHODIESTERASE; UNCLASSIFIED DRUG; YHJH PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL CLEARANCE; BACTERIAL STRAIN; BIOFILM; CONTROLLED STUDY; ESCHERICHIA COLI; FEMALE; FOREIGN BODY; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PERITONEAL CAVITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTION; SILICONE PROSTHESIS;

3',5'-CYCLIC-GMP PHOSPHODIESTERASES; ANIMALS; BIOFILMS; CYCLIC GMP; DISEASE MODELS, ANIMAL; ESCHERICHIA COLI PROTEINS; FEMALE; MICE; MICE, INBRED BALB C; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS;

EID: 84880687995     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00332-13     Document Type: Article

References (58)

1. Costerton JW, Stewart PS, Greenberg EP. 1999. Bacterial biofilms: a common cause of persistent infections. Science 284: 1318-1322.
2. Hentzer M, Wu H, Andersen JB, Riedel K, Rasmussen TB, Bagge N, Kumar N, Schembri MA, Song Z, Kristoffersen P, Manefield M, Coste-rton JW, Molin S, Eberl L, Steinberg P, Kjelleberg S, Hoiby N, Givskov M. 2003. Attenuation of Pseudomonas aeruginosa virulence by quorum sensing inhibitors. EMBO J. 22: 3803-3815.
3. Bjarnsholt T, Jensen PO, Burmolle M, Hentzer M, Haagensen JA, Hougen HP, Calum H, Madsen KG, Moser C, Molin S, Hoiby N, Givskov M. 2005. Pseudomonas aeruginosa tolerance to tobramycin, hydrogen peroxide and polymorphonuclear leukocytes is quorum-sensing dependent. Microbiology 151: 373-383.
4. Costerton JW, Lewandowski Z, Caldwell DE, Korber DR, Lappin-Scott HM. 1995. Microbial biofilms. Annu. Rev. Microbiol. 49: 711-745.
5. Koch C, Hoiby N. 1993. Pathogenesis of cystic fibrosis. Lancet 341: 1065-1069.
6. Gristina AG, Dobbins JJ, Giammara B, Lewis JC, DeVries WC. 1988. Biomaterial-centered sepsis and the total artificial heart: microbial adhesion versus tissue integration. JAMA 259: 870-874.
7. von EiffC, Jansen B, Kohnen W, Becker K. 2005. Infections associated with medical devices: pathogenesis, management, and prophylaxis. Drugs 65: 179-214.
8. Kirketerp-Moller K, Jensen PO, Fazli M, Madsen KG, Pedersen J, Moser C, Tolker-Nielsen T, Hoiby N, Givskov M, Bjarnsholt T. 2008. Distribution, organization, and ecology of bacteria in chronic wounds. J. Clin. Microbiol. 46: 2717-2722.
9. National Institutes of Health. 1997. Minutes of the National Advisory Dental and Craniofacial Research Council, 153rd meeting. National Institute of Dental and Craniofacial Research, Bethesda, MD.
10. Bjarnsholt T, Jensen PO, Rasmussen TB, Christophersen L, Calum H, Hentzer M, Hougen HP, Rygaard J, Moser C, Eberl L, Hoiby N, Givskov M. 2005. Garlic blocks quorum sensing and promotes rapid clearing of pulmonary Pseudomonas aeruginosa infections. Microbiology 151: 3873-3880.
11. Christensen LD, Moser C, Jensen PO, Rasmussen TB, Christophersen L, Kjelleberg S, Kumar N, Hoiby N, Givskov M, Bjarnsholt T. 2007. Impact ofPseudomonas aeruginosa quorum sensing onbiofilm persistence in an in vivo intraperitoneal foreign-body infection model. Microbiology 153: 2312-2320.
12. Christensen LD, van Gennip M, Jakobsen TH, Alhede M, Hougen HP, Hoiby N, Bjarnsholt T, Givskov M. 2012. Synergistic antibacterial efficacy of early combination treatment with tobramycin and quorum-sensing inhibitors against Pseudomonas aeruginosa in an intraperitoneal foreign-body infection mouse model. J. Antimicrob. Chemother. 67: 1198-1206.
