Improved biofilm antimicrobial activity of polyethylene glycol conjugated tobramycin compared to tobramycin in pseudomonas aeruginosa biofilms

Molecular Pharmaceutics

Volumn 12, Issue 5, 2015, Pages 1544-1553

  Du, Ju ^a   Bandara, H M H N ^a   Du, Ping ^a   Huang, Hui ^a   Hoang, Khang ^b   Nguyen, Dang ^a   Mogarala, Sri Vasudha ^a   Smyth, Hugh D C ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^b The University of Texas at Austin   (United States)

Author keywords

biofilm model; cystic fibrosis; minimum inhibitory concentration; PEGylation; planktonic

Indexed keywords

MACROGOL; TOBRAMYCIN; ANTIINFECTIVE AGENT; MACROGOL DERIVATIVE;

ANTIBIOTIC RESISTANCE; ANTIMICROBIAL ACTIVITY; ARTICLE; BIOFILM; CHEMICAL MODIFICATION; COMPARATIVE STUDY; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; DRUG CONJUGATION; DRUG EFFICACY; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PLANKTON; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; SCANNING ELECTRON MICROSCOPY; CHEMISTRY; DRUG EFFECTS; MICROBIAL SENSITIVITY TEST;

ANTI-INFECTIVE AGENTS; BIOFILMS; MICROBIAL SENSITIVITY TESTS; POLYETHYLENE GLYCOLS; PSEUDOMONAS AERUGINOSA; TOBRAMYCIN;

EID: 84929160999     PISSN: 15438384     EISSN: 15438392     Source Type: Journal    
DOI: 10.1021/mp500846u     Document Type: Article

References (68)

