Use of antimicrobial peptides against microbial biofilms: Advantages and limits

Current Medicinal Chemistry

Volumn 18, Issue 2, 2011, Pages 256-279

  Batoni, Giovanna ^a   Maisetta, Giuseppantonio ^a   Brancatisano, Franca Lisa ^a   Esin, Semih ^a   Campa, Mario ^a  

^a Dipartimento di Patologia Sperimentale Biotecnologie Mediche Infettivologia ed Epidemiologia   (Italy)

Author keywords

Antibiotic resistance; Antimicrobial peptides; Biofilm; Exopolysaccharides; Medical device; Peptidomimetics

Indexed keywords

ALPHA DEFENSIN; BETA DEFENSIN 1; BETA DEFENSIN 3; CATHELICIDIN ANTIMICROBIAL PEPTIDE LL 37; DERMASEPTIN; HISTATIN 5; HUMAN GROWTH HORMONE; IB 367; LACTOFERRIN; MAGAININ 1; MUCIN 7; NOVISPIRIN; OMIGANAN; ORITAVANCIN; POLYPEPTIDE ANTIBIOTIC AGENT; PROLINE RICH PROTEIN; TACHYPLESIN; UNCLASSIFIED DRUG;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL ARTHRITIS; BACTERIAL COLONIZATION; BACTERIAL LOAD; BIOFILM; CATHETER INFECTION; CENTRAL VENOUS CATHETER; CONTACT LENS; CYSTIC FIBROSIS; DRUG MECHANISM; ENDOCARDITIS; ENDOPHTHALMITIS; ENDOTRACHEAL TUBE; HEART VALVE; INTRAUTERINE CONTRACEPTIVE DEVICE; LUNG INFECTION; MICROBIAL BIOFILM; MINIMUM INHIBITORY CONCENTRATION; OTITIS MEDIA; PERIODONTAL DISEASE; PERIODONTITIS; PROSTATITIS; PSEUDOMONAS INFECTION; SINUSITIS; TREATMENT PLANNING; URINARY CATHETER; URINARY TRACT INFECTION;

ANTI-INFECTIVE AGENTS; ANTIMICROBIAL CATIONIC PEPTIDES; BIOFILMS; DRUG RESISTANCE, BACTERIAL; MICROBIAL SENSITIVITY TESTS; PEPTIDOMIMETICS; QUORUM SENSING;

EID: 78751493646     PISSN: 09298673     EISSN: None     Source Type: Journal    
DOI: 10.2174/092986711794088399     Document Type: Article

References (172)

1. Hancock, R. E.; Lehrer, R. Cationic peptides: a new source of antibiotics. Trends Biotechnol., 1998, 16, 82-88.
2. Hancock, R. E. Peptide antibiotics. Lancet, 1997, 349, 418-422.
3. Ganz, T. Defensins: antimicrobial peptides of innate immunity. Nat. Rev. Immunol., 2003, 3, 710-720. (Pubitemid 41070812)
4. Lehrer, R. I.; Ganz, T. Antimicrobial peptides in mammalian and insect host defence. Curr. Opin. Immunol., 1999, 11, 23-27.
5. Oyston, P. C.; Fox, M. A.; Richards, S. J.; Clark, G. C. Novel peptide therapeutics for treatment of infections. J. Med. Microbiol., 2009, 58, 977-987.
6. Harris, F.; Dennison, S. R.; Phoenix, D. A. Anionic antimicrobial peptides from eukaryotic organisms. Curr. Protein Pept. Sci., 2009, 10, 585-606.
7. Shai, Y. Mechanism of the binding, insertion and destabilization of phospholipid bilayer membranes by alpha-helical antimicrobial and cell non-selective membrane-lytic peptides. Biochim. Biophys. Acta, 1999, 1462, 55-70.
8. Brogden, K. A. Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nat. Rev. Microbiol., 2005, 3, 238-250.
9. Lai, Y.; Gallo, R. L. AMPed up immunity: how antimicrobial peptides have multiple roles in immune defense. Trends Immunol., 2009, 30, 131-141.
10. Maisetta, G.; Batoni, G.; Esin, S.; Florio, W.; Bottai, D.; Favilli, F.; Campa, M. In vitro bactericidal activity of human beta-defensin 3 against multidrug-resistant nosocomial strains. Antimicrob. Agents Chemother., 2006, 50, 806-809.
11. Nicolas, P. Multifunctional host defense peptides: intracellulartargeting antimicrobial peptides. FEBS J., 2009, 276, 6483-6496.
12. Holmberg, S. D.; Solomon, S. L.; Blake, P. A. Health and economic impacts of antimicrobial resistance. Rev. Infect. Dis., 1987, 9, 1065-1078.
13. Severin, A.; Tabei, K.; Tenover, F.; Chung, M.; Clarke, N.; Tomasz, A. High level oxacillin and vancomicycin resistance and altered cell wall composition in Staphylococcus aureus carrying the staphylococcal mecA and the enteroccoccal van A gene complex. J. Biol. Chem., 2004, 30, 3398-3407.
14. Pablos-Méndez, A.; Raviglione, M. C.; Laszlo, A.; Binkin, N.; Rieder, H. L.; Bustreo, F.; Cohn, D. L.; Lambregts-van Weezenbeek, C. S.; Kim, S. J.; Chaulet, P.; Nunn, P. Global surveillance for antituberculosis-drug resistance, 1994-1997. World Health Organization-International Union against tuberculosis and lung disease working group on anti-tuberculosis drug resistance surveillance. N. Engl. J. Med., 1998, 338, 1641-1649.
15. Jones, R. N. Contemporary antimicrobial susceptibility patterns of bacterial pathogens commonly associated with febrile patients with neutropenia. Clin. Infect. Dis., 1999, 29, 495-502.
