Skip to main content
Top
Published in: Journal of Infection and Chemotherapy 5/2012

01-10-2012 | Original Article

Effects of lactoferricin B against keratitis-associated fungal biofilms

Authors: Jayangshu Sengupta, Suman Saha, Archana Khetan, Sujoy K. Sarkar, Santi M. Mandal

Published in: Journal of Infection and Chemotherapy | Issue 5/2012

Login to get access

Abstract

Biofilms are considered as the most important developmental characteristics in ocular infections. Biofilm eradication is a major challenge today to overcome the incidence of drug resistance. This report demonstrates the in vitro ability of biofilm formation on contact lens by three common keratitis-associated fungal pathogens, namely, Aspergillus fumigatus, Fusarium solani, and Candida albicans. Antifungal sensitivity testing performed for both planktonic cells and biofilm revealed the sessile phenotype to be resistant at MIC levels for the planktonic cells and also at higher concentrations. A prototype lens care solution was also found to be partially effective in eradication of the mature biofilm from contact lenses. Lactoferricin B (Lacf, 64 μg/ml), an antimicrobial peptide, exhibited almost no effect on the sessile phenotype. However, the combinatory effect of Lacf with antifungals against planktonic cells and biofilms of three fungal strains that were isolated from keratitis patients exhibited a reduction of antifungal dose more than eightfold. Furthermore, the effect of Lacf in lens care solution against biofilms in which those strains formed was eradicated successfully. These results suggest that lactoferricin B could be a promising candidate for clinical use in improving biofilm susceptibility to antifungals and also as an antibiofilm-antifungal additive in lens care solution.
Literature
1.
go back to reference Agrawal V, Biswas J, Madhavan HN, Mangat G, Reddy MK, Saini, et al. Current perspectives in infectious keratitis. Ind J Ophthalmol. 1994;42:171–92. Agrawal V, Biswas J, Madhavan HN, Mangat G, Reddy MK, Saini, et al. Current perspectives in infectious keratitis. Ind J Ophthalmol. 1994;42:171–92.
2.
go back to reference Saha S, Banerjee D, Khetan A, Sengupta J. Epidemiological profile of fungal keratitis in urban population of West Bengal, India. Oman J Ophthalmol. 2009;2:114–8.PubMedCrossRef Saha S, Banerjee D, Khetan A, Sengupta J. Epidemiological profile of fungal keratitis in urban population of West Bengal, India. Oman J Ophthalmol. 2009;2:114–8.PubMedCrossRef
3.
go back to reference Srinivasan M, Gonzales CA, George C. Epidemiology and aetiological diagnosis of corneal ulceration in Madurai, South India. Br J Ophthalmol. 1997;81:965–71.PubMedCrossRef Srinivasan M, Gonzales CA, George C. Epidemiology and aetiological diagnosis of corneal ulceration in Madurai, South India. Br J Ophthalmol. 1997;81:965–71.PubMedCrossRef
4.
go back to reference Chang DC, Grant GB, O’Donnell K, Wannemuehler KA, Noble-Wang J, Rao CY, et al. Multistate outbreak of Fusarium keratitis associated with use of a contact lens solution. JAMA. 2006;296:953–63.PubMedCrossRef Chang DC, Grant GB, O’Donnell K, Wannemuehler KA, Noble-Wang J, Rao CY, et al. Multistate outbreak of Fusarium keratitis associated with use of a contact lens solution. JAMA. 2006;296:953–63.PubMedCrossRef
5.
