Plant-derived decapeptide osip108 interferes with candida albicans biofilm formation without affecting cell viability

Antimicrobial Agents and Chemotherapy

Volumn 58, Issue 5, 2014, Pages 2647-2656

  Delattin, Nicolas ^a   De Brucker, Katrijn ^a   Craik, David J ^b   Cheneval, Olivier ^b   Fröhlich, Mirjam ^c,g   Veber, Matija ^c   Girandon, Lenart ^c   Davis, Talya R ^d   Weeks, Anne E ^d   Kumamoto, Carol A ^d   Cos, Paul ^e   Coenye, Tom ^f   De Coninck, Barbara ^a,h   Cammue, Bruno P A ^a,h   Thevissen, Karin ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b UNIVERSITY OF QUEENSLAND   (Australia)

^c Educell ^*  (Slovenia)

^d TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF ANTWERP   (Belgium)

^f GHENT UNIVERSITY   (Belgium)

^g JO EF STEFAN INSTITUTE   (Slovenia)

^h DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

AMPHOTERICIN B; ANTIFUNGAL AGENT; CASPOFUNGIN; CELL MEMBRANE PROTEIN; OSIP108; PEPTIDE; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; OLIGOPEPTIDE;

ANTIFUNGAL ACTIVITY; ARTICLE; BIOFILM; CAENORHABDITIS ELEGANS; CANDIDA ALBICANS; CELL GROWTH; CELL VIABILITY; CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG POTENTIATION; FUNGAL CELL WALL; FUNGUS HYPHAE; FUNGUS MUTANT; HELMINTHIASIS; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MINIMUM INHIBITORY CONCENTRATION; MYCOSIS; NONHUMAN; PRIORITY JOURNAL; STRUCTURE ACTIVITY RELATION; DRUG EFFECTS; GROWTH, DEVELOPMENT AND AGING;

ANTIFUNGAL AGENTS; BIOFILMS; CANDIDA ALBICANS; OLIGOPEPTIDES;

EID: 84898657160     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.01274-13     Document Type: Article

References (68)

