Tobramycin and FDA-approved iron chelators eliminate Pseudomonas aeruginosa biofilms on cystic fibrosis cells

American Journal of Respiratory Cell and Molecular Biology

Volumn 41, Issue 3, 2009, Pages 305-313

  Moreau Marquis, Sophie ^a   O'Toole, George A ^a   Stanton, Bruce A ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

Antibiotic resistance; Biofilms; Cystic fibrosis model; Deferasirox; Deferoxamine

Indexed keywords

DEFERASIROX; DEFEROXAMINE; DEFEROXAMINE MESYLATE; IRON; TOBRAMYCIN;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL VIABILITY; BACTERIAL VIRULENCE; BIOFILM; BIOMASS; CONTROLLED STUDY; CYSTIC FIBROSIS; DRUG EFFECT; FOOD AND DRUG ADMINISTRATION; HUMAN; HUMAN CELL; IRON CHELATION; NONHUMAN; PSEUDOMONAS AERUGINOSA;

ANTI-BACTERIAL AGENTS; BENZOIC ACIDS; BIOFILMS; CELLS, CULTURED; CONALBUMIN; CYSTIC FIBROSIS; DEFEROXAMINE; EPITHELIAL CELLS; HUMANS; IRON CHELATING AGENTS; PSEUDOMONAS INFECTIONS; TOBRAMYCIN; TRIAZOLES; UNITED STATES; UNITED STATES FOOD AND DRUG ADMINISTRATION;

BACTERIA (MICROORGANISMS); PSEUDOMONAS AERUGINOSA;

EID: 69449107153     PISSN: 10441549     EISSN: None     Source Type: Journal    
DOI: 10.1165/rcmb.2008-0299OC     Document Type: Article

References (62)