13. Jakobsen TH, Bragason SK, Phipps RK, Christensen LD, van Gennip M, Alhede M, Skindersoe M, Larsen TO, Hoiby N, Bjarnsholt T, Givskov M. 2012. Food as a source for quorum sensing inhibitors: iberin from horseradish revealed as a quorum sensing inhibitor of Pseudomonas aeruginosa. Appl. Environ. Microbiol. 78: 2410-2421.
14. Jakobsen TH, van Gennip M, Phipps RK, Shanmugham MS, Chris-tensen LD, Alhede M, Skindersoe ME, Rasmussen TB, Friedrich K, Uthe F, Jensen PO, Moser C, Nielsen KF, Eberl L, Larsen TO, Tanner D, Hoiby N, Bjarnsholt T, Givskov M. 2012. Ajoene, a sulfur-rich molecule from garlic, inhibits genes controlled by quorum sensing. Anti-microb. Agents Chemother. 56: 2314-2325.
15. Rybtke MT, Jensen PO, Hoiby N, Givskov M, Tolker-Nielsen T, Bjarn-sholt T. 2011. The implication of Pseudomonas aeruginosa biofilms in infections. Inflamm. Allergy Drug Targets 10: 141-157.
16. Harmsen M, Yang L, Pamp SJ, Tolker-Nielsen T. 2010. An update on Pseudomonas aeruginosa biofilm formation, tolerance, and dispersal. FEMS Immunol. Med. Microbiol. 59: 253-268.
17. Jensen PO, Bjarnsholt T, Phipps R, Rasmussen TB, Calum H, Christ-offersen L, Moser C, Williams P, Pressler T, Givskov M, Hoiby N. 2007. Rapid necrotic killing of polymorphonuclear leukocytes is caused by quo-rum-sensing-controlled production of rhamnolipid by Pseudomonas aeruginosa. Microbiology 153: 1329-1338.
18. Alhede M, Bjarnsholt T, Jensen PO, Phipps RK, Moser C, Chris-tophersen L, Christensen LD, van Gennip M, Parsek M, Hoiby N, Rasmussen TB, Givskov M. 2009. Pseudomonas aeruginosa recognizes and responds aggressively to the presence of polymorphonuclear leukocytes. Microbiology 155: 3500-3508.
19. Allison DG, Evans DJ, Brown MR, Gilbert P. 1990. Possible involvement of the division cycle in dispersal of Escherichia coli from biofilms. J. Bacte-riol. 172: 1667-1669.
20. Sauer K, Camper AK, Ehrlich GD, Costerton JW, Davies DG. 2002. Pseudomonas aeruginosa displays multiple phenotypes during development as a biofilm. J. Bacteriol. 184: 1140-1154.
21. Sauer K, Cullen MC, Rickard AH, Zeef LA, Davies DG, Gilbert P. 2004. Characterization of nutrient-induced dispersion in Pseudomonas aerugi-nosa PAO1 biofilm. J. Bacteriol. 186: 7312-7326.
22. Gjermansen M, Ragas P, Sternberg C, Molin S, Tolker-Nielsen T. 2005. Characterization of starvation-induced dispersion in Pseudomonas putida biofilms. Environ. Microbiol. 7: 894-906.
23. Schleheck D, Barraud N, Klebensberger J, Webb JS, McDougald D, Rice SA, Kjelleberg S. 2009. Pseudomonas aeruginosa PAO1 preferentially growsasaggregates in liquid batch cultures and disperses upon starvation. PLoS One 4: e5513. doi :10.1371/journal.pone.0005513.
24. Gjermansen M, Ragas P, Tolker-Nielsen T. 2006. Proteins with GGDEF and EAL domains regulate Pseudomonas putida biofilm formation and dispersal. FEMS Microbiol. Lett. 265: 215-224.
