Attenuation of Pseudomonas aeruginosa virulence factors and biofilms by co-encapsulation of bismuth-ethanedithiol with tobramycin in liposomes

Journal of Antimicrobial Chemotherapy

Volumn 65, Issue 4, 2010, Pages 684-693

  Alipour, Misagh ^a   Suntres, Zacharias E ^a,b   Lafrenie, Robert M ^a,c   Omri, Abdelwahab ^a  

^a LAURENTIAN UNIVERSITY   (Canada)

^b LAKEHEAD UNIVERSITY   (Canada)

^c SUDBURY REGIONAL HOSPITAL   (Canada)

Author keywords

Antibiotics; Bacterial adhesion; Cystic fibrosis; Quorum sensing

Indexed keywords

BISMUTH; CHITINASE; ELASTASE; LIPOSOME; N ACYLHOMOSERINE LACTONE; PROTEINASE; PYOCYANINE; PYOVERDINE; TOBRAMYCIN; VIRULENCE FACTOR; 1,2 ETHANEDITHIOL; 1,2-ETHANEDITHIOL; ANTIINFECTIVE AGENT; BACTERIAL PROTEIN; DRUG DERIVATIVE; MERCAPTOETHANOL;

ARTICLE; BACTERIAL VIRULENCE; BIOFILM; CELL ADHESION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYSTIC FIBROSIS; DRUG DELIVERY SYSTEM; DRUG FORMULARY; ENCAPSULATION; ENZYME SYNTHESIS; IN VITRO STUDY; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PSEUDOMONAS AERUGINOSA; QUORUM SENSING; DRUG ANTAGONISM; DRUG EFFECT; HUMAN;

ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; BIOFILMS; HUMANS; LIPOSOMES; MERCAPTOETHANOL; PSEUDOMONAS AERUGINOSA; QUORUM SENSING; TOBRAMYCIN; VIRULENCE FACTORS;

EID: 77952557163     PISSN: 03057453     EISSN: 14602091     Source Type: Journal    
DOI: 10.1093/jac/dkq036     Document Type: Article

References (50)