1. Tümmler B, Kiewitz C. Cystic fibrosis: an inherited susceptibility to bacterial respiratory infections. Mol Med Today 1999;5:351-358. (Pubitemid 29364562)
2. Deneuville E, Perrot-Minot C, Pennaforte F, Roussey M, Zahm JM, Clavel C, Puchelle E, de Bentzmann S. Revisited physicochemical and transport properties of respiratory mucus in genotyped cystic fibrosis patients. Am J Respir Crit Care Med 1997;156:166-172. (Pubitemid 27293183)
3. Tomkiewicz R, App E, Zayas J, Ramirez O, Church N, Boucher R, Knowles M, King M. Amiloride inhalation therapy in cystic fibrosis: influence on ion content, hydration, and rheology of sputum. Am Rev Respir Dis 1993;148:1002-1007. (Pubitemid 23301221)
4. Gomez MI, Prince A. Opportunistic infections in lung disease: Pseudomonas infections in cystic fibrosis. Curr Opin Pharmacol 2007;7:244-251. (Pubitemid 46731196)
5. Ramsey BW. Management of pulmonary disease in patients with cystic fibrosis. N Engl J Med 1996;335:179-188. (Pubitemid 26249456)
6. Heijerman H. Infection and inflammation in cystic fibrosis: a short review. J Cyst Fibros 2005;4:3-5. (Pubitemid 41131322)
7. Lyczak JB, Cannon CL, Pier GB. Lung infections associated with cystic fibrosis. Clin Microbiol Rev 2002;15:194-222. (Pubitemid 34303763)
8. Hoiby N, Frederiksen B, Pressler T. Eradication of early Pseudomonas aeruginosa infection. J Cyst Fibros 2005;4:49-54. (Pubitemid 41131329)
9. Drenkard E, Ausubel FM. Pseudomonas biofilm formation and antibiotic resistance are linked to phenotypic variation. Nature 2002;416: 740-743. (Pubitemid 34429150)
10. Costerton JW, Stewart PS, Greenberg EP. Bacterial biofilms: a common cause of persistent infections. Science 1999;284:1318-1322. (Pubitemid 29289651)
11. Donlan RM, Costerton JW. Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev 2002;15:167-193.
12. Mah TF, O'Toole GA. Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol 2001;9:34-39. (Pubitemid 32467503)
13. Chernish R, Aaron S. Approach to resistant gram-negative bacterial pulmonary infections in patients with cystic fibrosis. Curr Opin Pulm Med 2003;9:509-515. (Pubitemid 37268216)
14. Gibson RL, Burns JL, Ramsey BW. Pathophysiology and management of pulmonary infections in cystic fibrosis. Am J Respir Crit Care Med 2003;168:918-951. (Pubitemid 37267172)
15. Singh P. Iron sequestration by human lactoferrin stimulates P. aeruginosa surface motility and blocks biofilm formation. Biometals 2004;17: 267-270. (Pubitemid 38987148)
16. Singh PK, Parsek MR, Greenberg EP, Welsh MJ. A component of innate immunity prevents bacterial biofilm development. Nature 2002; 417:552-555.
17. Patriquin GM, Banin E, Gilmour C, Tuchman R, Greenberg EP, Poole K. Influence of quorum-sensing and iron on twitching motility and biofilm formation in Pseudomonas aeruginosa. J Bacteriol 2008;190: 662-671. (Pubitemid 351360082)
18. Banin E, Vasil ML, Greenberg EP. Iron and Pseudomonas aeruginosa biofilm formation. Proc Natl Acad Sci USA 2005;102:11076-11081. (Pubitemid 41105995)
19. Berlutti F, Morea C, Battistoni A, Sarli S, Cipriani P, Superti F, Ammendolia M, Valenti P. Iron availability influences aggregation, biofilm, adhesion and invasion of Pseudomonas aeruginosa and Burkholderia cenocepacia. Int J Immunopathol Pharmacol 2005;18:661-670.
20. Moreau-Marquis S, Bomberger JM, Anderson GG, Swiatecka-Urban A, Ye S, O'Toole GA, Stanton BA. The DF508-CFTR mutation results in increased biofilm formation by P. aeruginosa by increasing iron availability. Am J Physiol Lung Cell Mol Physiol 2008;295:L25-L37.
21. Geller DE, Pitlick WH, Nardella PA, Tracewell WG, Ramsey BW. Pharmacokinetics and bioavailability of aerosolized tobramycin in cystic fibrosis. Chest 2002;122:219-226. (Pubitemid 34754166)
22. Harbitz O, Jenssen A, Smidsrød O. Lysozyme and lactoferrin in sputum from patients with chronic obstructive lung disease. Eur J Respir Dis 1984;65:512-520. (Pubitemid 14038811)
23. Thompson A, Bohling T, Payvandi F, Rennard S. Lower respiratory tract lactoferrin and lysozyme arise primarily in the airways and are elevated in association with chronic bronchitis. J Lab Clin Med 1990; 115:148-158. (Pubitemid 20084406)