1. Boucher, R. C. New concepts of the pathogenesis of cystic fibrosis lung disease Eur. Respir. J. 2004, 23 (1) 146-158
2. Hoiby, N.; Krogh-Johansen, H.; Moser, C.; Song, Z.; Ciofu, O.; Kharazmi, A. Pseudomonas aeruginosa and the in vitro and in vivo biofilm mode of growth Microbes. Infect. 2001, 3 (1) 23-35
3. Moss, R. B. Infection, inflammation, and the downward spiral of cystic fibrosis lung disease J. Pediatr. 2009, 154 (2) 162-163
4. Frederiksen, B.; Koch, C.; Hoiby, N. Changing epidemiology of Pseudomonas aeruginosa infection in Danish cystic fibrosis patients (1974-1995) Pediatr. Pulmonol. 1999, 28 (3) 159-166
5. Szaff, M.; Hoiby, N.; Flensborg, E. W. Frequent antibiotic therapy improves survival of cystic fibrosis patients with chronic Pseudomonas aeruginosa infection Acta Paediatr. 1983, 72 (5) 651-657
6. Hoffmann, N.; Rasmussen, T. B.; Jensen, P. Ø.; Stub, C.; Hentzer, M.; Molin, S.; Ciofu, O.; Givskov, M.; Johansen, H. K.; Høiby, N. Novel mouse model of chronic Pseudomonas aeruginosa lung infection mimicking cystic fibrosis Infect. Immun. 2005, 73 (4) 2504-2514
7. Jelsbak, L.; Johansen, H. K.; Frost, A. L.; Thøgersen, R.; Thomsen, L. E.; Ciofu, O.; Yang, L.; Haagensen, J. A.; Høiby, N.; Molin, S. Molecular epidemiology and dynamics of Pseudomonas aeruginosa populations in lungs of cystic fibrosis patients Infect. Immun. 2007, 75 (5) 2214-2224
8. Bjarnsholt, T.; Jensen, P. Ø.; Fiandaca, M. J.; Pedersen, J.; Hansen, C. R.; Andersen, C. B.; Pressler, T.; Givskov, M.; Høiby, N. Pseudomonas aeruginosa biofilms in the respiratory tract of cystic fibrosis patients Pediatr. Pulmonol. 2009, 44 (6) 547-558
9. Vu, B.; Chen, M.; Crawford, R. J.; Ivanova, E. P. Bacterial extracellular polysaccharides involved in biofilm formation Molecules. 2009, 14 (7) 2535-2554
10. Mah, T. F.; O'Toole, G. A. Mechanisms of biofilm resistance to antimicrobial agents Trends. Microbiol. 2001, 9 (1) 34-39
11. Potera, C. Antibiotic Resistance: Biofilm Dispersing Agent Rejuvenates Older Antibiotics Environ. Health. Perspect. 2010, 118 (7) A288
12. Hoiby, N.; Bjarnsholt, T.; Givskov, M.; Molin, S.; Ciofu, O. Antibiotic resistance of bacterial biofilms Int. J. Antimicrob. Agents. 2010, 35 (4) 322-332
13. d'Angelo, I.; Conte, C.; LaRotonda, M. I.; Miro, A.; Quaglia, F.; Ungaro, F. Improving the efficacy of inhaled drugs in cystic fibrosis: Challenges and emerging drug delivery strategies Adv. Drug. Delivery Rev. 2014, 75, 92-111
14. Fux, C. A.; Costerton, J. W.; Stewart, P. S.; Stoodley, P. Survival strategies of infectious biofilms Trends. Microbiol. 2005, 13 (1) 34-40
15. Stewart, P. S.; Costerton, J. W. Antibiotic resistance of bacteria in biofilms Lancet 2001, 358 (9276) 135-138
16. Hoiby, N.; Ciofu, O.; Bjarnsholt, T. Pseudomonas aeruginosa biofilms in cystic fibrosis Future Microbiol. 2010, 5 (11) 1663-1674
17. Costerton, J. W.; Stewart, P. S.; Greenberg, E. P. Bacterial biofilms: a common cause of persistent infections Science 1999, 284 (5418) 1318-1322
18. Lee, B.; Haagensen, J. A.; Ciofu, O.; Andersen, J. B.; Hoiby, N.; Molin, S. Heterogeneity of biofilms formed by nonmucoid Pseudomonas aeruginosa isolates from patients with cystic fibrosis J. Clin. Microbiol. 2005, 43 (10) 5247-5255
19. George, A. M.; Jones, P. M.; Middleton, P. G. Cystic fibrosis infections: treatment strategies and prospects FEMS Microbiol. Lett. 2009, 300 (2) 153-164
20. Flemming, H. C.; Wingender, J. The biofilm matrix Nat. Rev. Microbiol. 2010, 8 (9) 623-633
