Anti-biofilm and immunomodulatory activities of peptides that inhibit biofilms formed by pathogens isolated from cystic fibrosis patients

Antibiotics

Volumn 3, Issue 4, 2014, Pages 509-526

  de la Fuente Núñez, César ^a   Mansour, Sarah C ^a   Wang, Zhejun ^a   Jiang, Lucy ^a   Breidenstein, Elena B M ^a   Elliott, Melissa ^a   Reffuveille, Fany ^a   Speert, David P ^a   Reckseidler Zenteno, Shauna L ^b   Shen, Ya ^a   Haapasalo, Markus ^a   Hancock, Robert E W ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b ATHABASCA UNIVERSITY   (Canada)

Author keywords

Anti biofilm; Antibiotic resistance; Cystic fibrosis; Immunomodulation; Peptides

Indexed keywords

LACTATE DEHYDROGENASE; MONOCYTE CHEMOTACTIC PROTEIN 1; PEPTIDE; TUMOR NECROSIS FACTOR ALPHA;

ANTI BIOFILM ACTIVITY; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL VIABILITY; BIOFILM; COLONY FORMING UNIT; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; CYSTIC FIBROSIS; CYTOTOXICITY; DRUG ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; IMMUNOMODULATION ACTIVITY; LUNG DISEASE; MASS SPECTROMETRY; MINIMUM INHIBITORY CONCENTRATION; MOLECULAR WEIGHT; NONHUMAN; PATHOGENESIS; PERIPHERAL BLOOD MONONUCLEAR CELL; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; SCANNING ELECTRON MICROSCOPY;

EID: 84923189825     PISSN: None     EISSN: 20796382     Source Type: Journal    
DOI: 10.3390/antibiotics3040509     Document Type: Article

References (38)