16. Hancock, R. E. The therapeutic potential of cationic peptides. Expert Opin. Investig Drugs, 1998, 7, 167-174.
17. Maisetta, G.; Mangoni, M. L.; Esin, S.; Pichierri, G.; Capria, A. L.; Brancatisano, F. L.; Di Luca, M.; Barnini, S.; Barra, D.; Campa, M.; Batoni, G. In vitro bactericidal activity of the N-terminal fragment of the frog peptide esculentin-1b (Esc 1-18) in combination with conventional antibiotics against Stenotrophomonas maltophilia. Peptides, 2009, 30, 1622-1626.
18. Jerala, R.; Porro, M. Endotoxin neutralizing peptides. Curr. Top. Med. Chem., 2004, 4, 1173-1184.
19. Mangoni, M. L.; Maisetta, G.; Di Luca, M.; Gaddi, L. M.; Esin, S.; Florio, W.; Brancatisano, F. L.; Barra, D.; Campa, M.; Batoni, G. Comparative analysis of the bactericidal activities of amphibian peptide analogues against multidrug-resistant nosocomial bacterial strains. Antimicrob. Agents Chemother., 2008, 52, 85-91.
20. Baranska-Rybak, W.; Sonesson, A.; Nowicki, R.; Schmidtchen, A. Glycosaminoglycans inhibit the antibacterial activity of LL-37 in biological fluids. J. Antimicrob. Chemother., 2006, 57, 260-265.
21. Maisetta, G.; Batoni, G.; Esin, S.; Raco, G.; Bottai, D.; Favilli, F.; Florio, W.; Campa, M. Susceptibility of Streptococcus mutans and Actinobacillus actnomycetemcomitans to bactericidal activity of human beta defensin 3 in biological fluids. Antimicrob. Agents Chemother., 2005, 49, 1245-1248.
22. Eckert, R.; McHardy, I.; Yarbrough, D. K.; He, J.; Qi, F.; Anderson, M. H.; Shi, W. Stability and activity in sputum of G10KHc, a potent anti-Pseudomonas antimicrobial peptide. Chem. Biol. Drug. Des., 2007, 70, 456-460.
23. Batoni, G.; Maisetta, G.; Esin, S.; Campa, M. Human betadefensin-3: a promising antimicrobial peptide. Mini Rev. Med. Chem., 2006, 6, 1063-1073.
24. Felgentreff, K.; Beisswenger, C.; Griese, M.; Gulder, T.; Bringmann, G.; Bals, R. The antimicrobial peptide cathelicidin interacts with airway mucus. Peptides, 2006, 27, 3100-3106.
25. Bowdish, D. M.; Davidson, D. J.; Hancock, R. E. A re-evaluation of the role of host defence peptides in mammalian immunity. Curr. Protein Pept. Sci., 2005, 6, 35-51.
26. Svenson, J.; Brandsdal, B. O.; Stensen, W.; Svendsen, J. S. Albumin binding of short cationic antimicrobial micropeptides and its influence on the in vitro bactericidal effect. J. Med. Chem., 2007, 50, 3334-3339.
27. Yadava, P.; Zhang, C.; Sun, J.; Hughes, J. A. Antimicrobial activities of human beta-defensins against Bacillus species. Int. J. Antimicrob. Agents, 2006, 28, 132-137.
28. Maisetta, G.; Di Luca, M.; Esin, S.; Florio, W.; Brancatisano, F. L.; Bottai, D.; Campa, M.; Batoni, G. Evaluation of the inhibitory effects of human serum components on bactericidal activity of human beta defensin 3. Peptides, 2008, 29, 1-6.
29. Kraus, D.; Peschel, A. Molecular mechanisms of bacterial resistance to antimicrobial peptides. Curr. Top. Microbiol. Immunol., 2006, 306, 231-250. (Pubitemid 47400324)
30. Zasloff, M. Antimicrobial peptides of multicellular organisms. Nature, 2002, 415, 389-395.
31. Easton, D. M.; Nijnik, A.; Mayer, M. L.; Hancock, R. E. Potential of immunomodulatory host defense peptides as novel anti-infectives. Trends Biotechnol., 2009, 27, 582-590.
32. Donlan, R. M.; Costerton, J. W. Biofilms: survival mechanisms of clinically relevant microorganisms. Clin. Microbiol. Rev., 2002, 15, 167-193.
33. Donlan, R. M. Biofilms: microbial life on surfaces. Emerg. Infect. Dis., 2002, 8, 881-890.
34. Davey, M. E.; O'Toole, G. A. Microbial biofilms: from ecology to molecular genetics. Microbiol. Mol. Biol. Rev., 2000, 64, 847-867.
35. Costerton, J. W.; Lewandowski, Z.; Caldwell, D. E.; Korber, D. R.; Lappin-Scott, H. M. Microbial biofilms. Annu. Rev. Microbiol., 1995, 49, 711-745.
36. Habash, M.; Reid, G. Microbial biofilms: their development and significance for medical device-related infections. J. Clin. Pharmacol., 1999, 39, 887-898.
37. Agarwal, A.; Singh, K. P.; Jain, A. Medical significance and management of staphylococcal biofilm. FEMS Immunol. Med. Microbiol., 2010, 58, 147-160.
38. Singh R.; Paul, D.; Jain, R. K. Biofilms: implications in bioremediation. Trends Microbiol., 2006, 14, 389-397.
39. Dominic, R. M.; Shenoy, S.; Baliga, S. Candida biofilms in medical devices: evolving trends. Kathmandu Univ. Med. J. (KUMJ), 2007, 5, 431-436.
40. Schembri, M. A.; Kjaergaard, K.; Klemm, P. Global gene expression in Escherichia coli biofilms. Mol. Microbiol., 2003, 48, 253-267.