21. Giwercman, B.; Lambert, P. A.; Rosdahl, V. T.; Shand, G. H.; Hoiby, N. Rapid emergence of resistance in Pseudomonas aeruginosa in cystic fibrosis patients due to in-vivo selection of stable partially derepressed beta-lactamase producing strains J. Antimicrob. Chemother. 1990, 26 (2) 247-259
22. Giwercman, B.; Meyer, C.; Lambert, P. A.; Reinert, C.; Hoiby, N. High-level beta-lactamase activity in sputum samples from cystic fibrosis patients during antipseudomonal treatment Antimicrob. Agents Chemother. 1992, 36 (1) 71-76
23. Jalal, S.; Ciofu, O.; Hoiby, N.; Gotoh, N.; Wretlind, B. Molecular mechanisms of fluoroquinolone resistance in Pseudomonas aeruginosa isolates from cystic fibrosis patients Antimicrob. Agents Chemother. 2000, 44 (3) 710-712
24. Saiman, L.; Mehar, F.; Niu, W. W.; Neu, H. C.; Shaw, K. J.; Miller, G.; Prince, A. Antibiotic susceptibility of multiply resistant Pseudomonas aeruginosa isolated from patients with cystic fibrosis, including candidates for transplantation Clin. Infect. Dis. 1996, 23 (3) 532-537
25. Westbrock-Wadman, S.; Sherman, D. R.; Hickey, M. J.; Coulter, S. N.; Zhu, Y. Q.; Warrener, P.; Nguyen, L. Y.; Shawar, R. M.; Folger, K. R.; Stover, C. K. Characterization of a Pseudomonas aeruginosa efflux pump contributing to aminoglycoside impermeability Antimicrob. Agents Chemother. 1999, 43 (12) 2975-2983
26. Burns, J. L.; VanDalfsen, J. M.; Shawar, R. M.; Otto, K. L.; Garber, R. L.; Quan, J. M.; Montgomery, A. B.; Albers, G. M.; Ramsey, B. W.; Smith, A. L. Effect of chronic intermittent administration of inhaled tobramycin on respiratory microbial flora in patients with cystic fibrosis J. Infect. Dis. 1999, 179 (5) 1190-1196
27. MacLeod, D. L.; Nelson, L. E.; Shawar, R. M.; Lin, B. B.; Lockwood, L. G.; Dirk, J. E.; Miller, G. H.; Burns, J. L.; Garber, R. L. Aminoglycoside-resistance mechanisms for cystic fibrosis Pseudomonas aeruginosa isolates are unchanged by long-term, intermittent, inhaled tobramycin treatment J. Infect. Dis. 2000, 181 (3) 1180-1184
28. Denton, M.; Kerr, K.; Mooney, L.; Keer, V.; Rajgopal, A.; Brownlee, K.; Arundel, P.; Conway, S. Transmission of colistin-resistant Pseudomonas aeruginosa between patients attending a pediatric cystic fibrosis center Pediatr. Pulmonol. 2002, 34 (4) 257-261
29. Johansen, H. K.; Moskowitz, S. M.; Ciofu, O.; Pressler, T.; Hoiby, N. Spread of colistin resistant non-mucoid Pseudomonas aeruginosa among chronically infected Danish cystic fibrosis patients J. Cyst. Fibros. 2008, 7 (5) 391-397
30. Anderson, G. G.; Kenney, T. F.; Macleod, D. L.; Henig, N. R.; O'Toole, G. A. Eradication of Pseudomonas aeruginosa biofilms on cultured airway cells by a fosfomycin/tobramycin antibiotic combination Pathog. Dis. 2013, 67 (1) 39-45
31. Mesaros, N.; Nordmann, P.; Plésiat, P.; Roussel-Delvallez, M.; VanEldere, J.; Glupczynski, Y.; VanLaethem, Y.; Jacobs, F.; Lebecque, P.; Malfroot, A.; Tulkens, P. M.; VanBambeke, F. Pseudomonas aeruginosa: resistance and therapeutic options at the turn of the new millennium Clin. Microbiol. Infect. 2007, 13 (6) 560-578
32. Mingeot-Leclercq, M. P.; Glupczynski, Y.; Tulkens, P. M. Aminoglycosides: activity and resistance Antimicrob. Agents Chemother. 1999, 43 (4) 727-737
33. Tre-Hardy, M.; Traore, H.; El-Manssouri, N.; Vanderbist, F.; Vaneechoutte, M.; Devleeschouwer, M. J. Evaluation of long-term co-administration of tobramycin and clarithromycin in a mature biofilm model of cystic fibrosis clinical isolates of Pseudomonas aeruginosa Int. J. Antimicrob. Agents 2009, 34 (4) 370-374
