Concentration-dependent mechanisms of cell penetration and killing by the de novo designed antifungal hexapeptide PAF26

Molecular Microbiology

Volumn 85, Issue 1, 2012, Pages 89-106

  Muñoz, Alberto ^a   Marcos, Jose F ^b   Read, Nick D ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b INSTITUTO DE AGROQUÍMICA Y TECNOLOGÍA DE ALIMENTOS CSIC   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ANTIFUNGAL AGENT; CELL PROTEIN; HEXAPEPTIDE; PEPTIDE PAF26; PROTEIN RAB 5; PROTEIN RVS 161; PROTEIN RVS 167; UNCLASSIFIED DRUG;

ARTICLE; CALCIUM HOMEOSTASIS; CELL KILLING; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG ACCUMULATION; DRUG MECHANISM; DRUG TRANSPORT; ENDOCYTOSIS; FUNGICIDAL ACTIVITY; INTERNALIZATION; MEMBRANE DEPOLARIZATION; NEUROSPORA CRASSA; NONHUMAN; PRIORITY JOURNAL;

ANTIFUNGAL AGENTS; ANTIMICROBIAL CATIONIC PEPTIDES; CALCIUM; CELL MEMBRANE PERMEABILITY; CYTOPLASM; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOCYTOSIS; HOMEOSTASIS; MICROBIAL SENSITIVITY TESTS; MICROSCOPY, FLUORESCENCE; NEUROSPORA CRASSA; OLIGOPEPTIDES; VACUOLES;

NEUROSPORA CRASSA;

EID: 84862764313     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2012.08091.x     Document Type: Article

References (75)