41. Schoolnik, G. K.; Voskuil, M. I.; Schnappinger, D.; Yildiz, F. H.; Meibom, K.; Dolganov, N. A.; Wilson, M. A.; Chong, K. H. Whole genome DNA microarray expression analysis of biofilm development by Vibrio cholerae O1 E1 Tor. Methods Enzymol., 2001, 336, 3-18.
42. Beenken, K. E.; Dunman, P. M.; McAleese, F.; Macapagal, D.; Murphy, E.; Projan, S. J.; Blevins, J. S.; Smeltzer, M. S. Global gene expression in Staphylococcus aureus biofilms. J. Bacteriol., 2004, 186, 4665-4684. (Pubitemid 38891030)
43. Beloin, C.; Ghigo, J. M. Finding gene-expression patterns in bacterial biofilms. Trends Microbiol., 2005, 13, 16-19.
44. Kuhn, D. M.; George, T.; Chandra, J.; Mukherjee, P. K.; Ghannoum, M. A. Antifungal susceptibility of Candida biofilms: unique efficacy of amphotericin B lipid formulations and echinocandins. Antimicrob. Agents Chemother., 2002, 46, 1773-1780.
45. Mukherjee, P. K.; Chandra, J. Candida biofilm resistance. Drug Resist. Updat., 2004, 7, 301-309.
46. Mah, T. F.; O'Toole, G. A. Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol., 2001, 9, 34-39.
47. Molin, S.; Tolker-Nielsen, T. Gene transfer occurs with enhanced efficiency in biofilms and induces enhanced stabilisation of the biofilm structure. Curr. Opin. Biotechnol., 2003, 14, 255-261.
48. Singh, R.; Ray, P.; Das, A.; Sharma, M. Role of persisters and small-colony variants in antibiotic resistance of planktonic and biofilm-associated Staphylococcus aureus: an in vitro study. J. Med. Microbiol., 2009, 58, 1067-1073.
49. Keren, I.; Shah, D.; Spoering, A.; Kaldalu, N.; Lewis, K. Specialized persister cells and the mechanism of multidrug tolerance in Escherichia coli. J. Bacteriol., 2004, 186, 8172-8180.
50. La Fleur, M. D.; Kumamoto, C. A.; Lewis, K. Candida albicans biofilms produce antifungal-tolerant persister cells. Antimicrob. Agents Chemother., 2006, 50, 3839-3846.
51. Lewis, K. Multidrug tolerance of biofilms and persister cells. Curr. Top. Microbiol. Immunol., 2008;322, 107-131.
52. Stewart, P. S. Multicellular resistance: biofilms. Trends Microbiol., 2001, 9, 204.
53. Kharazmi, A. Mechanisms involved in the evasion of the host defence by Pseudomonas aeruginosa. Immunol. Lett., 1991, 30, 201-205.
54. Irie, Y.; Parsek, M. R. Quorum sensing and microbial biofilms. Curr. Top. Microbiol. Immunol., 2008, 322, 67-84.
55. Janssens, J. C.; De Keersmaecker, S. C.; De Vos, D. E.; Vanderleyden, J. Small molecules for interference with cell-cellcommunication systems in Gram-negative bacteria. Curr. Med. Chem., 2008, 15, 2144-2156.
56. Czárán, T.; Hoekstra, R. F. Microbial communication, cooperation and cheating: quorum sensing drives the evolution of cooperation in bacteria. PLoS One, 2009, 4, e6655.
57. Abraham, W. R. Controlling biofilms of gram-positive pathogenic bacteria. Curr. Med. Chem., 2006, 13, 1509-1524.
58. Davies, D. G.; Parsek, M. R.; Pearson, J. P.; Iglewski, B. H.; Costerton, J. W.; Greenberg, E. P. The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science, 1998, 280, 295-298.
59. Sakuragi, Y.; Kolter, R. Quorum-sensing regulation of the biofilm matrix genes (pel) of Pseudomonas aeruginosa. J. Bacteriol., 2007, 189, 5383-5386.
60. Zhu, J.; Mekalanos, J. J. Quorum sensing-dependent biofilms enhance colonization in Vibrio cholerae. Dev. Cell., 2003, 5, 647-656.
61. Alem, M. A.; Oteef, M. D.; Flowers, T. H.; Douglas, L. J. Production of tyrosol by Candida albicans biofilms and its role in quorum sensing and biofilm development. Eukaryot. Cell., 2006, 5, 1770-1779.
62. Atkinson, S.; Williams, P. Quorum sensing and social networking in the microbial world. J. R. Soc. Interface, 2009, 6, 959-978.
63. Davies, D. Understanding biofilm resistance to antibacterial agents. Nat. Rev. Drug Discov., 2003, 2, 114-122.
64. Hall-Stoodley, L.; Stoodley, P. Evolving concepts in biofilm infections. Cell. Microbiol., 2009, 11, 1034-1043.
65. Rioufol, C.; Devys, C.; Meunier, G.; Perraud, M.; Goullet, D. Quantitative determination of endotoxins released by bacterial biofilms. J. Hosp. Infect., 1999, 43, 203-209.
66. Vincent, F. C.; Tibi, A. R.; Darbord, J. C. A bacterial biofilm in a hemodialysis system. Assessment of disinfection and crossing of endotoxin. ASAIO Trans., 1989, 35, 310-313.
67. Cappelli, G.; Ballestri, M.; Perrone, S.; Ciuffreda, A.; Inguaggiato, P.; Albertazzi, A. Biofilms invade nephrology: effects in hemodialysis. Blood Purif., 2000, 18, 224-230.