34. Woodward, T. C.; Brown, R.; Sacco, P.; Zhang, J. Budget impact model of tobramycin inhalation solution for treatment of Pseudomonas aeruginosa in cystic fibrosis patients J. Med. Econ. 2010, 13 (3) 492-499
35. McKeage, K. Tobramycin inhalation powder: a review of its use in the treatment of chronic Pseudomonas aeruginosa infection in patients with cystic fibrosis Drugs 2013, 73 (16) 1815-1827
36. Pier, G. B. The challenges and promises of new therapies for cystic fibrosis J. Exp. Med. 2012, 209 (7) 1235-1239
37. Ratjen, F. A. Cystic fibrosis: pathogenesis and future treatment strategies Respir. Care 2009, 54 (5) 595-605
38. Tseng, B. S.; Zhang, W.; Harrison, J. J.; Quach, T. P.; Song, J. L.; Penterman, J.; Singh, P. K.; Chopp, D. L.; Packman, A. I.; Parsek, M. R. The extracellular matrix protects Pseudomonas aeruginosa biofilms by limiting the penetration of tobramycin Environ. Microbiol. 2013, 15 (10) 2865-2878
39. Stewart, P. S. Theoretical aspects of antibiotic diffusion into microbial biofilms Antimicrob. Agents Chemother. 1996, 40 (11) 2517-2522
40. Alconcel, S. N. S.; Baas, A. S.; Maynard, H. D. FDA-approved poly(ethylene glycol)-protein conjugate drugs Polym. Chem. 2011, 2, 1442-1448
41. Veronese, F. M.; Schiavon, O.; Pasut, G.; Mendichi, R.; Andersson, L.; Tsirk, A.; Ford, J.; Wu, G.; Kneller, S.; Davies, J.; Duncan, R. PEG-doxorubicin conjugates: influence of polymer structure on drug release, in vitro cytotoxicity, biodistribution, and antitumor activity Bioconjugate Chem. 2005, 16 (4) 775-784
42. Yang, H.; Lopina, S. T. Penicillin V-conjugated PEG-PAMAM star polymers J. Biomater. Sci. Polym. Ed. 2003, 14 (10) 1043-1056
43. Liu, Z.; Robinson, J. T.; Sun, X.; Dai, H. PEGylated nanographene oxide for delivery of water-insoluble cancer drugs J. Am. Chem. Soc. 2008, 130 (33) 10876-10877
44. van-Vlerken, L. E.; Vyas, T. K.; Amiji, M. M. Poly (ethylene glycol)-modified nanocarriers for tumor-targeted and intracellular delivery Pharm. Res. 2007, 24 (8) 1405-1414
45. Suk, J. S.; Kim, A. J.; Trehan, K.; Schneider, C. S.; Cebotaru, L.; Woodward, O. M.; Boylan, N. J.; Boyle, M. P.; Lai, S. K.; Guggino, W. B.; Hanes, J. Lung gene therapy with highly compacted DNA nanoparticles that overcome the mucus barrier J. Controlled Release 2014, 178, 8-17
46. Shaul, P.; Green, K. D.; Rutenberg, R.; Kramer, M.; Berkov-Zrihen, Y.; Breiner-Goldstein, E.; Garneau-Tsodikova, S.; Fridman, M. Assessment of 6′- and 6-N-acylation of aminoglycosides as a strategy to overcome bacterial resistance Org. Biomol. Chem. 2011, 9 (11) 4057-4063
47. Luten, J.; van-Steenbergen, M. J.; Lok, M. C.; de-Graaff, A. M.; van-Nostrum, C. F.; Talsma, H.; Hennink, W. E. Degradable PEG-folate coated poly(DMAEA-co-BA)phosphazene-based polyplexes exhibit receptor-specific gene expression Eur. J. Pharm. Sci. 2008, 33 (3) 241-251
48. Popielarski, S. R.; Pun, S. H.; Davis, M. E. A nanoparticle-based model delivery system to guide the rational design of gene delivery to the liver. 1. Synthesis and characterization Bioconjugate Chem. 2005, 16 (5) 1063-1070
49. Wu, Y.; Liu, C.; Zhao, X.; Xiang, J. A new biodegradable polymer: PEGylated chitosan-g-PEI possessing a hydroxyl group at the PEG end J. Polym. Res. 2008, 15 (3) 181-185
50. El-Sherbiny, I. M.; McGill, S.; Smyth, H. D. Swellable microparticles as carriers for sustained pulmonary drug delivery J. Pharm. Sci. 2010, 99 (5) 2343-2356
51. Bandara, H. M.; Yau, J. Y.; Watt, R. M.; Jin, L. J.; Samaranayake, L. P. Pseudomonas aeruginosa inhibits in-vitro Candida biofilm development BMC Microbiol. 2010, 10, 125