24. Banin E, Brady KM, Greenberg EP. Chelator-induced dispersal and killing of Pseudomonas aeruginosa cells in a biofilm. Appl Environ Microbiol 2006;72:2064-2069.
25. Yakandawala N, Gawande PV, LoVetri K, Madhyastha S. Effect of ovotransferrin, protamine sulfate and EDTA combination on biofilm formation by catheter-associated bacteria. J Appl Microbiol 2007;102: 722-727. (Pubitemid 46271211)
26. Kite P, Eastwood K, Sugden S, Percival SL. Use of in vivo-generated biofilms from hemodialysis catheters to test the efficacy of a novel antimicrobial catheter lock for biofilm eradication in vitro. J Clin Microbiol 2004;42:3073-3076. (Pubitemid 38938060)
27. Raad I, Chatzinikolaou I, Chaiban G, Hanna H, Hachem R, Dvorak T, Cook G, Costerton W. In vitro and ex vivo activities of minocycline and EDTA against microorganisms embedded in biofilm on catheter surfaces. Antimicrob Agents Chemother 2003;47:3580-3585.
28. Ayres HM, Payne DN, Furr JR, Russell AD. Effect of permeabilizing agents on antibacterial activity against a simple Pseudomonas aeruginosa biofilm. Lett Appl Microbiol 1998;27:79-82.
29. Kaneko Y, Thoendel M, Olakanmi O, Britigan BE, Singh PK. The transition metal gallium disrupts Pseudomonas aeruginosa iron metabolism and has antimicrobial and antibiofilm activity. J Clin Invest 2007;117:877-888. (Pubitemid 46556744)
30. Banin E, Lozinski A, Brady KM, Berenshtein E, Butterfield PW, Moshe M, Chevion M, Greenberg EP, Banin E. The potential of desferrioxamine-gallium as an anti-Pseudomonas therapeutic agent. Proc Natl Acad Sci USA 2008;105:16761- 16765.
31. Halwani M, Yebio B, Suntres Z, Alipour M, Azghani A, Omri A. Coencapsulation of gallium with gentamicin in liposomes enhances antimicrobial activity of gentamicin against Pseudomonas aeruginosa. J Antimicrob Chemother 2008;62:1291-1297.
32. Bruscia E, Sangiuolo F, Sinibaldi P, Goncz K, Novelli G, Gruenert D. Isolation of CF cell lines corrected at DeltaF508-CFTR locus by SFHR-mediated targeting. Gene Ther 2002;9:683-685. (Pubitemid 34591465)
33. Cozens A, Yezzi M, Kunzelmann K, Ohrui T, Chin L, Eng K, Finkbeiner W, Widdicombe J, Gruenert D. CFTR expression and chloride secretion in polarized immortal human bronchial epithelial cells. Am J Respir Cell Mol Biol 1994;10:38-47.
34. Bloemberg G, O'Toole G, Lugtenberg B, Kolter R. Green fluorescent protein as a marker for Pseudomonas spp. Appl Environ Microbiol 1997;63:4543-4551. (Pubitemid 27485787)
35. Kuchma SL, Connolly JP, O'Toole GA. A three-component regulatory system regulates biofilm maturation and type III secretion in Pseudomonas aeruginosa. J Bacteriol 2005;187:1441-1454. (Pubitemid 40305269)
36. Heydorn A, Ersboll BK, Hentzer M, Parsek MR, Givskov M, Molin S. Experimental reproducibility in flow-chamber biofilms. Microbiology 2000;146:2409-2415.
37. Heydorn A, Nielsen AT, Hentzer M, Sternberg C, Givskov M, Ersboll BK, Molin S. Quantification of biofilm structures by the novel computer program COMSTAT. Microbiology 2000;146:2395-2407. (Pubitemid 30806650)
38. Anderson GG, Moreau-Marquis S, Stanton BA, O'Toole GA. In vitro analysis of tobramycin-treated Pseudomonas aeruginosa biofilms on cystic fibrosis-derived airway epithelial cells. Infect Immun 2008;76: 1423-1433.
39. O'Toole GA, Kolter R. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol Microbiol 1998;30:295-304. (Pubitemid 28480181)
40. Kadouri D, O'Toole G. Susceptibility of biofilms to Bdellovibrio bacteriovorus attack. Appl Environ Microbiol 2005;71:4044-4051. (Pubitemid 40980577)
41. Stites S, Walters B, O'Brien-Ladner A, Bailey K, Wesselius L. Increased iron and ferritin content of sputum from patients with cystic fibrosis or chronic bronchitis. Chest 1998;114:814-819. (Pubitemid 28433746)
42. Stites SW, Plautz MW, Bailey K, O'Brien-Ladner AR, Wesselius LJ. Increased concentrations of iron and isoferritins in the lower respiratory tract of patients with stable cystic fibrosis. Am J Respir Crit Care Med 1999;160:796-801. (Pubitemid 29442011)
43. Alexis N, Richards J, Carter JD, Ghio AJ. Iron-binding and storage proteins in sputum. Inhal Toxicol 2002;14:387-400.