68. Estrela, A. B.; Heck, M. G.; Abraham, W. R. Novel approaches to control biofilm infections. Curr. Med. Chem., 2009, 16, 1512-1530.
69. Wagner, V. E.; Iglewski, B. H. P. aeruginosa biofilms in CF infection. Clin. Rev. Allergy Immunol., 2008, 35, 124-134.
70. Poole, K. Aminoglycoside resistance in Pseudomonas aeruginosa. Antimicrob. Agents Chemother., 2005, 49, 479-487.
71. Burton, M. F.; Steel, P. G. The chemistry and biology of LL-37. Nat. Prod. Rep., 2009, 26, 1572-1584.
72. Nijnik, A.; Hancock, R. E. The roles of cathelicidin LL-37 in immune defences and novel clinical applications. Curr. Opin. Hematol., 2009, 16, 41-47.
73. Overhage, J.; Campisano, A.; Bains, M.; Torfs, E. C.; Rehm, B. H.; Hancock, R. E. Human host defense peptide LL-37 prevents bacterial biofilm formation. Infect. Immun., 2008, 76, 4176-4182.
74. Singh, P. K. Iron sequestration by human lactoferrin stimulates P. aeruginosa surface motility and blocks biofilm formation. Biometals, 2004, 17, 267-270.
75. Eckert, R.; Qi, F.; Yarbrough, D. K.; He, J.; Anderson, M. H.; Shi, W. Adding selectivity to antimicrobial peptides: rational design of a multidomain peptide against Pseudomonas spp. Antimicrob. Agents Chemother., 2006, 50, 1480-1488.
76. Eckert, R.; He, J.; Yarbrough, D. K.; Qi, F.; Anderson, M. H.; Shi, W. Targeted killing of Streptococcus mutans by a pheromoneguided "smart" antimicrobial peptide. Antimicrob. Agents Chemother., 2006, 50, 3651-3657.
77. Eckert, R.; Brady, K. M.; Greenberg, E. P.; Qi, F.; Yarbrough, D. K.; He, J.; McHardy, I.; Anderson, M. H.; Shi, W. Enhancement of antimicrobial activity against Pseudomonas aeruginosa by coadministration of G10KHc and tobramycin. Antimicrob. Agents Chemother., 2006, 50, 3833-3838.
78. Beloin, C.; Roux, A.; Ghigo, J. M. Structural effects on inhibition of planktonic growth and biofilm formation of Escherichia coli by Trp/Arg containing antimicrobial peptides. Curr. Top. Microbiol. Immunol., 2008, 322, 249-290.
79. Kaper, J. B.; Nataro, J. P.; Mobley, H. L. Pathogenic Escherichia coli. Nat. Rev. Microbiol., 2004, 2, 123-140.
80. Trautner, B. W.; Darouiche, R. O. Role of biofilm in catheterassociated urinary tract infection. Am. J. Infect. Control., 2004, 32, 177-183.
81. Hunstad, D. A.; Justice, S. S. Intracellular lifestyles and immune evasion strategies of uropathogenic Escherichia coli. Annu. Re.v Microbiol., 2010, 64, 203-221.
82. Soto, S. M.; Smithson, A.; Horcajada, J. P.; Martinez, J. A.; Mensa, J. P.; Vila, J. Implication of biofilm formation in the persistence of urinary tract infections caused by uropathogenic Escherichia coli. Clin. Microbiol. Infect., 2006, 12, 1034-1036.
83. Kanamaru, S.; Kurazono, H.; Terai, A.; Monden, K.; Kumon, H.; Mizunoe, Y.; Ogawa, O.; Yamamoto, S. Increased biofilm formation in Escherichia coli isolated from acute prostatitis. Int. J. Antimicrob. Agents, 2006, Suppl 1, S21-25.
84. Hou, S.; Liu, Z.; Young, A. W.; Mark, S. L.; Kallenbach, N. R.; Ren, D. Effects of Trp-and Arg-containing antimicrobial-peptide structure on inhibition of Escherichia coli planktonic growth and biofilm formation. Appl. Environ. Microbiol., 2010, 76, 1967-1974.
85. Tam, J. P.; Lu, Y. A.; Yang, J. L. Antimicrobial dendrimeric peptides. Eur. J. Biochem., 2002, 269, 923-932.
86. Hou, S.; Zhou, C.; Liu, Z.; Young, A. W.; Shi, Z.; Ren, D.; Kallenbach, N. R. Antimicrobial dendrimer active against Escherichia coli biofilms. Bioorg. Med. Chem. Lett., 2009, 19, 5478-5481.
87. Otto, M. Staphylococcal biofilms. Human cathelicidin peptide LL-37 inhibits both attachment capability and biofilm formation of Staphylococcus epidermidis. Curr. Top. Microbiol. Immunol., 2008, 322, 207-229.
88. Hell, É.; Giske, C. G.; Nelson, A.; Römling, U.; Marchini, G. Human cathelicidin peptide LL37 inhibits both attachment capability and biofilm formation of Staphylococcus epidermidis. Lett. Appl. Microbiol., 2010, 50, 211-215.
89. Belley, A.; Neesham-Grenon, E.; McKay, G.; Arhin, F. F.; Harris, R.; Beveridge, T.; Parr, T. R. Jr.; Moeck, G. Oritavancin kills stationary-phase and biofilm Staphylococcus aureus cells in vitro. Antimicrob. Agents Chemother., 2009, 53, 918-925.
90. Allen, N. E.; Nicas, T. I. Mechanism of action of oritavancin and related glycopeptide antibiotics. FEMS Microbiol. Rev., 2003, 26, 511-532.
91. Flemming, K.; Klingenberg, C.; Cavanagh, J. P.; Sletteng, M.; Stensen, W.; Svendsen, J. S.; Flaegstad, T. High in vitro antimicrobial activity of synthetic antimicrobial peptidomimetics against staphylococcal biofilms. J. Antimicrob. Chemother., 2009, 63, 136-145.