1. López, D.; Vlamakis, H.; Kolter, R. Biofilms. Cold Spring Harb. Perspect. Biol. 2010, 2, a000398.
2. De la Fuente-Núñez, C.; Reffuveille, F.; Fernández, L.; Hancock, R.E.W. Bacterial biofilm development as a multicellular adaptation: Antibiotic resistance and new therapeutic strategies. Curr. Opin. Microbiol. 2013, 16, 580-589.
3. Moreau-Marquis, S.; Stanton, B.A.; O'Toole, G.A. Pseudomonas aeruginosa biofilm formation in the cystic fibrosis airway. Pulm. Pharmacol. Ther. 2008, 21, 595-599.
4. Singh, P.K.; Schaefer, A.L.; Parsek, M.R.; Moninger, T.O.; Welsh, M.J.; Greenberg, E.P. Quorum-sensing signals indicate that cystic fibrosis lungs are infected with bacterial biofilms. Nature 2000, 407, 762-764.
5. Breidenstein, E.B.M.; de la Fuente-Núñez, C.; Hancock, R.E.W. Pseudomonas aeruginosa: All roads lead to resistance. Trends. Microbiol. 2011, 19, 419-426.
6. Hoffman, L.R.; D'Argenio, D.A.; MacCoss, M.J.; Zhang, Z.; Jones, R.A.; Miller, S.I. Aminoglycoside antibiotics induce bacterial biofilm formation. Nature 2005, 436, 1171-1175.
7. Linares, J.F.; Gustafsson, I.; Baquero, F.; Martinez, J.L. Antibiotics as intermicrobial signaling agents instead of weapons. Proc. Natl. Acad. Sci. USA 2006, 103, 19484-19489.
8. Wahba, A.H.; Darrell, J.H. The identification of atypical strains of Pseudomonas aeruginosa. J. Gen. Microbiol. 1965, 38, 329-342.
9. Stapper, A.P.; Narasimhan, G.; Ohman, D.E.; Barakat, J.; Hentzer, M.; Molin, S.; Kharazmi, A.; Høiby, N.; Mathee, K. Alginate production affects Pseudomonas aeruginosa biofilm development and architecture, but is not essential for biofilm formation. J. Med. Microbiol. 2004, 53, 679-690.
10. Leid, J.G.; Willson, C.J.; Shirtliff, M.E.; Hassett, D.J.; Parsek, M.R.; Jeffers, A.K. The exopolysaccharide alginate protects Pseudomonas aeruginosa biofilm bacteria from IFN-gamma-mediated macrophage killing. J. Immunol. 2005, 175, 7512-7518.
11. D'Argenio, D.A.; Calfee, M.W.; Rainey, P.B.; Pesci, E.C. Autolysis and autoaggregation in Pseudomonas aeruginosa colony morphology mutants. J. Bacteriol. 2002, 184, 6481-6489.
12. Häussler, S.; Ziegler, I.; Löttel, A.; von Götz, F.; Rohde, M.; Wehmhöhner, D.; Saravanamuthu, S.; Tümmler, B.; Steinmetz, I. Highly adherent small-colony variants of Pseudomonas aeruginosa in cystic fibrosis lung infection. J. Med. Microbiol. 2003, 52, 295-301.
13. Ikeno, T.; Fukuda, K.; Ogawa, M.; Honda, M.; Tanabe, T.; Taniguchi, H. Small and rough colony Pseudomonas aeruginosa with elevated biofilm formation ability isolated in hospitalized patients. Microbiol. Immunol. 2007, 51, 929-938.
14. Loutet, S.A.; Valvano, M.A. Extreme antimicrobial peptide and polymyxin B resistance in the genus Burkholderia. Front. Microbiol. 2011, 2, e159.
15. Mahenthiralingam, E.; Vandamme, P.; Campbell, M.E.; Henry, D.A.; Gravelle, A.M.; Wong, L.T.; Davidson, A.G.; Wilcox, P.G.; Nakielna, B.; Speert, D.P. Infection with Burkholderia cepacia complex genomovars in patients with cystic fibrosis: Virulent transmissible strains of genomovar III can replace Burkholderia multivorans. Clin. Infect. Dis. 2001, 33, 1469-1475.
16. Hancock, R.E.W.; Sahl, H.G. Antimicrobial and host-defense peptides as new anti-infective therapeutic strategies. Nat. Biotechnol. 2006, 24, 1551-1557.
17. Hilchie, A.L.; Wuerth, K.; Hancock, R.E.W. Immune modulation by multifaceted cationic host defense (antimicrobial) peptides. Nat. Chem. Biol. 2013, 9, 761-768.
18. Overhage, J.; Campisano, A.; Bains, M.; Torfs, E.C.; Rehm, B.H.; Hancock, R.E.W. Human host defense peptide LL-37 prevents bacterial biofilm formation. Infect. Immun. 2008, 76, 4176-4182.
19. Amer, L.S.; Bishop, B.M.; van Hoek, M.L. Antimicrobial and antibiofilm activity of cathelicidins and short, synthetic peptides against Francisella. Biochem. Biophys. Res. Commun. 2010, 396, 246-251.
20. Pompilio, A.; Scocchi, M.; Pomponio, S.; Guida, F.; di Primio, A.; Fiscarelli, E.; Gennaro, R.; di Bonaventura, G. Antibacterial and anti-biofilm effects of cathelicidin peptides against pathogens isolated from cystic fibrosis patients. Peptides 2011, 32, 1807-1814.