44. Nick H, Acklin P, Lattmann R, Buehlmayer P, Hauffe S, Schupp J, Alberti D. Development of tridentate iron chelators: from desferrithiocin to ICL670. Curr Med Chem 2003;10:1065-1076. (Pubitemid 36582249)
45. Mah TF, Pitts B, Pellock B, Walker GC, Stewart PS, O'Toole GA. A genetic basis for Pseudomonas aeruginosa biofilm antibiotic resistance. Nature 2003;426:306-310. (Pubitemid 37463151)
46. Nickel JC, Ruseska I, Wright JB, Costerton JW. Tobramycin resistance of Pseudomonas aeruginosa cells growing as a biofilm on urinary catheter material. Antimicrob Agents Chemother 1985;27:619-624. (Pubitemid 15097672)
47. Musk DJ, Hergenrother PJ. Chelated iron sources are inhibitors of Pseudomonas aeruginosa biofilms and distribute efficiently in an in vitro model of drug delivery to the human lung. J Appl Microbiol 2008;105:380-388.
48. Kozlowska WJ, Bush A, Wade A, Aurora P, Carr SB, Castle RA, Hoo A-F, Lum S, Price J, Ranganathan S, et al. Lung function from infancy to the preschool years after clinical diagnosis of cystic fibrosis. Am J Respir Crit Care Med 2008;178:42-49. (Pubitemid 351919192)
49. Javadpour S, Jones A, Brownlee K. Longitudinal analysis of FEV1 changes related to antibiotic therapy in children with cystic fibrosis. Ir Med J 2007;100:529-532.
50. Konstan M, Morgan W, Butler S, Pasta D, Craib M, Silva S, Stokes D, Wohl M, Wagener J, Regelmann W, et al. Risk factors for rate of decline in forced expiratory volume in one second in children and adolescents with cystic fibrosis. J Pediatr 2007;151:134-139. (Pubitemid 47069405)
51. Courtney J, Bradley J, Mccaughan J, O'Connor T, Shortt C, Bredin C, Bradbury I, Elborn J. Predictors of mortality in adults with cystic fibrosis. Pediatr Pulmonol 2007;42:525-532. (Pubitemid 46870384)
52. Ren C, Morgan W, Konstan M, Schechter M, Wagener J, Fisher K, Regelmann W; Investigators and Coordinators of the Epidemiologic Study of Cystic Fibrosis. Presence of methicillin resistant Staphylococcus aureus in respiratory cultures from cystic fibrosis patients is associated with lower lung function. Pediatr Pulmonol 2007;42:513-518.
53. Fischer R, Simmerlein R, Huber RM, Schiffl H, Lang SM. Lung disease severity, chronic inflammation, iron deficiency, and erythropoietin response in adults with cystic fibrosis. Pediatr Pulmonol 2007;42:1193-1197. (Pubitemid 350231871)
54. Reid DW, Withers NJ, Francis L, Wilson JW, Kotsimbos TC. Iron deficiency in cystic fibrosis: relationship to lung disease severity and chronic Pseudomonas aeruginosa Infection. Chest 2002;121:48-54. (Pubitemid 34114227)
55. Ater J, Herbst J, Landaw S, O'Brien R. Relative anemia and iron deficiency in cystic fibrosis. Pediatrics 1983;71:810-814.
56. Llamas MA, Sparrius M, Kloet R, Jimenez CR, Vandenbroucke-Grauls C, Bitter W. The heterologous siderophores ferrioxamine B and ferrichrome activate signaling pathways in Pseudomonas aeruginosa. J Bacteriol 2006;188:1882-1891. (Pubitemid 43346867)
57. Cuiv PO, Keogh D, Clarke P, O'Connell M. FoxB of Pseudomonas aeruginosa functions in the utilization of the xenosiderophores ferrichrome, ferrioxamine B, and schizokinen: evidence for transport redundancy at the inner membrane. J Bacteriol 2007;189:284-287. (Pubitemid 46036247)
58. Mustard R, Bohnen J, Mullen J, Schouten B, Swanson H. Deferoxamine induces hypotension in experimental gram-negative septicemia. Shock 1994;1:221-227.
59. Moch D, Schröppel B, Schoenberg M, Schulz H, Thorab F, Marzinzag M, Hedlund B, Brückner U. Protective effects of hydroxyethyl starch-deferoxamine in early sepsis. Shock 1995;4:425-432.
60. Lamont IL, Beare PA, Ochsner U, Vasil AI, Vasil ML. Siderophore-mediated signaling regulates virulence factor production in Pseudomonas aeruginosa. Proc Natl Acad Sci USA 2002;99:7072-7077. (Pubitemid 34526257)
61. Vasil ML, Ochsner UA. The response of Pseudomonas aeruginosa to iron: genetics, biochemistry and virulence. Mol Microbiol 1999;34: 399-413.
62. Wilderman PJ, Vasil AI, Johnson Z, Wilson MJ, Cunliffe HE, Lamont IL, Vasil ML. Characterization of an endoprotease (PrpL) encoded by a PvdS-regulated gene in Pseudomonas aeruginosa. Infect Immun 2001;69:5385-5394. (Pubitemid 32786470)