92. Loesche, W. Dental caries and periodontitis: contrasting two infections that have medical implications. Infect. Dis. Clin. North Am., 2007, 21, 471-502.
93. Schaudinn, C.; Gorur, A.; Keller, D.; Sedghizadeh, P. P.; Costerton J. W. Periodontitis: an archetypical biofilm disease. J. Am. Dent. Assoc., 2009, 140, 978-986.
94. Filoche, S.; Wong, L.; Sissons, C. H. Oral biofilms: emerging concepts in microbial ecology. J. Dent. Res., 2010, 89, 8-18.
95. Devine, D. A.; Cosseau, C. Host defense peptides in the oral cavity. Adv. Appl. Microbiol., 2008, 63, 281-322.
96. Arslan, S. Y.; Leung, K. P.; Wu, C. D. The effect of lactoferrin on oral bacterial attachment. Oral. Microbiol. Immunol., 2009, 24, 411-416.
97. Scannapieco, F. A. Saliva-bacterium interactions in oral microbial ecology. Crit. Rev. Oral Biol. Med., 1994, 5, 203-248.
98. Drobni, M.; Li, T., Krüger, C.; Loimaranta, V.; Kilian, M.; Hammarström, L.; Jörnvall, H.; Bergman, T.; Strömberg, N. Hostderived pentapeptide affecting adhesion, proliferation, and local pH in biofilm communities composed of Streptococcus and Actinomyces species. Infect. Immun., 2006, 74, 6293-6299.
99. Lee, I. H.; Cho, Y.; Lehrer, R. I. Effects of pH and salinity on the antimicrobial properties of clavanins. Infect. Immun., 1997, 65, 2898-2903.
100. van Kan, E. J.; Demel, R. A.; van der Bent, A.; de Kruiff, B. The role of the abundant phenylalanines in the mode of action of the antimicrobial peptide clavanin. Biochim. Biophys. Acta, 2003, 1615, 84-92.
101. Li, L.; He, J.; Eckert, R.; Yarbrough, D.; Lux, R.; Anderson, M.; Shi, W. Design and characterization of an acid-activated antimicrobial peptide. Chem. Biol. Drug Des., 2010, 75, 127-132.
102. Dashper, S. G.; O'Brien-Simpson, N. M.; Cross, K. J.; Paolini, R. A.; Hoffmann B.; Catmull, D. V.; Malkoski, M.; Reynolds, E. C. Divalent metal cations increase the activity of the antimicrobial Peptide kappacin. Antimicrob. Agents Chemother., 2005, 49, 2322-2328.
103. Wei, G. X.; Campagna, A. N.; Bobek, L. A. Effect of MUC7 peptides on the growth of bacteria and on Streptococcus mutans biofilm. J. Antimicrob. Chemother., 2006, 57, 1100-1109.
104. Leung, K. P.; Crowe, T. D.; Abercrombie, J. J.; Molina, C. M.; Bradshaw, C. J.; Jensen, C. L.; Luo, Q.; Thompson, G. A. Control of oral biofilm formation by an antimicrobial decapeptide. J. Dent. Res. 2005, 84, 1172-1177.
105. Leung, K. P.; Abercrombie, J. J.; Campbell, T. M.; Gilmore, K. D.; Bell, C. A.; Faraj, J. A.; De Luca, P. P. Antimicrobial peptides for plaque control. Adv. Dent. Res., 2009, 21, 57-62.
106. Nicolas, P.; El Amri, C. The dermaseptin superfamily: a genebased combinatorial library of antimicrobial peptides. Biochim. Biophys. Acta, 2009, 1788, 1537-1550.
107. Altman, H.; Steinberg, D.; Porat, Y.; Mor, A.; Fridman, D.; Friedman, M.; Bachrach, G. In vitro assessment of antimicrobial peptides as potential agents against several oral bacteria. J. Antimicrob. Chemother., 2006, 58, 198-201.
108. Porat, Y.; Marynka, K.; Tam, A.; Steinberg, D.; Mor, A. Acylsubstituted dermaseptin S4 derivatives with improved bactericidal properties, including on oral microflora. Antimicrob. Agents Chemother., 2006, 50, 4153-4160.
109. Beckloff, N.; Laube, D.; Castro, T.; Furgang, D.; Park, S.; Perlin, D.; Clements, D.; Tang, H.; Scott, R. W.; Tew, G. N. Activity of an antimicrobial peptide mimetic against planktonic and biofilm cultures of oral pathogens. Antimicrob. Agents Chemother., 2007, 51, 4125-4132.
110. Edgerton, M.; Koshlukova, S. E. Salivary histatin 5 and its similarities to the other antimicrobial proteins in human saliva. Adv. Dent. Res., 2000, 14, 16-21.
111. Li, X. S.; Sun, J. N.; Okamoto-Shibayama, K.; Edgerton, M. Candida albicans cell wall ssa proteins bind and facilitate import of salivary histatin 5 required for toxicity. J. Biol. Chem., 2006, 281, 22453-22463.
112. Koshlukova, S. E.; Araujo, M. W.; Baev, D.; Edgerton, M. Released ATP is an extracellular cytotoxic mediator in salivary histatin 5-induced killing of Candida albicans. Infect. Immun., 2000, 68, 6848-6856.
113. Pusateri, C. R.; Monaco, E. A.; Edgerton, M. Sensitivity of Candida albicans biofilm cells grown on denture acrylic to antifungal proteins and chlorhexidine. Arch. Oral. Biol., 2009, 54, 588-594.
114. Mitchell, T. G.; Perfect, J. R. Cryptococcosis in the era of AIDS-100 years after the discovery of Cryptococcus neoformans. Clin. Microbiol. Rev., 1995, 8, 515-548.