25. Barraud N, Hassett DJ, Hwang SH, Rice SA, Kjelleberg S, Webb JS. 2006. Involvement of nitric oxide in biofilm dispersal of Pseudomonas aeruginosa. J. Bacteriol. 188: 7344-7353.
26. Barraud N, Schleheck D, Klebensberger J, Webb JS, Hassett DJ, Rice SA, Kjelleberg S. 2009. Nitric oxide signaling in Pseudomonas aeruginosa biofilms mediates phosphodiesterase activity, decreased cyclic di-GMP levels, and enhanced dispersal. J. Bacteriol. 191: 7333-7342.
27. Simm R, Morr M, Kader A, Nimtz M, Romling U. 2004. GGDEF and EAL domains inversely regulate cyclic di-GMP levels and transition from sessility to motility. Mol. Microbiol. 53: 1123-1134.
28. Hickman JW, Tifrea DF, Harwood CS. 2005. A chemosensory system that regulates biofilm formation through modulationofcyclic diguanylate levels. Proc. Natl. Acad. Sci. U. S. A. 102: 14422-14427.
29. Fazli M, O'Connell A, Nilsson M, Niehaus K, Dow JM, Givskov M, Ryan RP, Tolker-Nielsen T. 2011. The CRP/FNR family protein Bcam1349 is a c-di-GMP effector that regulates biofilm formation in the respiratory pathogen Burkholderia cenocepacia. Mol. Microbiol. 82: 327-341.
30. Goymer P, Kahn SG, Malone JG, Gehrig SM, Spiers AJ, Rainey PB. 2006. Adaptive divergence in experimental populations of Pseudomonas fluorescens. II. Role of the GGDEF regulator WspR in evolution and development of the wrinkly spreader phenotype. Genetics 173: 515-526.
31. Kulasakara H, Lee V, Brencic A, Liberati N, Urbach J, Miyata S, Lee DG, Neely AN, Hyodo M, Hayakawa Y, Ausubel FM, Lory S. 2006. Analysis of Pseudomonas aeruginosa diguanylate cyclases and phospho-diesterases reveals a role for bis-(3=-5=)-cyclic-GMP in virulence. Proc. Natl. Acad. Sci. U. S. A. 103: 2839-2844.
32. Lim B, Beyhan S, Meir J, Yildiz FH. 2006. Cyclic-diGMP signal trans-duction systems in Vibrio cholerae: modulation of rugosity and biofilm formation. Mol. Microbiol. 60: 331-348.
33. Ryan RP, Lucey J, O'Donovan K, McCarthy Y, Yang L, Tolker-Nielsen T, Dow JM. 2009. HD-GYP domain proteins regulate biofilm formation and virulence in Pseudomonas aeruginosa. Environ. Microbiol. 11: 1126-1136.
34. Rybtke MT, Borlee BR, Murakami K, Irie Y, Hentzer M, Nielsen TE, Givskov M, Parsek MR, Tolker-Nielsen T. 2012. Fluorescence-based reporter for gauging cyclic di-GMP levels in Pseudomonas aeruginosa. Appl. Environ. Microbiol. 78: 5060-5069.
35. Clark DJ, Maaløe O. 1967. DNA replication and the division cycle in Escherichia coli. J. Mol. Biol. 23: 99-112.
36. Klausen M, Heydorn A, Ragas P, Lambertsen L, Aaes-Jorgensen A, Molin S, Tolker-Nielsen T. 2003. Biofilm formation by Pseudomonas aeruginosa wild type, flagella, and type IV pilus mutants. Mol. Microbiol. 48: 1511-1524.
37. Newman JR, 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.
38. West SE, Schweizer HP, Dall C, Sample AK, Runyen-Janecky LJ. 1994. Construction of improved Escherichia-Pseudomonas shuttle vectors derived from pUC18/19 and sequence of the region required for their replication in Pseudomonas aeruginosa. Gene 148: 81-86.