1. Cheung JC, Deber CM. Misfolding of the cystic fibrosis transmembrane conductance regulator and disease. Biochemistry 2008; 47: 1465-73.
2. Buchanan PJ, Ernst RK, Elborn JS et al. Role of CFTR, Pseudomonas aeruginosa and Toll-like receptors in cystic fibrosis lung inflammation. Biochem Soc Trans 2009; 37: 863-7.
3. Saiman L, Chen Y, Gabriel PS et al. Synergistic activities of macrolide antibiotics against Pseudomonas aeruginosa, Burkholderia cepacia, Stenotrophomonas maltophilia, and Alcaligenes xylosoxidans isolated from patients with cystic fibrosis. Antimicrob Agents Chemother 2002; 46: 1105-7.
4. Lyczak JB, Cannon CL, Pier GB. Establishment of Pseudomonas aeruginosa infection: lessons from a versatile opportunist. Microbes Infect 2000; 2: 1051-60.
5. Sauer K, Camper AK, Ehrlich GD et al. Pseudomonas aeruginosa displays multiple phenotypes during development as a biofilm. J Bacteriol 2002; 184: 1140-54.
6. Moreau-Marquis S, Stanton BA, O'Toole GA. Pseudomonas aeruginosa biofilm formation in the cystic fibrosis airway. Pulm Pharmacol Ther 2008; 21: 595-9.
7. Walker TS, Tomlin KL, Worthen GS et al. Enhanced Pseudomonas aeruginosa biofilm development mediated by human neutrophils. Infect Immun 2005; 73: 3693-701.
8. Hassett DJ, Sutton MD, Schurr MJ et al. Pseudomonas aeruginosa hypoxic or anaerobic biofilm infections within cystic fibrosis airways. Trends Microbiol 2009; 17: 130-8.
9. Hooshangi S, Bentley WE. From unicellular properties to multicellular behavior: bacteria quorum sensing circuitry and applications. Curr Opin Biotechnol 2008; 19: 550-5.
10. Winstanley C, Fothergill JL. The role of quorum sensing in chronic cystic fibrosis Pseudomonas aeruginosa infections. FEMS Microbiol Lett 2009; 290:1-9.
11. Azghani AO, Baker JW, Shetty S et al. Pseudomonas aeruginosa elastase stimulates ERK signaling pathway and enhances IL-8 production by alveolar epithelial cells in culture. Inflamm Res 2002; 51: 506-10.
12. Azghani AO. Pseudomonas aeruginosa and epithelial permeability: role of virulence factors elastase and exotoxin A. Am J Respir Cell Mol Biol 1996; 15: 132-40.
13. Kirisits MJ, Parsek MR. Does Pseudomonas aeruginosa use intercellular signalling to build biofilm communities? Cell Microbiol 2006; 8: 1841-9.
14. Davies JC, Bilton D. Bugs, biofilms, and resistance in cystic fibrosis. Respir Care 2009; 54: 628-40.
15. O'May CY, Reid DW, Kirov SM. Anaerobic culture conditions favor biofilm-like phenotypes in Pseudomonas aeruginosa isolates from patients with cystic fibrosis. FEMS Immunol Med Microbiol 2006; 48: 373-80.
16. Parsek MR, Tolker-Nielsen T. Pattern formation in Pseudomonas aeruginosa biofilms. Curr Opin Microbiol 2008; 11: 560-6.
17. Kim J, Hahn JS, Franklin MJ et al. Tolerance of dormant and active cells in Pseudomonas aeruginosa PA01 biofilm to antimicrobial agents. J Antimicrob Chemother 2009; 63: 129-35.
18. Kim J, Pitts B, Stewart PS et al. Comparison of the antimicrobial effects of chlorine, silver ion, and tobramycin on biofilm. Antimicrob Agents Chemother 2008; 52: 1446-53.
19. Lee TW. Eradication of early Pseudomonas infection in cystic fibrosis. Chron Respir Dis 2009; 6: 99-107.
20. Bauernfeind A, Bertele RM, Harms K et al. Qualitative and quantitative microbiological analysis of sputa of 102 patients with cystic fibrosis. Infection 1987; 15: 270-7.
21. Geller DE. Aerosol antibiotics in cystic fibrosis. Respir Care 2009; 54: 658-70.
22. Newton TJ. Respiratory care of the hospitalized patient with cystic fibrosis. Respir Care 2009; 54: 769-75; discussion 75-6.
23. Islam S, Oh H, Jalal S et al. Chromosomal mechanisms of aminoglycoside resistance in Pseudomonas aeruginosa isolates from cystic fibrosis patients. Clin Microbiol Infect 2009; 15:60-6.
24. Mulrennan SA, Helm J, Thomas RB et al. Aminoglycoside ototoxicity susceptibility in cystic fibrosis. Thorax 2009; 64: 271-2.
25. Domenico P, O'Leary R, Cunha BA. Differential effects of bismuth and salicylate salts on the antibiotic susceptibility of Pseudomonas aeruginosa. Eur J Clin Microbiol Infect Dis 1992; 11: 170-5.
26. Domenico P, Salo RJ, Novick SG et al. Enhancement of bismuth antibacterial activity with lipophilic thiol chelators. Antimicrob Agents Chemother 1997; 41: 1697-703.