go back to reference Khor WB, Aung T, Saw SM, Wong TY, Tambyah PA, Tan AL, et al. An outbreak of Fusarium keratitis associated with contact lens wear in Singapore. JAMA. 2006;295:2867–73.PubMedCrossRef Khor WB, Aung T, Saw SM, Wong TY, Tambyah PA, Tan AL, et al. An outbreak of Fusarium keratitis associated with contact lens wear in Singapore. JAMA. 2006;295:2867–73.PubMedCrossRef
6.
go back to reference Sun Y, Chandra J, Mukherjee P, Szczotka-Flynn L, Ghannoum MA, Pearlman E, et al. Model of contact lens-associated Fusarium keratitis. Invest Ophthalmol Vis Sci. 2010;51:1511–6.PubMedCrossRef Sun Y, Chandra J, Mukherjee P, Szczotka-Flynn L, Ghannoum MA, Pearlman E, et al. Model of contact lens-associated Fusarium keratitis. Invest Ophthalmol Vis Sci. 2010;51:1511–6.PubMedCrossRef
7.
go back to reference Holden BA, Sankaridurg PR, Sweeney DF, Stretton S, Naduvilath TJ, Rao GN. Microbial keratitis in prospective studies of extended wear with disposable hydrogel contact lenses. Cornea. 2005;24:156–61.PubMedCrossRef Holden BA, Sankaridurg PR, Sweeney DF, Stretton S, Naduvilath TJ, Rao GN. Microbial keratitis in prospective studies of extended wear with disposable hydrogel contact lenses. Cornea. 2005;24:156–61.PubMedCrossRef
8.
go back to reference Costerton JW, Stewart PS, Greenberg EP. Bacterial biofilms: a common cause of persistent infections. Science. 1999;284:1318–22.PubMedCrossRef Costerton JW, Stewart PS, Greenberg EP. Bacterial biofilms: a common cause of persistent infections. Science. 1999;284:1318–22.PubMedCrossRef
9.
go back to reference De Lucca AJ, Walsh TJ. Antifungal peptides: origin, activity, and therapeutic potential. Rev Iberoam Micol. 2000;17:116–20. De Lucca AJ, Walsh TJ. Antifungal peptides: origin, activity, and therapeutic potential. Rev Iberoam Micol. 2000;17:116–20.
10.
go back to reference Mandal SM, Migliolo L, Franco OL, Ghosh AK. Identification of an antifungal peptide from Trapa natans fruits with inhibitory effects on Candida tropicalis biofilm formation. Peptides. 2011;32:1741–7.PubMedCrossRef Mandal SM, Migliolo L, Franco OL, Ghosh AK. Identification of an antifungal peptide from Trapa natans fruits with inhibitory effects on Candida tropicalis biofilm formation. Peptides. 2011;32:1741–7.PubMedCrossRef
11.
go back to reference Gifford JL, Hunter HN, Vogel HJ. Lactoferricin: a lactoferrin-derived peptide with antimicrobial, antiviral, antitumor and immunological properties. Cell Mol Life Sci. 2005;62:2588–98.PubMedCrossRef Gifford JL, Hunter HN, Vogel HJ. Lactoferricin: a lactoferrin-derived peptide with antimicrobial, antiviral, antitumor and immunological properties. Cell Mol Life Sci. 2005;62:2588–98.PubMedCrossRef
12.
go back to reference Chandra J, Kuhn DM, Mukherjee PK, Hoyer LL, McCormick T, Ghannoum MA. Biofilm formation by the fungal pathogen Candida albicans: development, architecture and drug resistance. J Bacteriol. 2001;183:5385–94.PubMedCrossRef Chandra J, Kuhn DM, Mukherjee PK, Hoyer LL, McCormick T, Ghannoum MA. Biofilm formation by the fungal pathogen Candida albicans: development, architecture and drug resistance. J Bacteriol. 2001;183:5385–94.PubMedCrossRef
13.
go back to reference Hawser SP, Norris H, Jessup CJ, Ghannoum MA. Comparison of a 2,3-bis(2-methoxy-4-nitro-5-sulfophenyl)-5-[(phenylamino)carbonyl]-2H-tetrazolium hydroxide (XTT) colorimetric method with the standardized National Committee for Clinical Laboratory standards method of testing clinical yeast isolates for susceptibility to antifungal agents. J Clin Microbiol. 1998;36:1450–2.PubMed Hawser SP, Norris H, Jessup CJ, Ghannoum MA. Comparison of a 2,3-bis(2-methoxy-4-nitro-5-sulfophenyl)-5-[(phenylamino)carbonyl]-2H-tetrazolium hydroxide (XTT) colorimetric method with the standardized National Committee for Clinical Laboratory standards method of testing clinical yeast isolates for susceptibility to antifungal agents. J Clin Microbiol. 1998;36:1450–2.PubMed
