Anti-Candida activity of 1-18 fragment of the frog skin peptide esculentin-1b: In vitro and in vivo studies in a Caenorhabditis elegans infection model

Cellular and Molecular Life Sciences

Volumn 71, Issue 13, 2014, Pages 2535-2546

  Luca, Vincenzo ^a   Olivi, Massimiliano ^b   Di Grazia, Antonio ^a   Palleschi, Claudio ^b   Uccelletti, Daniela ^b   Mangoni, Maria Luisa ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

Anti Candida activity; Antimicrobial peptide; Caenorhabditis elegans; Membrane permeabilization; Simple infection model

Indexed keywords

AMPHOTERICIN B; ESCULENTIN 1B; POLYPEPTIDE ANTIBIOTIC AGENT; UNCLASSIFIED DRUG;

ADULT; AMINO TERMINAL SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIFUNGAL ACTIVITY; ANURA; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; FUNGUS GROWTH; FUNGUS HYPHAE; GROWTH INHIBITION; IN VITRO STUDY; IN VIVO STUDY; NEMATODIASIS; NONHUMAN; REVIEW; SURVIVAL RATE; YEAST CELL;

ANURA; CAENORHABDITIS ELEGANS; CANDIDA; CANDIDA ALBICANS;

AMPHIBIAN PROTEINS; ANIMALS; ANTI-INFECTIVE AGENTS; ANTIMICROBIAL CATIONIC PEPTIDES; ANURA; CAENORHABDITIS ELEGANS; CANDIDA ALBICANS; SKIN;

EID: 84903317155     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-013-1500-4     Document Type: Review

References (79)