1. Wisplinghoff H, Bischoff T, Tallent SM, Seifert H, Wenzel RP, Edmond MB. 2004. Nosocomial bloodstream infections in US hospitals: analysis of 24,179 cases from a prospective nationwide surveillance study. Clin. Infect. Dis. 39:309-317. http://dx.doi.org/10.1086/421946.
2. Lai CC, Tan CK, Huang YT, Shao PL, Hsueh PR. 2008. Current challenges in the management of invasive fungal infections. J. Infect. Chemother. 14:77-85. http://dx.doi.org/10.1007/s10156-007-0595-7.
3. Marr KA. 2004. Invasive Candida infections: the changing epidemiology. Oncology 18:9-14.
4. Pfaller MA, Diekema DJ. 2010. Epidemiology of invasive mycoses in North America. Crit. Rev. Microbiol. 36:1-53. http://dx.doi.org/10.3109/ 10408410903241444.
5. Pfaller MA. 2012. Antifungal drug resistance: mechanisms, epidemiology, and consequences for treatment. Am. J. Med. 125(1 Suppl):S3-S13. http://dx.doi.org/10.1016/j.amjmed.2011.11.001.
6. Costerton JW, Stewart PS, Greenberg EP. 1999. Bacterial biofilms: a common cause of persistent infections. Science 284:1318-1322. http://dx.doi.org/10.1126/science.284.5418.1318.
7. Douglas LJ. 2003. Candida biofilms and their role in infection. Trends Microbiol. 11:30-36. http://dx.doi.org/10.1016/S0966-842X(02)00002-1.
8. Fanning S, Mitchell AP. 2012. Fungal biofilms. PLoS Pathog. 8:e1002585. http://dx.doi.org/10.1371/journal.ppat.1002585.
9. Ramage G, Rajendran R, Sherry L, Williams C. 2012. Fungal biofilm resistance. Int. J. Microbiol. 2012:528521. http://dx.doi.org/10.1155/2012/ 528521.
10. Kuhn DM, George T, Chandra J, Mukherjee PK, Ghannoum MA. 2002. Antifungal susceptibility of Candida biofilms: unique efficacy of amphotericin B lipid formulations and echinocandins. Antimicrob. Agents Chemother. 46:1773-1780. http://dx.doi.org/10.1128/AAC.46.6.1773-1780.2002.
11. Brown GD, Denning DW, Levitz SM. 2012. Tackling human fungal infections. Science 336:647. http://dx.doi.org/10.1126/science.1222236.
12. Kojic EM, Darouiche RO. 2004. Candida infections of medical devices. Clin. Microbiol. Rev. 17:255-267. http://dx.doi.org/10.1128/CMR.17.2.255-267. 2004.
13. Ramage G, Martinez JP, Lopez-Ribot JL. 2006. Candida biofilms on implanted biomaterials: a clinically significant problem. FEMS Yeast Res. 6:979-986. http://dx.doi.org/10.1111/j.1567-1364.2006.00117.x.
14. Danscher G, Locht LJ. 2010. In vivo liberation of silver ions from metallic silver surfaces. Histochem. Cell Biol. 133:359-366. http://dx.doi.org/10.1007/s00418-009-0670-5.
15. Sardi JC, Scorzoni L, Bernardi T, Fusco-Almeida AM, Mendes Giannini MJ. 2013. Candida species: current epidemiology, pathogenicity, biofilm formation, natural antifungal products and new therapeutic options. J. Med. Microbiol. 62:10-24. http://dx.doi.org/10.1099/jmm.0.045054-0.
16. De Coninck B, Carron D, Tavormina P, Willem L, Craik DJ, Vos C, Thevissen K, Mathys J, Cammue BP. 2013. Mining the genome of Arabidopsis thaliana as a basis for the identification of novel bioactive peptides involved in oxidative stress tolerance. J. Exp. Bot. 64:5297-5307. http://dx.doi.org/10.1093/jxb/ ert295.
17. Fonzi WA, Irwin MY. 1993. Isogenic strain construction and gene mapping in Candida albicans. Genetics 134:717-728.
18. Davis D, Edwards JE, Jr, Mitchell AP, Ibrahim AS. 2000. Candida albicans RIM101 pH response pathway is required for host-pathogen interactions. Infect. Immun. 68:5953-5959. http://dx.doi.org/10.1128/IAI.68.10.5953-5959.2000.
19. de Wit K, Paulussen C, Matheeussen A, van Rossem K, Cos P, Maes L. 2010. In vitro profiling of pramiconazole and in vivo evaluation in Microsporum canis dermatitis and Candida albicans vaginitis laboratory models. Antimicrob. Agents Chemother. 54:4927-4929. http://dx.doi.org/10.1128/AAC.00730-10.
20. Kaur R, Ma B, Cormack BP. 2007. A family of glycosylphosphatidylinositol- linked aspartyl proteases is required for virulence of Candida glabrata. Proc. Natl. Acad. Sci. U. S. A. 104:7628-7633. http://dx.doi.org/10.1073/pnas. 0611195104.