52. Bandara, H. M.; Cheung, B. P. K.; Watt, R. M.; Jin, L. J.; Samaranayake, L. P. Pseudomonas aeruginosa lipopolysaccharide inhibits Candida albicans hyphae formation and alters gene expression during biofilm development Mol. Oral. Microbiol. 2013, 28 (1) 54-69
53. Bandara, H. M.; Lam, O. L.; Watt, R. M.; Jin, L. J.; Samaranayake, L. P. Bacterial lipopolysaccharides variably modulate in vitro biofilm formation of Candida species J. Med. Microbiol. 2010, 59 (10) 1225-1234
54. Alhede, M.; Qvortrup, K.; Liebrechts, R.; Hoiby, N.; Givskov, M.; Bjarnsholt, T. Combination of microscopic techniques reveals a comprehensive visual impression of biofilm structure and composition FEMS Immunol. Med. Microbiol. 2012, 65 (2) 335-342
55. Reznikov, L. R.; Abou-Alaiwa, M. H.; Dohrn, C. L.; Gansemer, N. D.; Diekema, D. J.; Stoltz, D. A.; Welsh, M. J. Antibacterial properties of the CFTR potentiator ivacaftor J. Cystic Fibrosis 2014, 13 (5) 515-519
56. Tin, S.; Sakharkar, K. R.; Lim, C. S.; Sakharkar, M. K. Activity of Chitosans in combination with antibiotics in Pseudomonas aeruginosa Int. J. Biol. Sci. 2009, 5 (2) 153-160
57. Wiegand, I.; Hilpert, K.; Hancock, R. E. Agar and broth dilution methods to determine the minimal inhibitory concentration (MIC) of antimicrobial substances Nat. Protoc. 2008, 3 (2) 163-175
58. Lai, S. K.; Wang, Y. Y.; Hanes, J. Mucus-penetrating nanoparticles for drug and gene delivery to mucosal tissues Adv. Drug. Delivery Rev. 2009, 61 (2) 158-171
59. Mert, O.; Lai, S. K.; Ensign, L.; Yang, M.; Wang, Y. Y.; Wood, J.; Hanes, J. A poly (ethylene glycol)-based surfactant for formulation of drug-loaded mucus penetrating particles J. Controlled Release 2012, 157 (3) 455-460
60. Nickel, J. C.; Ruseska, I.; Wright, J. B.; Costerton, J. W. Tobramycin resistance of Pseudomonas aeruginosa cells growing as a biofilm on urinary catheter material Antimicrob. Agents Chemother. 1985, 27 (4) 619-624
61. Klepser, M. E.; Ernst, E. J.; Ernst, M. E.; Messer, S. A.; Pfaller, M. A. Evaluation of endpoints for antifungal susceptibility determinations with LY303366 Antimicrob. Agents Chemother. 1998, 42 (6) 1387-1391
62. Xu, X.; Zhou, X. D.; Wu, C. D. Tea catechin epigallocatechin gallate inhibits Streptococcus mutans biofilm formation by suppressing gtf genes Arch. Oral. Biol. 2012, 57 (6) 678-683
63. Kotra, L. P.; Haddad, J.; Mobashery, S. Aminoglycosides: perspectives on mechanisms of action and resistance and strategies to counter resistance Antimicrob. Agents Chemother. 2000, 44 (12) 3249-3256
64. Magnet, S.; Blanchard, J. S. Molecular insights into aminoglycoside action and resistance Chem. Rev. 2005, 105 (2) 477-498
65. Hancock, R. E.; Farmer, S. W.; Li, Z. S.; Poole, K. Interaction of aminoglycosides with the outer membranes and purified lipopolysaccharide and OmpF porin of Escherichia coli Antimicrob. Agents Chemother. 1991, 35 (7) 1309-1314
66. Jana, S.; Deb, J. K. Molecular understanding of aminoglycoside action and resistance Appl. Microbiol. Biotechnol. 2006, 70 (2) 140-150
67. Wu, L.; Zaborina, O.; Zaborin, A.; Chang, E. B.; Musch, M.; Holbrook, C.; Shapiro, J.; Turner, J. R.; Wu, G.; Lee, K. Y.; Alverdy, J. C. High-molecular-weight polyethylene glycol prevents lethal sepsis due to intestinal Pseudomonas aeruginosa Gastroenterology. 2004, 126 (2) 488-498
68. Dhondikubeer, R.; Bera, S.; Zhanel, G. G.; Schweizer, F. Antibacterial activity of amphiphilic tobramycin J. Antibiot. 2012, 65 (10) 495-498