1. Leleu G, Aegerter P, Guidet B (2002) Systemic candidiasis in intensive care units: a multicenter, matched-cohort study. J Crit Care 17:168-175
2. Leroy O, Gangneux JP, Montravers P, Mira JP, Gouin F, Sollet JP, Carlet J, Reynes J, Rosenheim M, Regnier B, Lortholary O (2009) Epidemiology, management, and risk factors for death of invasive Candida infections in critical care: a multicenter, prospective, observational study in France (2005-2006). Crit Care Med 37:1612-1618
3. Alangaden GJ (2011) Nosocomial fungal infections: epidemiology, infection control, and prevention. Infect Dis Clin North Am 25:201-225
4. Bajwa S, Kulshrestha A (2013) Fungal infections in intensive care unit: challenges in diagnosis and management. Ann Med Health Sci Res 3:238-244
5. Kao AS, Brandt ME, Pruitt WR, Conn LA, Perkins BA, Stephens DS, Baughman WS, Reingold AL, Rothrock GA, Pfaller MA, Pinner RW, Hajjeh RA (1999) The epidemiology of candidemia in two United States cities: results of a population-based active surveillance. Clin Infect Dis 29:1164-1170 (Pubitemid 30265634)
6. Klotz SA, Chasin BS, Powell B, Gaur NK, Lipke PN (2007) Polymicrobial bloodstream infections involving Candida species: analysis of patients and review of the literature. Diagn Microbiol Infect Dis 59:401-406 (Pubitemid 350184233)
7. Lockhart SR, Iqbal N, Cleveland A, Farley MM, Harrison LH, Bolden CB, Baughman W, Stein B, Hollick R, Park BJ, Chiller T (2012) Species identification and antifungal susceptibility testing of Candida bloodstream isolates from population-based surveillance studies in two US cities from 2008 to 2011. J Clin Microbiol 50:3435-3442
8. Sudbery P, Gow N, Berman J (2004) The distinct morphogenic states of Candida albicans. Trends Microbiol 12:317-324 (Pubitemid 38829652)
9. Maganti H, Yamamura D, Xu J (2011) Prevalent nosocomial clusters among causative agents for candidemia in Hamilton, Canada. Med Mycol 49:530-538
10. Gow NA, Brown AJ, Odds FC (2002) Fungal morphogenesis and host invasion. Curr Opin Microbiol 5:366-371
11. Saville SP, Lazzell AL, Monteagudo C, Lopez-Ribot JL (2003) Engineered control of cell morphology in vivo reveals distinct roles for yeast and filamentous forms of Candida albicans during infection. Eukaryot Cell 2:1053-1060 (Pubitemid 37298719)
12. Huang G (2012) Regulation of phenotypic transitions in the fungal pathogen Candida albicans. Virulence 3:251-261
13. Kumamoto CA, Vinces MD (2005) Contributions of hyphae and hypha-co-regulated genes to Candida albicans virulence. Cell Microbiol 7:1546-1554 (Pubitemid 41511912)
14. Berman J (2006) Morphogenesis and cell cycle progression in Candida albicans. Curr Opin Microbiol 9:595-601
15. Sudbery PE (2011) Growth of Candida albicans hyphae. Nat Rev Microbiol 9:737-748
16. Odds FC (1987) Candida infections: an overview. Crit Rev Microbiol 15:1-5
17. Berman J, Sudbery PE (2002) Candida albicans: a molecular revolution built on lessons from budding yeast. Nat Rev Genet 3:918-930 (Pubitemid 35423504)
18. White TC, Marr KA, Bowden RA (1998) Clinical, cellular, and molecular factors that contribute to antifungal drug resistance. Clin Microbiol Rev 11:382-402 (Pubitemid 28197359)
19. Prasad R, Kapoor K (2005) Multidrug resistance in yeast Candida. Int Rev Cytol 242:215-248 (Pubitemid 39642964)
20. Cannon RD, Lamping E, Holmes AR, Niimi K, Tanabe K, Niimi M, Monk BC (2007) Candida albicans drug resistance another way to cope with stress. Microbiology 153:3211-3217 (Pubitemid 47629526)
21. Ramirez E, Garcia-Rodriguez J, Borobia AM, Ortega JM, Lei S, Barrios-Fernandez A, Sanchez M, Carcas AJ, Herrero A, de la Puente JM, Frias J (2012) Use of antifungal agents in pediatric and adult high-risk areas. Eur J Clin Microbiol Infect Dis 31:337-347
22. Kinsky SC (1970) Antibiotic interaction with model membranes. Annu Rev Pharmacol 10:119-142
23. Lanternier F, Lortholary O (2008) Liposomal amphotericin B: what is its role in 2008? Clin Microbiol Infect 14:71-83 (Pubitemid 351593919)
24. Georgopapadakou NH, Walsh TJ (1994) Human mycoses: drugs and targets for emerging pathogens. Science 264:371-373 (Pubitemid 24986721)
25. Hancock RE (2001) Cationic peptides: effectors in innate immunity and novel antimicrobials. Lancet Infect Dis 1:156-164
26. Boman HG (2003) Antibacterial peptides: basic facts and emerging concepts. J Intern Med 254:197-215
27. Beisswenger C, Bals R (2005) Functions of antimicrobial peptides in host defense and immunity. Curr Protein Pept Sci 6:255-264 (Pubitemid 40812749)
28. Mangoni ML, Saugar JM, Dellisanti M, Barra D, Simmaco M, Rivas L (2005) Temporins, small antimicrobial peptides with leishmanicidal activity. J Biol Chem 280:984-990
29. Mookherjee N, Rehaume LM, Hancock RE (2007) Cathelicidins and functional analogues as antisepsis molecules. Expert Opin Ther Targets 11:993-1004 (Pubitemid 47240677)