21. Sullivan DJ, Westerneng TJ, Haynes KA, Bennett DE, Coleman DC. 1995. Candida dubliniensis sp. nov.: phenotypic and molecular characterization of a novel species associated with oral candidosis in HIV-infected individuals. Microbiology 141(Pt 7):1507-1521.
22. Wilson RB, Davis D, Mitchell AP. 1999. Rapid hypothesis testing with Candida albicans through gene disruption with short homology regions. J. Bacteriol. 181:1868-1874.
23. McCluskey K, Wiest A, Plamann M. 2010. The Fungal Genetics Stock Center: a repository for 50 years of fungal genetics research. J. Biosci. 35:119-126. http://dx.doi.org/10.1007/s12038-010-0014-6.
24. Plaine A, Walker L, Da Costa G, Mora-Montes HM, McKinnon A, Gow NA, Gaillardin C, Munro CA, Richard ML. 2008. Functional analysis of Candida albicans GPI-Anchored proteins: roles in cell wall integrity and caspofungin sensitivity. Fungal Genet. Biol. 45:1404-1414. http://dx.doi.org/10.1016/j.fgb. 2008.08.003.
25. Terras FR, Schoofs HM, De Bolle MF, Van Leuven F, Rees SB, Vanderleyden J, Cammue BP, Broekaert WF. 1992. Analysis of two novel classes of plant antifungal proteins from radish (Raphanus sativus L.) seeds. J. Biol. Chem. 267:15301-15309.
26. Halai R, Clark RJ, Nevin ST, Jensen JE, Adams DJ, Craik DJ. 2009. Scanning mutagenesis of alpha-conotoxin Vc1.1 reveals residues crucial for activity at the alpha9alpha10 nicotinic acetylcholine receptor. J. Biol. Chem. 284:20275-20284. http://dx.doi.org/10.1074/jbc.M109.015339.
27. Simonsen SM, Sando L, Rosengren KJ, Wang CK, Colgrave ML, Daly NL, Craik DJ. 2008. Alanine scanning mutagenesis of the prototypic cyclotide reveals a cluster of residues essential for bioactivity. J. Biol. Chem. 283:9805-9813. http://dx.doi.org/10.1074/jbc.M709303200.
28. Greenfield NJ. 2006. Using circular dichroism spectra to estimate protein secondary structure. Nat. Protoc. 1:2876-2890. http://dx.doi.org/10.1038/nprot. 2006.202.
29. Sando L, Henriques ST, Foley F, Simonsen SM, Daly NL, Hall KN, Gustafson KR, Aguilar MI, Craik DJ. 2011. A synthetic mirror image of kalata B1 reveals that cyclotide activity is independent of a protein receptor. Chembiochem 12: 2456-2462. http://dx.doi.org/10.1002/cbic.201100450.
30. Clinical and Laboratory Standards Institute. 2008. Reference method for broth dilution antifungal susceptibility testing of yeast, approved standard. CLSI document M27-A3. Clinical and Laboratory Standards Institute, Wayne, PA.
31. O'Brien J, Wilson I, Orton T, Pognan F. 2000. Investigation of the Alamar Blue (resazurin) fluorescent dye for the assessment of mammalian cell cytotoxicity. Eur. J. Biochem. 267:5421-5426. http://dx.doi.org/10.1046/j.1432- 1327.2000.01606.x.
32. Tellier R, Krajden M, Grigoriew GA, Campbell I. 1992. Innovative endpoint determination system for antifungal susceptibility testing of yeasts. Antimicrob. Agents Chemother. 36:1619-1625. http://dx.doi.org/10.1128/AAC.36.8. 1619.
33. Delattin N, De Brucker K, Vandamme K, Meert E, Marchand A, Chaltin P, Cammue BP, Thevissen K. 27 November 2013. Repurposing as a means to increase the activity of amphotericin B and caspofungin against C. albicans biofilms. J. Antimicrob. Chemother. http://dx.doi.org/10.1093/jac/dkt449.
34. Odds FC. 2003. Synergy, antagonism, and what the chequerboard puts between them. J. Antimicrob. Chemother. 52:1. http://dx.doi.org/10.1093/jac/ dkg301.
35. Breger J, Fuchs BB, Aperis G, Moy TI, Ausubel FM, Mylonakis E. 2007. Antifungal chemical compounds identified using a C. elegans pathogenicity assay. PLoS Pathog. 3:e18. http://dx.doi.org/10.1371/journal.ppat.0030018.
36. Kumamoto CA. 2005. A contact-Activated kinase signals Candida albicans invasive growth and biofilm development. Proc. Natl. Acad. Sci. U. S. A. 102:5576-5581. http://dx.doi.org/10.1073/pnas.0407097102.