21. De la Fuente-Núñez, C.; Korolik, V.; Bains, M.; Nguyen, U.; Breidenstein, E.B.; Horsman, S.; Lewenza, S.; Burrows, L.; Hancock, R.E.W. Inhibition of bacterial biofilm formation and swarming motility by a small synthetic cationic peptide. Antimicrob. Agents Chemother. 2012, 56, 2696-2704.
22. De la Fuente-Núñez, C.; Reffuveille, F.; Haney, E.F.; Straus, S.K.; Hancock, R.E.W. Broad-spectrum anti-biofilm peptide that targets a cellular stress response. PLoS Pathog. 2014, 10, e1004152.
23. Feng, X.; Sambanthamoorthy, K.; Palys, T.; Paranavitana, C. The human antimicrobial peptide LL-37 and its fragments possess both antimicrobial and antibiofilm activities against multidrug-resistant Acinetobacter baumannii. Peptides 2013, 49, 131-137.
24. Hirt, H.; Gorr, S.U. Antimicrobial peptide GL13K is effective in reducing biofilms of Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 2013, 57, 4903-4910.
25. Zaïri, A.; Ferrières, L.; Latour-Lambert, P.; Beloin, C.; Tangy, F.; Ghigo, J.M.; Hani, K. In vitro activities of dermaseptins K4S4 and K4K20S4 against Escherichia coli, Staphylococcus aureus, and Pseudomonas aeruginosa planktonic growth and biofilm formation. Antimicrob Agents Chemother. 2014, 58, 2221-2228.
26. Gopal, R.; Kim, Y.G.; Lee, J.H.; Lee, S.K.; Chae, J.D.; Son, B.K.; Seo, C.H.; Park, Y. Synergistic effects and antibiofilm properties of chimeric peptides against multidrug-resistant Acinetobacter. baumannii strains. Antimicrob. Agents Chemother. 2014, 58, 1622-1629.
27. Reffuveille, F.; de la Fuente-Núñez, C.; Mansour, S.; Hancock, R.E.W. A broad-spectrum anti-biofilm peptide enhances antibiotic action against bacterial biofilms. Antimicrob. Agents Chemother. 2014, 58, 5363-5371.
28. Wieczorek, M.; Jenssen, H.; Kindrachuk, J.; Scott, W.R.; Elliott, M.; Hilpert, K.; Cheng, J.T.; Hancock, R.E.W.; Straus, S.K. Structural studies of a peptide with immune modulating and direct antimicrobial activity. Chem. Biol. 2010, 17, 970-980.
29. Achtman, A.H.; Pilat, S.; Law, C.W.; Lynn, D.J.; Janot, L.; Mayer, M.L.; Ma, S.; Kindrachuk, J.; Finlay, B.B.; Brinkman, F.S.; et al. Effective adjunctive therapy by an innate defense regulatory peptide in a pre-clinical model of severe malaria. Sci. Transl. Med. 2012, 4, 135ra64.
30. Rivas-Santiago, B.; Castañeda-Delgado, J.E.; Rivas Santiago, C.E.; Waldbrook, M.; González-Curiel, I.; León-Contreras, J.C.; Enciso-Moreno, J.A.; del Villar, V.; Mendez-Ramos, J.; Hancock, R.E.W.; et al. Ability of innate defence regulator peptides IDR-1002, IDR-HH2 and IDR-1018 to protect against Mycobacterium tuberculosis infections in animal models. PLoS One 2013, 8, e59119.
31. Rao, S.; Grigg, J. New insights into pulmonary inflammation in cystic fibrosis. Arch. Dis. Child. 2006, 91, 786-788.
32. Moore, R.A.; Hancock, R.E.W. Involvement of outer membrane of Pseudomonas cepacia in aminoglycoside and polymyxin resistance. Antimicrob. Agents Chemother. 1986, 30, 923-926.
33. Cherkasov, A.; Hilpert, K.; Jenssen, H.; Fjell, C.D.; Waldbrook, M.; Mullaly, S.C.; Volkmer, R.; Hancock, R.E.W. Use of artificial intelligence in the design of small peptide antibiotics effective against a broad spectrum of highly antibiotic-resistant superbugs. ACS Chem. Biol. 2009, 4, 65-74.
34. Shen, Y.; Qian, W.; Chung, C.; Olsen, I.; Haapasalo, M. Evaluation of the effect of two chlorhexidine preparations on biofilm bacteria in vitro: A three-dimensional quantitative analysis. J. Endod. 2009, 35, 981-985.
35. Bowdish, D.M.; Davidson, D.J.; Scott, M.G.; Hancock, R.E.W. Immunomodulatory activities of small host defense peptides. Antimicrob. Agents Chemother. 2005, 49, 1727-1732.
36. Benoit, M.R.; Conant, C.G.; Ionescu-Zanetti, C.; Schwartz, M.; Matin, A. New device for high-throughput viability screening of flow biofilms. Appl. Environ. Microbiol. 2010, 76, 4136-4142.
37. Shen, Y.; Stojicic, S.; Haapasalo, M. Antimicrobial efficacy of chlorhexidine against bacteria in biofilms at different stages of development. J. Endod. 2011, 37, 657-661.
38. Shen, Y.; Stojicic, S.; Haapasalo, M. Bacterial viability in starved and revitalized biofilms: Comparison of viability staining and direct culture. J. Endod. 2010, 36, 1820-1823.