30. Mookherjee N, Hancock RE (2007) Cationic host defence peptides: innate immune regulatory peptides as a novel approach for treating infections. Cell Mol Life Sci 64:922-933 (Pubitemid 46597762)
31. Yeung AT, Gellatly SL, Hancock RE (2011) Multifunctional cationic host defence peptides and their clinical applications. Cell Mol Life Sci 68:2161-2176
32. Shai Y (2002) Mode of action of membrane active antimicrobial peptides. Biopolymers 66:236-248
33. Mangoni ML (2011) Host-defense peptides: from biology to therapeutic strategies. Cell Mol Life Sci 68:2157-2159
34. Mangoni ML, Fiocco D, Mignogna G, Barra D, Simmaco M (2003) Functional characterisation of the 1-18 fragment of esculentin-1b, an antimicrobial peptide from Rana esculenta. Peptides 24:1771-1777 (Pubitemid 38198084)
35. Simmaco M, Mignogna G, Barra D, Bossa F (1994) Antimicrobial peptides from skin secretions of Rana esculenta. Molecular cloning of cDNAs encoding esculentin and brevinins and isolation of new active peptides. J Biol Chem 269:11956-11961
36. Ponti D, Mignogna G, Mangoni ML, De Biase D, Simmaco M, Barra D (1999) Expression and activity of cyclic and linear analogues of esculentin-1, an anti-microbial peptide from amphibian skin. Eur J Biochem 263:921-927 (Pubitemid 29361968)
37. Avrahami D, Shai Y (2004) A new group of antifungal and antibacterial lipopeptides derived from non-membrane active peptides conjugated to palmitic acid. J Biol Chem 279:12277-12285 (Pubitemid 38445793)
38. Marcellini L, Borro M, Gentile G, Rinaldi AC, Stella L, Aimola P, Barra D, Mangoni ML (2009) Esculentin-1b(1-18)-a membraneactive antimicrobial peptide that synergizes with antibiotics and modifies the expression level of a limited number of proteins in Escherichia coli. FEBS J 276:5647-5664
39. Uccelletti D, Zanni E, Marcellini L, Palleschi C, Barra D, Mangoni ML (2010) Anti-Pseudomonas activity of frog skin antimicrobial peptides in a Caenorhabditis elegans infection model: a plausible mode of action in vitro and in vivo. Antimicrob Agents Chemother 54:3853-3860
40. Marsh EK, May RC (2012) Caenorhabditis elegans, a model organism for investigating immunity. Appl Environ Microbiol 78:2075-2081
41. Stiernagel T (2006) Maintenance of C. elegans, Wormbook, ed. The C. elegans Research Community, Wormbook. doi:10.895/wormbook.1.101.1. http://www.wormbook.org 11 Feb 2006
42. Grieco P, Carotenuto A, Auriemma L, Saviello MR, Campiglia P, Gomez-Monterrey IM, Marcellini L, Luca V, Barra D, Novellino E, Mangoni ML (2013) The effect of d-amino acid substitution on the selectivity of temporin L towards target cells: identification of a potent anti-Candida peptide. Biochim Biophys Acta 1828:652-660
43. Hawser S, Francolini M, Islam K (1996) The effects of antifungal agents on the morphogenetic transformation by Candida albicans in vitro. J Antimicrob Chemother 38:579-587 (Pubitemid 26390399)
44. Cleary IA, Reinhard SM, Miller CL, Murdoch C, Thornhill MH, Lazzell AL, Monteagudo C, Thomas DP, Saville SP (2011) Candida albicans adhesin Als3p is dispensable for virulence in the mouse model of disseminated candidiasis. Microbiology 157:1806-1815
45. Valenti P, Visca P, Antonini G, Orsi N (1985) Antifungal activity of ovotransferrin towards genus Candida. Mycopathologia 89:169-175 (Pubitemid 15114783)
46. Luca V, Stringaro A, Colone M, Pini A, Mangoni ML (2013) Esculentin(1-21), an amphibian skin membrane-active peptide with potent activity on both planktonic and biofilm cells of the bacterial pathogen Pseudomonas aeruginosa. Cell Mol Life Sci 70:2773-2786
47. Mangoni ML, Papo N, Barra D, Simmaco M, Bozzi A, Di Giulio A, Rinaldi AC (2004) Effects of the antimicrobial peptide temporin L on cell morphology, membrane permeability and viability of Escherichia coli. Biochem J 380:859-865 (Pubitemid 38850528)
48. 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
49. Moy TI, Ball AR, Anklesaria Z, Casadei G, Lewis K, Ausubel FM (2006) Identification of novel antimicrobials using a live-animal infection model. Proc Natl Acad Sci USA 103:10414-10419 (Pubitemid 44051181)
50. Chevalier M, Medioni E, Precheur I (2012) Inhibition of Candida albicans yeast-hyphal transition and biofilm formation by Solidago virgaurea water extracts. J Med Microbiol 61:1016-1022
51. Douglas LJ (2003) Candida biofilms and their role in infection. Trends Microbiol 11:30-36
52. Jabra-Rizk MA, Falkler WA, Meiller TF (2004) Fungal biofilms and drug resistance. Emerg Infect Dis 10:14-19 (Pubitemid 38040687)
53. Canton E, Peman J, Gobernado M, Viudes A, Espinel-Ingroff A (2004) Patterns of amphotericin B killing kinetics against seven Candida species. Antimicrob Agents Chemother 48:2477-2482 (Pubitemid 38823413)