14.
go back to reference Mowat E, Butcher J, Lang S, Williams C, Ramage G. Development of a simple model for studying the effects of antifungal agents on multicellular communities of Aspergillus fumigatus. J Med Microbiol. 2007;56:1205–12.PubMedCrossRef Mowat E, Butcher J, Lang S, Williams C, Ramage G. Development of a simple model for studying the effects of antifungal agents on multicellular communities of Aspergillus fumigatus. J Med Microbiol. 2007;56:1205–12.PubMedCrossRef
15.
go back to reference Pierce CG, Uppuluri P, Tristan AR, Wormley FR Jr, Mowat E, Ramage G, Lopez-Ribot JL. A simple and reproducible 96-well plate-based method for the formation of fungal biofilms and its application to antifungal susceptibility testing. Nat Protoc. 2008;3:1494–500.PubMedCrossRef Pierce CG, Uppuluri P, Tristan AR, Wormley FR Jr, Mowat E, Ramage G, Lopez-Ribot JL. A simple and reproducible 96-well plate-based method for the formation of fungal biofilms and its application to antifungal susceptibility testing. Nat Protoc. 2008;3:1494–500.PubMedCrossRef
16.
go back to reference National Committee for Clinical Laboratory Standards. Reference method for broth dilution antifungal susceptibility testing of yeasts. Approved standard, NCCLS document M27-A. National Committee for Clinical Laboratory Standards, Wayne, PA, 1997. National Committee for Clinical Laboratory Standards. Reference method for broth dilution antifungal susceptibility testing of yeasts. Approved standard, NCCLS document M27-A. National Committee for Clinical Laboratory Standards, Wayne, PA, 1997.
17.
go back to reference Melo AS, Bizerra FC, Freymüller E, Arthington-Skaggs BA, Colombo AL. Biofilm production and evaluation of antifungal susceptibility amongst clinical Candida spp. isolates, including strains of the Candida parapsilosis complex. Med Mycol. 2011;49:253–62.PubMedCrossRef Melo AS, Bizerra FC, Freymüller E, Arthington-Skaggs BA, Colombo AL. Biofilm production and evaluation of antifungal susceptibility amongst clinical Candida spp. isolates, including strains of the Candida parapsilosis complex. Med Mycol. 2011;49:253–62.PubMedCrossRef
18.
go back to reference Imamura Y, Chandra J, Mukherjee PK, Lattif AA, Szczotka-Flynn LB, Pearlman E, et al. Fusarium and Candida albicans biofilms on soft contact lenses: model development, influence of lens type, and susceptibility to lens care solutions. Antimicrob Agents Chemother. 2008;52:171–82.PubMedCrossRef Imamura Y, Chandra J, Mukherjee PK, Lattif AA, Szczotka-Flynn LB, Pearlman E, et al. Fusarium and Candida albicans biofilms on soft contact lenses: model development, influence of lens type, and susceptibility to lens care solutions. Antimicrob Agents Chemother. 2008;52:171–82.PubMedCrossRef
19.
go back to reference Kucharíkova S, Tournu H, Lagrou K, van Dijck P, Bujdáková H. Detailed comparison of Candida albicans and Candida glabrata biofilms under different conditions and their susceptibility to caspofungin and anidulafungin. J Med Microbiol. 2011;60:1261–9.PubMedCrossRef Kucharíkova S, Tournu H, Lagrou K, van Dijck P, Bujdáková H. Detailed comparison of Candida albicans and Candida glabrata biofilms under different conditions and their susceptibility to caspofungin and anidulafungin. J Med Microbiol. 2011;60:1261–9.PubMedCrossRef