39. O'Toole GA, Kolter R. 1998. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol. Microbiol. 30: 295-304.
40. Hoiby N. 1974. Pseudomonas aeruginosa infection in cystic fibrosis: relationship between mucoid strains of Pseudomonas aeruginosa and the humoral immune response. Acta Pathol. Microbiol. Scand. B Microbiol. Immunol. 82: 551-558.
41. Crusz SA, Popat R, Rybtke MT, Camara M, Givskov M, Tolker-Nielsen T, Diggle SP, Williams P. 2012. Bursting the bubble on bacterial biofilms: a flow cell methodology. Biofouling 28: 835-842.
42. Pamp SJ, Tolker-Nielsen T. 2007. Multiple roles of biosurfactants in structural biofilm development by Pseudomonas aeruginosa. J. Bacteriol. 189: 2531-2539.
43. Thormann KM, Duttler S, Saville RM, Hyodo M, Shukla S, Hayakawa Y, Spormann AM. 2006. Control of formation and cellular detachment from Shewanella oneidensis MR-1 biofilms by cyclic di-GMP. J. Bacteriol. 188: 2681-2691.
44. Rainey PB, Travisano M. 1998. Adaptive radiation in a heterogeneous environment. Nature 394: 69-72.
45. Spiers AJ, Kahn SG, Bohannon J, Travisano M, Rainey PB. 2002. Adaptive divergence in experimental populations of Pseudomonas fluore-scens. I. Genetic and phenotypic basesof wrinkly spreader fitness. Genetics 161: 33-46.
46. 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.
47. Friedman L, Kolter R. 2004. Genes involved in matrix formation in Pseudomonas aeruginosa PA14 biofilms. Mol. Microbiol. 51: 675-690.
48. Branda SS, Vik S, Friedman L, Kolter R. 2005. Biofilms: the matrix revisited. Trends Microbiol. 13: 20-26.
49. D'Argenio DA, Calfee MW, Rainey PB, Pesci EC. 2002. Autolysis and autoaggregation in Pseudomonas aeruginosa colony morphology mutants. J. Bacteriol. 184: 6481-6489.
50. Gjermansen M, Nilsson M, Yang L, Tolker-Nielsen T. 2010. Characterization of starvation-induced dispersion in Pseudomonas putida biofilms: genetic elements and molecular mechanisms. Mol. Microbiol. 75: 815-826.
51. Sintim HO, Smith JA, Wang J, Nakayama S, Yan L. 2010. Paradigm shift in discovering next-generation anti-infective agents: targeting quorum sensing, c-di-GMP signaling and biofilm formation in bacteria with small molecules. Future Med. Chem. 2: 1005-1035.
52. Nilsson M, Chiang WC, Fazli M, Gjermansen M, Givskov M, Tolker-Nielsen T. 2011. Influence of putative exopolysaccharide genes on Pseu-domonas putida KT2440 biofilm stability. Environ. Microbiol. 13: 1357-1369.
53. Matsukawa M, Greenberg EP. 2004. Putative exopolysaccharide synthesis genes influence Pseudomonas aeruginosa biofilm development. J. Bac-teriol. 186: 4449-4456.
54. 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. Bacte-riol. 186: 4466-4475.
55. Hickman JW, Harwood CS. 2008. Identification of FleQ from Pseudomo-nas aeruginosa as a c-di-GMP-responsive transcription factor. Mol. Mi-crobiol. 69: 376-389.
56. Lee VT, Matewish JM, Kessler JL, Hyodo M, Hayakawa Y, Lory S. 2007. A cyclic-di-GMP receptor required for bacterial exopolysaccharide production. Mol. Microbiol. 65: 1474-1484.
57. Merighi M, Lee VT, Hyodo M, Hayakawa Y, Lory S. 2007. The second messenger bis-(3=-5=)-cyclic-GMP and its PilZ domain-containing receptor Alg44 are required for alginate biosynthesis in Pseudomonas aerugi-nosa. Mol. Microbiol. 65: 876-895.
58. Ryan RP, Tolker-Nielsen T, Dow JM. 2012. When the PilZ don't work: effectors for cyclic di-GMP action in bacteria. Trends Microbiol. 20: 235-242.