37. Nailis H, Vandenbroucke R, Tilleman K, Deforce D, Nelis H, Coenye T. 2009. Monitoring ALS1 and ALS3 gene expression during in vitro Candida albicans biofilm formation under continuous flow conditions. Mycopathologia 167:9-17. http://dx.doi.org/10.1007/s11046-008-9148-6.
38. Overhage J, Campisano A, Bains M, Torfs EC, Rehm BH, Hancock RE. 2008. Human host defense peptide LL-37 prevents bacterial biofilm formation. Infect. Immun. 76:4176-4182. http://dx.doi.org/10.1128/IAI.00318-08.
39. Hell E, Giske CG, Nelson A, Romling U, Marchini G. 2010. Human cathelicidin peptide LL37 inhibits both attachment capability and biofilm formation of Staphylococcus epidermidis. Lett. Appl. Microbiol. 50:211-215. http://dx.doi.org/10.1111/j.1472-765X.2009.02778.x.
40. Tsai PW, Yang CY, Chang HT, Lan CY. 2011. Human antimicrobial peptide LL-37 inhibits adhesion of Candida albicans by interacting with yeast cell-wall carbohydrates. PLoS One 6:e17755. http://dx.doi.org/10.1371/journal.pone. 0017755.
41. Chang HT, Tsai PW, Huang HH, Liu YS, Chien TS, Lan CY. 2012. LL37 and hBD-3 elevate the beta-1,3-exoglucanase activity of Candida albicans Xog1p, resulting in reduced fungal adhesion to plastic. Biochem. J. 441: 963-970. http://dx.doi.org/10.1042/BJ20111454.
42. Theberge S, Semlali A, Alamri A, Leung KP, Rouabhia M. 2013. C. albicans growth, transition, biofilm formation, and gene expression modulation by antimicrobial decapeptide KSL-W. BMC Microbiol. 13:246. http://dx.doi.org/10. 1186/1471-2180-13-246.
43. Thankappan B, Jeyarajan S, Hiroaki S, Anbarasu K, Natarajaseenivasan K, Fujii N. 2013. Antimicrobial and antibiofilm activity of designed and synthesized antimicrobial peptide, KABT-AMP. Appl. Biochem. Biotechnol. 170:1184-1193. http://dx.doi.org/10.1007/s12010-013-0258-3.
44. Hamamoto K, Kida Y, Zhang Y, Shimizu T, Kuwano K. 2002. Antimicrobial activity and stability to proteolysis of small linear cationic peptides with D-Amino acid substitutions. Microbiol. Immunol. 46:741-749. http://dx.doi.org/ 10.1111/j.1348-0421.2002.tb02759.x.
45. Clark RJ, Jensen J, Nevin ST, Callaghan BP, Adams DJ, Craik DJ. 2010. The engineering of an orally active conotoxin for the treatment of neuropathic pain. Angew. Chem. Int. Ed. Engl. 49:6545-6548. http://dx.doi.org/10.1002/anie. 201000620.
46. Darby C, Hsu JW, Ghori N, Falkow S. 2002. Caenorhabditis elegans: plague bacteria biofilm blocks food intake. Nature 417:243-244. http://dx.doi.org/10. 1038/417243a.
47. Joshua GW, Karlyshev AV, Smith MP, Isherwood KE, Titball RW, Wren BW. 2003. A Caenorhabditis elegans model of Yersinia infection: biofilm formation on a biotic surface. Microbiology 149:3221-3229. http://dx.doi.org/10.1099/mic.0. 26475-0.
48. Tan L, Darby C. 2004. A movable surface: formation of Yersinia sp. biofilms on motile Caenorhabditis elegans. J. Bacteriol. 186:5087-5092. http://dx.doi.org/10.1128/JB.186.15.5087-5092.2004.
49. Begun J, Gaiani JM, Rohde H, Mack D, Calderwood SB, Ausubel FM, Sifri CD. 2007. Staphylococcal biofilm exopolysaccharide protects against Caenorhabditis elegans immune defenses. PLoS Pathog. 3:e57. http://dx.doi.org/10.1371/journal. ppat.0030057.
50. Edwards S, Kjellerup BV. 2012. Exploring the applications of invertebrate hostpathogenmodelsfor in vivobiofilminfections.FEMSImmunol.Med.Microbiol. 65:205-214. http://dx.doi.org/10.1111/j.1574-695X.2012.00975.x.
51. Ricicova M, Kucharikova S, Tournu H, Hendrix J, Bujdakova H, Van Eldere J, Lagrou K, Van Dijck P. 2010. Candida albicans biofilm formation in a new in vivo rat model. Microbiology 156:909-919. http://dx.doi.org/10.1099/mic.0. 033530-0.
52. Burgers R, Hahnel S, Reichert TE, Rosentritt M, Behr M, Gerlach T, Handel G, Gosau M. 2010. Adhesion of Candida albicans to various dental implant surfaces and the influence of salivary pellicle proteins. Acta Biomater. 6:2307-2313. http://dx.doi.org/10.1016/j.actbio.2009.11.003.