54. Hong SY, Oh JE, Lee KH (1999) In vitro antifungal activity and cytotoxicity of a novel membrane-active peptide. Antimicrob Agents Chemother 43:1704-1707 (Pubitemid 29331251)
55. Younsi M, Ramanandraibe E, Bonaly R, Donner M, Coulon J (2000) Amphotericin B resistance and membrane fluidity in Kluyveromyces lactis strains. Antimicrob Agents Chemother 44:1911-1916 (Pubitemid 30422947)
56. Mayer FL, Wilson D, Hube B (2013) Candida albicans pathogenicity mechanisms. Virulence 4:119-128
57. Kuriyama T, Williams DW, Bagg J, Coulter WA, Ready D, Lewis MA (2005) In vitro susceptibility of oral Candida to seven antifungal agents. Oral Microbiol Immunol 20:349-353 (Pubitemid 41564346)
58. Pfaller MA, Boyken L, Hollis RJ, Messer SA, Tendolkar S, Diekema DJ (2005) In vitro activities of anidulafungin against more than 2,500 clinical isolates of Candida spp., including 315 isolates resistant to fluconazole. J Clin Microbiol 43:5425-5427 (Pubitemid 41612308)
59. Kontoyiannis DP, Lewis RE (2002) Antifungal drug resistance of pathogenic fungi. Lancet 359:1135-1144 (Pubitemid 34270742)
60. Benincasa M, Scocchi M, Pacor S, Tossi A, Nobili D, Basaglia G, Busetti M, Gennaro R (2006) Fungicidal activity of five cathelicidin peptides against clinically isolated yeasts. J Antimicrob Chemother 58:950-959
61. Sung WS, Lee J, Lee DG (2008) Fungicidal effect and the mode of action of piscidin 2 derived from hybrid striped bass. Biochem Biophys Res Commun 371:551-555
62. den Hertog AL, van Marle J, van Veen HA, Van't Hof W, Bolscher JG, Veerman EC, Nieuw Amerongen AV (2005) Candidacidal effects of two antimicrobial peptides: histatin 5 causes small membrane defects, but LL-37 causes massive disruption of the cell membrane. Biochem J 388:689-695 (Pubitemid 40839946)
63. Makovitzki A, Avrahami D, Shai Y (2006) Ultrashort antibacterial and antifungal lipopeptides. Proc Natl Acad Sci USA 103:15997-16002 (Pubitemid 44657581)
64. Wang P, Nan YH, Shin SY (2010) Candidacidal mechanism of a Leu/Lys-rich alpha-helical amphipathic model antimicrobial peptide and its diastereomer composed of d, l-amino acids. J Pept Sci 16:601-606
65. Aerts AM, Francois IE, Meert EM, Li QT, Cammue BP, Thevissen K (2007) The antifungal activity of RsAFP2, a plant defensin from raphanus sativus, involves the induction of reactive oxygen species in Candida albicans. J Mol Microbiol Biotechnol 13:243-247 (Pubitemid 47378154)
66. 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
67. Choi H, Lee DG (2013) The influence of the N-terminal region of antimicrobial peptide pleurocidin on fungal apoptosis. J Microbiol Biotechnol [Epub ahead of print]
68. Maurya IK, Thota CK, Sharma J, Tupe SG, Chaudhary P, Singh MK, Thakur IS, Deshpande M, Prasad R, Chauhan VS (2013) Mechanism of action of novel synthetic dodecapeptides against Candida albicans. Biochim Biophys Acta 1830:5193-5203
69. Gow NA, van de Veerdonk FL, Brown AJ, Netea MG (2011) Candida albicans morphogenesis and host defence: discriminating invasion from colonization. Nat Rev Microbiol 10:112-122
70. Baillie GS, Douglas LJ (2000) Matrix polymers of Candida biofilms and their possible role in biofilm resistance to antifungal agents. J Antimicrob Chemother 46:397-403
71. Ghannoum MA, Janini G, Khamis L, Radwan SS (1986) Dimorphism-associated variations in the lipid composition of Candida albicans. J Gen Microbiol 132:2367-2375 (Pubitemid 16047862)
72. Hitchcock CA, Barrett-Bee KJ, Russell NJ (1989) The lipid composition and permeability to the triazole antifungal antibiotic ICI 153066 of serum-grown mycelial cultures of Candida albicans. J Gen Microbiol 135:1949-1955 (Pubitemid 19197058)
73. Thevissen K, Osborn RW, Acland DP, Broekaert WF (1997) Specific, high affinity binding sites for an antifungal plant defensin on Neurospora crassa hyphae and microsomal membranes. J Biol Chem 272:32176-32181 (Pubitemid 28011892)
74. Thevissen K, Terras FR, Broekaert WF (1999) Permeabilization of fungal membranes by plant defensins inhibits fungal growth. Appl Environ Microbiol 65:5451-5458 (Pubitemid 129520636)
75. Wong JH, Ng TB, Legowska A, Rolka K, Hui M, Cho CH (2011) Antifungal action of human cathelicidin fragment (LL13-37) on Candida albicans. Peptides 32:1996-2002
76. Ewbank JJ, Zugasti O (2011) C. elegans: model host and tool for antimicrobial drug discovery. Dis Model Mech 4:300-304
77. Pukkila-Worley R, Peleg AY, Tampakakis E, Mylonakis E (2009) Candida albicans hyphal formation and virulence assessed using a Caenorhabditis elegans infection model. Eukaryot Cell 8:1750-1758
78. Pukkila-Worley R, Ausubel FM, Mylonakis E (2011) Candida albicans infection of Caenorhabditis elegans induces antifungal immune defenses. PLoS Pathog 7:e1002074
79. Coleman JJ, Ghosh S, Okoli I, Mylonakis E (2011) Antifungal activity of microbial secondary metabolites. PLoS One 6:e25321