115. Martinez, L. R.; Casadevall, A. Cryptococcus neoformans cells in biofilms are less susceptible than planktonic cells to antimicrobial molecules produced by the innate immune system. Infect. Immun., 2006, 74, 6118-6123.
116. Burrows, L. L.; Stark, M.; Chan, C.; Glukhov, E.; Sinnadurai, S.; Deber, C. M. Activity of novel non-amphipathic cationic antimicrobial peptides against Candida species. J. Antimicrob. Chemother., 2006, 57, 899-907.
117. Cheng, R. P.; Gellman, S. H.; De Grado, W. F. Beta-peptides: from structure to function. Chem. Rev., 2001, 10, 3219-3232.
118. Karlsson, A. J.; Pomerantz, W. C.; Weisblum, B.; Gellman, S. H.; Palecek, S. P. Antifungal activity from 14-helical beta-peptides. J. Am. Chem. Soc., 2006, 128, 12630-12631.
119. Karlsson, A. J.; Pomerantz, W. C.; Neilsen, K. J.; Gellman, S. H.; Palecek, S. P. Effect of sequence and structural properties on 14-helical beta-peptide activity against Candida albicans planktonic cells and biofilms. ACS Chem. Biol., 2009, 4, 567-579.
120. Jones, C. A. Central venous catheter infection in adults in acute hospital settings. Br. J. Nurs., 2006, 15, 364-368.
121. Viale, P.; Stefani, S. Vascular catheter-associated infections: a microbiological and therapeutic update. J. Chemother., 2006, 18, 235-249.
122. Cirioni, O.; Giacometti, A.; Ghiselli, R.; Kamysz, W.; Orlando, F.; Mocchegiani, F.; Silvestri, C.; Licci, A.; Chiodi, L.; Lukasiak, J.; Saba, V.; Scalise, G. Citropin 1.1-treated central venous catheters improve the efficacy of hydrophobic antibiotics in the treatment of experimental staphylococcal catheter-related infection. Peptides, 2006, 27, 1210-1216. (Pubitemid 43767009)
123. Fernandez, D. I.; Gehman, J. D.; Separovic, F. Membrane interactions of antimicrobial peptides from Australian frogs. Biochim. Biophys. Acta., 2009, 1788, 1630-1638.
124. Cirioni, O.; Giacometti, A.; Ghiselli, R.; Bergnach, C.; Orlando, F.; Mocchegiani, F.; Silvestri, C.; Licci, A.; Skerlavaj, B.; Zanetti, M.; Saba, V.; Scalise, G. Pre-treatment of central venous catheters with the cathelicidin BMAP-28 enhances the efficacy of antistaphylococcal agents in the treatment of experimental catheter-related infection. Peptides, 2006, 27, 2104-2110. (Pubitemid 44189607)
125. Ghiselli, R.; Giacometti, A.; Cirioni, O.; Mocchegiani, F.; Silvestri, C.; Orlando, F.; Kamysz, W.; Licci, A.; Nadolski, P.; Della Vittoria, A.; Lukasiak, J.; Scalise, G.; Saba, V. Pretreatment with the protegrin IB-367 affects Gram-positive biofilm and enhances the therapeutic efficacy of linezolid in animal models of central venous catheter infection. JPEN J. Parenter. Enteral. Nutr., 2007, 31, 463-468.
126. Sader, H. S.; Fedler, K. A.; Rennie, R. P.; Stevens, S.; Jones, R. N. Omiganan pentahydrochloride (MBI 226), a topical 12-amino-acid cationic peptide: spectrum of antimicrobial activity and measurements of bactericidal activity. Antimicrob. Agents Chemother., 2004, 48, 3112-3118.
127. Fritsche, T. R.; Rhomberg, P. R.; Sader, H. S.; Jones, R. N. A Antimicrobial activity of omiganan pentahydrochloride against contemporary fungal pathogens responsible for catheter-associated infections. J. Antimicrob. Chemother., 2008, 61, 1092-1098.
128. Fritsche, T. R.; Rhomberg, P. R.; Sader, H. S.; Jones, R. N. Antimicrobial activity of omiganan pentahydrochloride against contemporary fungal pathogens responsible for catheter-associated infections. Antimicrob. Agents Chemother., 2008, 52, 1187-1189.
129. Rubinchik, E.; Dugourd, D.; Algara, T.; Pasetka, C.; Friendland, H. D. Antimicrobial and antifungal activities of a novel cationic antimicrobial peptide, omiganan, in experimental skin colonisation models. Int. J. Antimicrob. Agents., 2009, 34, 457-461.
130. Balaban, N.; Gov, Y.; Giacometti, A.; Cirioni, O.; Ghiselli, R.; Mocchegiani, F.; Orlando, F.; D'Amato, G.; Saba, V.; Scalise, G.; Bernes, S.; Mor, A. A chimeric peptide composed of a dermaseptin derivative and an RNA III-inhibiting peptide prevents graftassociated infections by antibiotic-resistant staphylococci. Antimicrob. Agents Chemother., 2004, 48, 2544-2550.
131. Balaban, N.; Giacometti, A.; Cirioni, O.; Gov, Y.; Ghiselli, R.; Mocchegiani, F.; Viticchi, C.; Del Prete, M. S.; Saba, V.; Scalise, G.; Dell'Acqua, G. Use of the quorum-sensing inhibitor RNAIII-inhibiting peptide to prevent biofilm formation in vivo by drugresistant Staphylococcus epidermidis. J. Infect. Dis., 2003, 187, 625-630.