20.
go back to reference Xu KD, McFeters GA, Stewart PS. Biofilm resistance to antimicrobial agents. Microbiology. 2000;146:547–9.PubMed Xu KD, McFeters GA, Stewart PS. Biofilm resistance to antimicrobial agents. Microbiology. 2000;146:547–9.PubMed
21.
go back to reference Ramage G, Walle KV, Wickes BL, López-Ribot JL. Standardized method for in vitro antifungal susceptibility testing of Candida albicans biofilms. Antimicrob Agents Chemother. 2000;45:2475–9.CrossRef Ramage G, Walle KV, Wickes BL, López-Ribot JL. Standardized method for in vitro antifungal susceptibility testing of Candida albicans biofilms. Antimicrob Agents Chemother. 2000;45:2475–9.CrossRef
22.
go back to reference Lynch S, Robertson GT. Bacterial and fungal biofilm infections. Annu Rev Med. 2000;59:415–28.CrossRef Lynch S, Robertson GT. Bacterial and fungal biofilm infections. Annu Rev Med. 2000;59:415–28.CrossRef
23.
go back to reference Bellamy W, Yamauchi K, Wakabayashi H, Takase M, Takakura N, Simamura S, et al. Antifungal properties of lactoferricin B, a peptide derived from the N-terminal region of bovine lactoferrin. Lett Appl Microbiol. 1994;18:230–3.CrossRef Bellamy W, Yamauchi K, Wakabayashi H, Takase M, Takakura N, Simamura S, et al. Antifungal properties of lactoferricin B, a peptide derived from the N-terminal region of bovine lactoferrin. Lett Appl Microbiol. 1994;18:230–3.CrossRef
24.
go back to reference Wakabayashi H, Abe S, Teraguchi S, Hayasawa H, Yamaguchi H. Inhibition of hyphal growth of azole-resistant strains of Candida albicans by triazole antifungal agents in the presence of lactoferrin-related compounds. Antimicrob Agents Chemother. 1998;42:1587–91.PubMed Wakabayashi H, Abe S, Teraguchi S, Hayasawa H, Yamaguchi H. Inhibition of hyphal growth of azole-resistant strains of Candida albicans by triazole antifungal agents in the presence of lactoferrin-related compounds. Antimicrob Agents Chemother. 1998;42:1587–91.PubMed
25.
go back to reference Lupetti A, Paulusma-Annema A, Welling MW, Senesi S, van Dissel JT, Nibbering P. Candidacidal activities of human lactoferrin peptides derived from the N-terminus. Antimicrob Agents Chemother. 2000;44:3257–63.PubMedCrossRef Lupetti A, Paulusma-Annema A, Welling MW, Senesi S, van Dissel JT, Nibbering P. Candidacidal activities of human lactoferrin peptides derived from the N-terminus. Antimicrob Agents Chemother. 2000;44:3257–63.PubMedCrossRef
26.
go back to reference Ueta E, Tanida T, Osaki T. A novel bovine lactoferrin peptide, FKCRRWQWRM, suppresses Candida cell growth and activates neutrophils. J Pept Res. 2001;57:240–9.PubMedCrossRef Ueta E, Tanida T, Osaki T. A novel bovine lactoferrin peptide, FKCRRWQWRM, suppresses Candida cell growth and activates neutrophils. J Pept Res. 2001;57:240–9.PubMedCrossRef
Metadata
Title
Effects of lactoferricin B against keratitis-associated fungal biofilms
Authors
Jayangshu Sengupta
Suman Saha
Archana Khetan
Sujoy K. Sarkar
Santi M. Mandal
Publication date
01-10-2012
Publisher
Springer Japan
Published in
Journal of Infection and Chemotherapy / Issue 5/2012
Print ISSN: 1341-321X
Electronic ISSN: 1437-7780
DOI
https://doi.org/10.1007/s10156-012-0398-3

Other articles of this Issue 5/2012

Journal of Infection and Chemotherapy 5/2012 Go to the issue