53. De Prijck K, De Smet N, Coenye T, Schacht E, Nelis HJ. 2010. Prevention of Candida albicans biofilm formation by covalently bound dimethylaminoethylmethacrylate and polyethylenimine. Mycopathologia 170: 213-221. http://dx.doi.org/10.1007/s11046-010-9316-3.
54. Finkel JS, Mitchell AP. 2011. Genetic control of Candida albicans biofilm development. Nat. Rev. Microbiol. 9:109-118. http://dx.doi.org/10.1038/ nrmicro2475.
55. Baillie GS, Douglas LJ. 1999. Role of dimorphism in the development of Candida albicans biofilms. J. Med. Microbiol. 48:671-679. http://dx.doi.org/10. 1099/00222615-48-7-671.
56. Verna J, Lodder A, Lee K, Vagts A, Ballester R. 1997. A family of genes required for maintenance of cell wall integrity and for the stress response in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. U. S. A. 94:13804-13809. http://dx.doi.org/10.1073/pnas.94.25.13804.
57. Zu T, Verna J, Ballester R. 2001. Mutations in WSC genes for putative stress receptors result in sensitivity to multiple stress conditions and impairment of Rlm1-dependent gene expression in Saccharomyces cerevisiae. Mol. Genet. Genomics 266:142-155. http://dx.doi.org/10.1007/s004380100537.
58. Norice CT, Smith FJ, Jr, Solis N, Filler SG, Mitchell AP. 2007. Requirement for Candida albicans Sun41 in biofilm formation and virulence. Eukaryot. Cell 6:2046-2055. http://dx.doi.org/10.1128/EC.00314-07.
59. Albrecht A, Felk A, Pichova I, Naglik JR, Schaller M, de Groot P, Maccallum D, Odds FC, Schafer W, Klis F, Monod M, Hube B. 2006. Glycosylphosphatidylinositol-Anchored proteases of Candida albicans target proteins necessary for both cellular processes and host-pathogen interactions. J. Biol. Chem. 281:688-694. http://dx.doi.org/10.1074/jbc.M509297200.
60. Sanglard D, Ischer F, Marchetti O, Entenza J, Bille J. 2003. Calcineurin A of Candida albicans: involvement in antifungal tolerance, cell morphogenesis and virulence. Mol. Microbiol. 48:959-976. http://dx.doi.org/10.1046/j.1365- 2958.2003.03495.x.
61. Bader T, Bodendorfer B, Schroppel K, Morschhauser J. 2003. Calcineurin is essential for virulence in Candida albicans. Infect. Immun. 71:5344-5354. http://dx.doi.org/10.1128/IAI.71.9.5344-5354.2003.
62. Lane S, Zhou S, Pan T, Dai Q, Liu H. 2001. The basic helix-loop-helix transcription factor Cph2 regulates hyphal development in Candida albicans partly via TEC1. Mol. Cell. Biol. 21:6418-6428. http://dx.doi.org/10.1128/MCB. 21.19.6418-6428.2001.
63. Liu H. 2001. Transcriptional control of dimorphism in Candida albicans. Curr.Opin.Microbiol.4:728-735.http://dx.doi.org/10.1016/S1369-5274-(01)00275-2.
64. Thevissen K, de Mello Tavares P, Xu D, Blankenship J, Vandenbosch D, Idkowiak-Baldys J, Govaert G, Bink A, Rozental S, de Groot PW, Davis TR, Kumamoto CA, Vargas G, Nimrichter L, Coenye T, Mitchell A, Roemer T, Hannun YA, Cammue BP. 2012. The plant defensin RsAFP2 induces cell wall stress, septin mislocalization and accumulation of ceramides in Candida albicans. Mol. Microbiol. 84:166-180. http://dx.doi.org/10.1111/j.1365-2958.2012.08017.x.
65. Shareck J, Nantel A, Belhumeur P. 2011. Conjugated linoleic acid inhibits hyphal growth in Candida albicans by modulating Ras1p cellular levels and downregulating TEC1 expression. Eukaryot. Cell 10:565-577. http://dx.doi.org/10. 1128/EC.00305-10.
66. Silva S, Negri M, Henriques M, Oliveira R, Williams DW, Azeredo J. 2011. Adherence and biofilm formation of non-Candida albicans Candida species. Trends Microbiol. 19:241-247. http://dx.doi.org/10.1016/j.tim.2011.02.003.
67. Ramage G, Mowat E, Jones B, Williams C, Lopez-Ribot J. 2009. Our current understanding of fungal biofilms. Crit. Rev. Microbiol. 35:340-355. http://dx.doi.org/10.3109/10408410903241436.
68. Ramage G, Vande Walle K, Wickes BL, Lopez-Ribot JL. 2001. Biofilm formation by Candida dubliniensis. J. Clin. Microbiol. 39:3234-3240. http://dx.doi.org/10.1128/JCM.39.9.3234-3240.2001.