132. Giacometti, A.; Cirioni, O.; Gov, Y.; Ghiselli, R.; Del Prete, M. S.; Mocchegiani, F.; Saba, V.; Orlando, F.; Scalise, G.; Balaban, N.; Dell'Acqua, G. RNA III inhibiting peptide inhibits in vivo biofilm formation by drug-resistant Staphylococcus aureus. Antimicrob. Agents Chemother., 2003, 47, 1979-1983.
133. Minardi, D.; Ghiselli, R.; Cirioni, O.; Giacometti, A.; Kamysz, W.; Orlando, F.; Silvestri, C.; Parri, G.; Kamysz, E.; Scalise, G.; Saba, V.; Giovanni, M. The antimicrobial peptide tachyplesin III coated alone and in combination with intraperitoneal piperacillintazobactam prevents ureteral stent Pseudomonas infection in a rat subcutaneous pouch model. Peptides, 2007, 28, 2293-2298.
134. Nakamura, T.; Furunaka, H.; Miyata, T.; Tokunaga, F.; Muta, T.; Iwanaga, S.; Niwa, M.; Takao, T.; Shimonishi, Y. Tachyplesin, a class of antimicrobial peptide from the hemocytes of the horseshoe crab (Tachypleus tridentatus). Isolation and chemical structure. J. Biol. Chem., 1988, 263, 16709-16713.
135. Cirioni, O.; Giacometti, A.; Kamysz, W.; Silvestri, C.; Riva, A.; Della Vittoria, A.; Abbruzzetti, A.; Lukasiak, J.; Scalise, G. In vitro activities of tachyplesin III against Pseudomonas aeruginosa. Peptides, 2007, 4, 747-751.
136. Shukla, A.; Fleming, K. E.; Chuang, H. F.; Chau, T. M.; Loose, C. R.; Stephanopoulos, G. N. Hammond, P. T. Controlling the release of peptide antimicrobial agents from surfaces. Biomaterials, 2010, 31, 2348-2357.
137. Khoo, X.; Hamilton P.; O'Toole, G. A.; Snyder, B. D.; Kenan, D. J.; Grinstaff M. W. Directed assembly of PEGylated-peptide coatings for infection-resistant titanium metal. J. Am. Chem. Soc., 2009, 131, 10992-10997.
138. Conway, S. P.; Brownlee, K. G.; Denton, M.; Peckham, D. G. Antibiotic treatment of multidrug-resistant organisms in cystic fibrosis. Am. J. Respir. Med., 2003, 2, 321-332.
139. Song, Z.; Wu, H.; Mygind, P.; Raventos, D.; Sonksen, C.; Kristensen, H. H.; Hoiby, N. Effects of intratracheal administration of novispirin G10 on a rat model of mucoid Pseudomonas aeruginosa lung infection. Antimicrob. Agents Chemother., 2005, 49, 3868-3874.
140. Steinstraesser, L.; Tack, B. F.; Waring, A. J.; Hong, T.; Boo, L. M.; Fan, M. H.; Remick, D. I.; Su, G. L.; Lehrer, R. I.; Wang, S. C. Activity of novispirin G10 against Pseudomonas aeruginosa in vitro and in infected burns. Antimicrob. Agents Chemother., 2002, 46, 1837-1844.
141. Chennupati, S. K.; Chiu, A. G.; Tamashiro, E.; Banks C. A.; Cohen, M. B.; Bleier, B. S.; Kofonow, J. M.; Tam, E.; Cohen, N. A. Effects of an LL-37-derived antimicrobial peptide in an animal model of biofilm Pseudomonas sinusitis. Am. J. Rhinol. Allergy, 2009, 23, 46-51.
142. Johansson, J.; Gudmundsson, G. H.; Rottenberg, M. E.; Berndt, K. D.; Agerberth B. Conformation-dependent antibacterial activity of the naturally occurring human peptide LL-37. J. Biol. Chem., 1998, 273, 3718-3724.
143. Niyonsaba, F.; Iwabuchi, K.; Someya, A.; Hirata, M.; Matsuda, H.; Ogawa, H.; Nagaoka, I. A cathelicidin family of human antibacterial peptide LL-37 induces mast cell chemotaxis. Immunology, 2002, 106, 20-26.
144. Nell, M. J.; Tjabringab, G. S.; Wafelmanc, A. R.; Verrijkd, R.; Hiemstrab, P. S.; Drijfhoute, J. W.; Grote, J. J. Development of novel LL-37 derived antimicrobial peptides with LPS and LTA neutralizing and antimicrobial activities for therapeutic application. Peptides, 2006, 27, 649-660.
145. Otto, M. Bacterial evasion of antimicrobial peptides by biofilm formation. Curr. Top. Microbiol. Immunol., 2006, 306, 251-258.
146. Gacesa, P. Bacterial alginate biosynthesis-recent progress and future prospects. Microbiology, 1998, 144, 1133-1143.
147. Evans, L. R.; Linker, A. Production and characterization of the slime polysaccharide of Pseudomonas aeruginosa. J. Bacteriol., 1973, 116, 915-924.
148. Gordon, C. A.; Hodges, N. A.; Marriott, C. Antibiotic interaction and diffusion through alginate and exopolysaccharide of cystic fibrosis-derived Pseudomonas aeruginosa. J. Antimicrob. Chemother., 1988, 22, 667-674.
149. Nichols, W. W.; Dorrington, S. M.; Slack, M. P.; Walmsley, H. L. Inhibition of tobramycin diffusion by binding to alginate. Antimicrob. Agents Chemother., 1988, 32, 518-523.
150. Chan, C.; Burrows, L. L.; Deber, C. M. Helix induction in antimicrobial peptides by alginate in biofilms. J. Biol. Chem., 2004, 279, 38749-38754.