27. Veloira WG, Domenico P, LiPuma JJ et al. In vitro activity and synergy of bismuth thiols and tobramycin against Burkholderia cepacia complex. J Antimicrob Chemother 2003; 52: 915-9.
28. Wu CL, Domenico P, Hassett DJ et al. Subinhibitory bismuth-thiols reduce virulence of Pseudomonas aeruginosa. Am J Respir Cell Mol Biol 2002; 26: 731-8.
29. Halwani M, Blomme S, Suntres ZE et al. Liposomal bismuth- ethanedithiol formulation enhances antimicrobial activity of tobramycin. Int J Pharm 2008; 358: 278-84.
30. Halwani M, Hebert S, Suntres ZE et al. Bismuth-thiol incorporation enhances biological activities of liposomal tobramycin against bacterial biofilm and quorum sensing molecules production by Pseudomonas aeruginosa. Int J Pharm 2009; 373: 141-6.
31. Immordino ML, Dosio F, Cattel L. Stealth liposomes: review of the basic science, rationale, and clinical applications, existing and potential. Int J Nanomed 2006; 1: 297-315.
32. Alipour M, Suntres ZE, Halwani M et al. Activity and interactions of liposomal antibiotics in presence of polyanions and sputum of patients with cystic fibrosis. PLoS One 2009; 4: e5724.
33. Clark DJ, Maaloe O. DNA replication and the division cycle in Escherichia coli. J Mol Biol 1967; 23: 99-112.
34. McLean RJ, Pierson LS III, Fuqua C. A simple screening protocol for the identification of quorum signal antagonists. J Microbiol Methods 2004; 58: 351-60.
35. Wagner T, Soong G, Sokol S et al. Effects of azithromycin on clinical isolates of Pseudomonas aeruginosa from cystic fibrosis patients. Chest 2005; 128: 912-9.
36. Bohn YS, Brandes G, Rakhimova E et al. Multiple roles of Pseudomonas aeruginosa TBCF10839 PilY1 in motility, transport and infection. Mol Microbiol 2009; 71: 730-47.
37. Ni N, Li M, Wang J et al. Inhibitors and antagonists of bacterial quorum sensing. Med Res Rev 2009; 29: 65-124.
38. Domenico P, Baldassarri L, Schoch PE et al. Activities of bismuth thiols against staphylococci and staphylococcal biofilms. Antimicrob Agents Chemother 2001; 45: 1417-21.
39. Domenico P, Landolphi DR, Cunha BA. Reduction of capsular polysaccharide and potentiation of aminoglycoside inhibition in Gram-negative bacteria by bismuth subsalicylate. J Antimicrob Chemother 1991; 28: 801-10.
40. Domenico P, Reich J, Madonia W et al. Resistance to bismuth among Gram-negative bacteria is dependent upon iron and its uptake. J Antimicrob Chemother 1996; 38: 1031-40.
41. Goller CC, Romeo T. Environmental influences on biofilm development. Curr Top Microbiol Immunol 2008; 322: 37-66.
42. Bjarnsholt T, Jensen PO, Rasmussen TB et al. Garlic blocks quorum sensing and promotes rapid clearing of pulmonary Pseudomonas aeruginosa infections. Microbiology 2005; 151: 3873-80.
43. Rasmussen TB, Bjarnsholt T, Skindersoe ME et al. Screening for quorum-sensing inhibitors (QSI) by use of a novel genetic system, the QSI selector. J Bacteriol 2005; 187: 1799-814.
44. Rasmussen TB, Skindersoe ME, Bjarnsholt T et al. Identity and effects of quorum-sensing inhibitors produced by Penicillium species. Microbiology 2005; 151: 1325-40.
45. Hoffman LR, D'Argenio DA, MacCoss MJ et al. Aminoglycoside antibiotics induce bacterial biofilm formation. Nature 2005; 436: 1171-5.
46. Linares JF, Gustafsson I, Baquero F et al. Antibiotics as intermicrobial signaling agents instead of weapons. Proc Natl Acad Sci USA 2006; 103: 19484-9.
47. Ahmed K, Gribbon PN, Jones MN. The application of confocal microscopy to the study of liposome adsorption onto bacterial biofilms. J Liposome Res 2002; 12: 285-300.
48. Meers P, Neville M, Malinin V et al. Biofilm penetration, triggered release and in vivo activity of inhaled liposomal amikacin in chronic Pseudomonas aeruginosa lung infections. J Antimicrob Chemother 2008; 61: 859-68.
49. Tre-Hardy M, Mace C, El Manssouri N et al. Effect of antibiotic co-administration on young and mature biofilms of cystic fibrosis clinical isolates: the importance of the biofilm model. Int J Antimicrob Agents 2009; 33:40-5.
50. Domenico P, Gurzenda E, Giacometti A et al. BisEDT and RIP act in synergy to prevent graft infections by resistant staphylococci. Peptides 2004; 25: 2047-53.