151. Kuo, H. H.; Chan, C.; Burrows, L. L.; Deber, C. M. Hydrophobic interactions in complexes of antimicrobial peptides with bacterial polysaccharides. Chem. Biol. Drug Des., 2007, 69, 405-412.
152. Chan, C.; Burrows, L. L.; Deber, C. M. J. Alginate as an auxiliary bacterial membrane: binding of membrane-active peptides by polysaccharides. Peptid. Res., 2005, 65, 343-351.
153. Mack, D.; Fischer, W.; Krokotsch, A.; Leopold, K.; Hartmann, R.; Egge, H.; Laufs, R. The intercellular adhesin involved in biofilm accumulation of Staphylococcus epidermidis is a linear beta-1, 6-linked glucosaminoglycan: purification and structural analysis. J. Bacteriol., 1996, 178, 175-183.
154. Vuong, C.; Voyich, J. M.; Fischer, E. R.; Braughton, K. R.; Whitney, A. R.; De Leo, F. R.; Otto, M. Polysaccharide intercellular adhesin (PIA) protects Staphylococcus epidermidis against major components of the human innate immune system. Cell. Microbiol., 2004, 6, 269-275.
155. Vuong, C.; Kocianova, S.; Voyich, J. M.; Yao, Y.; Fischer, E. R.; De Leo, F. R.; Otto, M. A crucial role for exopolysaccharide modification in bacterial biofilm formation, immune evasion, and virulence. J. Biol. Chem., 2004, 279, 54881-54886.
156. Erratum in: J. Biol. Chem., 2005, 280, 12064.
157. Ezzell, J. W.; Welkos, S. L. The capsule of Bacillus anthracis, a review. J. App. l Microbiol., 1999, 87, 250.
158. Kocianova, S.; Vuong, C.; Yao, Y.; Voyich, J. M.; Fischer, E. R.; De Leo, F. R.; Otto, M. Key role of poly-gamma-DL-glutamic acid in immune evasion and virulence of Staphylococcus epidermidis. J. Clin. Invest., 2005, 115, 688-694.
159. Yao, Y.; Sturdevant, D. E.; Otto, M. Genomewide analysis of gene expression in Staphylococcus epidermidis biofilms: insights into the pathophysiology of S. epidermidis biofilms and the role of phenol-soluble modulins in formation of biofilms. J. Infect. Dis., 2005, 191, 289-298.
160. Otto, M. Bacterial sensing of antimicrobial peptides. Contrib. Microbiol., 2009, 16, 136-149.
161. Gooderham, W. J.; Bains, M.; McPhee, J. B.; Wiegand, I.; Hancock, R. E. Induction by cationic antimicrobial peptides and involvement in intrinsic polymyxin and antimicrobial peptide resistance, biofilm formation, and swarming motility of PsrA in Pseudomonas aeruginosa. J. Bacteriol., 2008, 190, 5624-5634.
162. Macfarlane, E. L.; Kwasnicka, A.; Hancock, R. E. Role of Pseudomonas aeruginosa PhoP-phoQ in resistance to antimicrobial cationic peptides and aminoglycosides. Microbiology, 2000, 146, 2543-2354.
163. Gooderham, W. J.; Gellatly, S. L.; Sanschagrin, F.; McPhee, J. B., Bains, M.; Cosseau, C.; Levesque, R. C.; Hancock, R. E. The sensor kinase PhoQ mediates virulence in Pseudomonas aeruginosa. Microbiology, 2009, 155, 699-711.
164. Ramsey, M. M.; Whiteley, M. Pseudomonas aeruginosa attachment and biofilm development in dynamic environments. Mol. Microbiol., 2004, 53, 1075-1087.
165. Fabretti, F.; Theilacker, C.; Baldassarri, L.; Kaczynski, Z.; Kropec, A.; Holst, O.; Huebner, J. Alanine esters of enterococcal lipoteichoic acid play a role in biofilm formation and resistance to antimicrobial peptides. Infect. Immun., 2006, 74, 4164-4171.
166. Pamp, S. J.; Gjermansen, M.; Johansen, H. K.; Tolker-Nielsen, T. Tolerance to the antimicrobial peptide colistin in Pseudomonas aeruginosa biofilms is linked to metabolically active cells, and depends on the pmr and mexAB-oprM genes. Mol. Microbiol., 2008, 68, 223-240.
167. Chen, G.; Zhou, M.; Chen, S.; Lv, G.; Yao, J. Nanolayer biofilm coated on magnetic nanoparticles by using a dielectric barrier discharge glow plasma fluidized bed for immobilizing an antimicrobial peptide. Nanotechnology, 2009, 20, 465706.
168. Flemming, H. C.; Wingender, J. The biofilm matrix. Nature Rev. Microbiol., 2010, 8, 623-633.
169. Tetz, V. V.; Tetz, G. V. Effect of extracellular DNA destruction by DNase I on characteristics of forming biofilms. DNA Cell. Biol., 2010, 29, 399-405.
170. Tetz G. V.; Artemenko, N. K.; Tetz, V. V. Effect of DNase and antibiotics on biofilm characteristics. Antimicrob. Agents Chemother., 2009, 53, 1204-1209.
171. Donelli, G.; Francolini, I.; Romoli, D.; Guaglianone, E.; Piozzi, A.; Ragunath, C.; Kaplan, J. B. Synergistic activity of dispersin B and cefamandole nafate in inhibition of staphylococcal biofilm growth on polyurethanes. Antimicrob. Agents Chemother., 2007, 51, 2733-2740.
172. Gakhar, L.; Bartlett, J. A.; Penterman, J.; Mizrachi, D.; Singh, P. K.; Mallampalli, R. K.; Ramaswamy, S.; McCray, P. B. Jr. PLUNC is a novel airway surfactant protein with anti-biofilm activity. Plos One, 2010, 5, e9098.