1. Alves, I.D., Jiao, C.Y., Aubry, S., Aussedat, B., Burlina, F., Chassaing, G., and Sagan, S. (2010) Cell biology meets biophysics to unveil the different mechanisms of penetratin internalization in cells. Biochim Biophys Acta 1798: 2231-2239.
2. Atkinson, H.A., Daniels, A., and Read, N.D. (2002) Live-cell imaging of endocytosis during conidial germination in the rice blast fungus, Magnaporthe grisea. Fungal Genet Biol 37: 233-244.
3. Berepiki, A., Lichius, A., Shoji, J., Tilsner, J., and Read, N.D. (2010) F-actin dynamics in Neurospora crassa. Eukaryot Cell 9: 547-557.
4. Berepiki, A., Lichius, A., and Read, N.D. (2011) Actin organization and dynamics in filamentous fungi. Nat Rev Microbiol 9: 876-897.
5. Binder, U., Chu, M., Read, N.D., and Marx, F. (2010) The antifungal activity of the Penicillium chrysogenum protein PAF disrupts calcium homeostasis in Neurospora crassa. Eukaryot Cell 9: 1374-1382.
6. Binder, U., Bencina, M., Eigentler, A., Meyer, V., and Marx, F. (2011) The Aspergillus giganteus antifungal protein AFPNN5353 activates the cell wall integrity pathway and perturbs calcium homeostasis. BMC Microbiol 11: 209.
7. Brogden, K.A. (2005) Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nat Rev Microbiol 3: 238-250.
8. Brown, K.L., and Hancock, R.E.W. (2006) Cationic host defense (antimicrobial) peptides. Curr Opin Immunol 18: 24-30.
9. Burston, H.E., Maldonado-Báez, L., Davey, M., Montpetit, B., Schluter, C., Wendland, B., and Conibear, E. (2009) Regulators of yeast endocytosis identified by systematic quantitative analysis. J Cell Biol 185: 1097-1110.
10. Castle, M., Nazarian, A., Yi, S.S., and Tempst, P. (1999) Lethal effects of apidaecin on Escherichia coli involve sequential molecular interactions with diverse targets. J Biol Chem 274: 32555-32564.
11. Cotter, P.D., Hill, C., and Ross, R.P. (2005) Bacteriocins: developing innate immunity for food. Nat Rev Microbiol 3: 777-788.
12. Douglas, L.M., Martin, S.W., and Konopka, J.B. (2009) BAR domain proteins Rvs161 and Rvs167 contribute to Candida albicans endocytosis, morphogenesis, and virulence. Infect Immun 77: 4150-4160.
13. Duchardt, F., Fotin-Mleczek, M., Schwarz, H., Fischer, R., and Brock, R. (2007) A comprehensive model for the cellular uptake of cationic cell-penetrating peptides. Traffic 8: 848-866.
14. Findlay, B., Zhanel, G.G., and Schweizer, F. (2010) Cationic amphiphiles, a new generation of antimicrobials inspired by the natural antimicrobial peptide scaffold. Antimicrob Agents Chemother 54: 4049-4058.
15. Fischer-Parton, S., Parton, R.M., Hickey, P.C., Dijksterhuis, J., Atkinson, H.A., and Read, N.D. (2000) Confocal microscopy of FM4-64 as a tool for analysing endocytosis and vesicle trafficking in living fungal hyphae. J Microsc 198: 246-259.
16. Freitag, M., Hickey, P.C., Raju, N.B., Selker, E.U., and Read, N.D. (2004) GFP as a tool to analyze the organization, dynamics and function of nuclei and microtubules in Neurospora crassa. Fungal Genet Biol 41: 897-910.
17. Gould, G.W., and Lippincott-Schwartz, J. (2009) New roles for endosomes: from vesicular carriers to multi-purpose platforms. Nat Rev Mol Cell Biol 10: 287-292.
18. Hancock, R.E.W., and Sahl, H.G. (2006) Antimicrobial and host-defense peptides as new anti-infective therapeutic strategies. Nat Biotechnol 24: 1551-1557.
19. Haugland, R.P. (1996) Handbook of Fluorescence Probes. Eugene, OR: Molecular Probes.
20. Hauser, M., Narita, V., Donhardt, A.M., Naider, F., and Becker, J.M. (2001) Multiplicity and regulation of genes encoding peptide transporters in Saccharomyces cerevisiae. Mol Membr Biol 18: 105-112.
21. Helmerhorst, E.J., Van't Hof, W., Breeuwer, P., Veerman, E.C.I., Abee, T., Troxler, R.F., etal. (2001) Characterization of Histatin 5 with respect to amphipathicity, hydrophobicity, and effects on cell and mitochondrial membrane integrity excludes a candidacidal mechanism of pore formation. J Biol Chem 276: 5643-5649.
22. Henriques, S.T., Melo, M.N., and Castanho, M.A.R.B. (2006) Cell-penetrating peptides and antimicrobial peptides: how different are they? Biochem J 399: 1-7.
23. Herce, H.D., and Garcia, A.E. (2007) Cell penetrating peptides: how do they do it? J Biol Phys 33: 345-356.
24. Hickey, P.C., Jacobson, D.J., Read, N.D., and Glass, N.L. (2002) Live-cell imaging of vegetative hyphal fusion in Neurospora crassa. Fungal Genet Biol 37: 109-119.
25. Hickey, P.C., Swift, S.R., Roca, M.G., and Read, N.D. (2005) Live-cell imaging of filamentous fungi using vital fluorescent dyes. In Methods in Microbiology, Vol. 34. Microbial Imaging. Savidge, T., and Pothoulakis, C. (eds). Amsterdam: Elsevier, pp. 63-87.
26. Hoffmann, J., and Mendgen, K. (1998) Endocytosis and membrane turnover in the germ tube of Uromyces fabae. Fungal Genet Biol 24: 77-85.
27. Jang, W.S., Li, X.W.S., Sun, J.N.N., and Edgerton, M. (2008) The P-113 fragment of Histatin 5 requires a specific peptide sequence for intracellular translocation in Candida albicans, which is independent of cell wall binding. Antimicrob Agents Chemother 52: 497-504.
28. Jang, W.S., Bajwa, J.S., Sun, J.N., and Edgerton, M. (2010) Salivary histatin 5 internalization by translocation, but not endocytosis, is required for fungicidal activity in Candida albicans. Mol Microbiol 77: 354-370.
29. Janmey, P.A., and Kinnunen, P.K.J. (2006) Biophysical properties of lipids and dynamic membranes. Trends Cell Biol 16: 538-546.
30. Jarver, P., and Langel, U. (2006) Cell-penetrating peptides - a brief introduction. Biochim Biophys Acta 1758: 260-263.
31. Jones, A.T. (2008) Gateways and tools for drug delivery: endocytic pathways and the cellular dynamics of cell penetrating peptides. Int J Pharm 354: 34-38.
32. Jones, S.K. Jr, and Bennett, R.J. (2011) Fungal mating pheromones: choreographing the dating game. Fungal Genet Biol 48: 668-676.
33. Kaksonen, M., Toret, C.P., and Drubin, D.G. (2005) A modular design for the clathrin- and actin-mediated endocytosis machinery. Cell 123: 305-320.
34. Koshlukova, S.E., Lloyd, T.L., Araujo, M.W.B., and Edgerton, M. (1999) Salivary histatin 5 induces non-lytic release of ATP from Candida albicans leading to cell death. J Biol Chem 274: 18872-18879.
35. Kragol, G., Lovas, S., Varadi, G., Condie, B.A., Hoffmann, R., and Otvos, L. Jr (2001) The antibacterial peptide pyrrhocoricin inhibits the ATPase actions of DnaK and prevents chaperone-assisted protein folding. Biochemistry 40: 3016-3026.
36. Leiter, E., Szappanos, H., Oberparleiter, C., Kaiserer, L., Csernoch, L., Pusztahelyi, T., etal. (2005) Antifungal protein PAF severely affects the integrity of the plasma membrane of Aspergillus nidulans and induces an apoptosis-like phenotype. Antimicrob Agents Chemother 49: 2445-2453.
37. Lindgren, M.E. (2000) Cell-penetrating peptides. Trends Pharmacol Sci 21: 99-103.
38. Lis, M., Liu, T.T., Barker, K.S., Rogers, P.D., and Bobek, L.A. (2010) Antimicrobial peptide MUC7 12-mer activates the calcium/calcineurin pathway in Candida albicans. FEMS Yeast Res 10: 579-586.
39. Lobo, D.S., Pereira, I.B., Fragel-Madeira, L., Medeiros, L.N., Cabral, L.M., Faria, J., etal. (2007) Antifungal Pisum sativum defensin 1 interacts with Neurospora crassa cyclin F related to the cell cycle. Biochemistry 46: 987-996.
40. López-García, B., Pérez-Payá, E., and Marcos, J.F. (2002) Identification of novel hexapeptides bioactive against phytopathogenic fungi through screening of a synthetic peptide combinatorial library. Appl Environ Microbiol 68: 2453-2460.
41. López-García, B., Ubhayasekera, W., Gallo, R.L., and Marcos, J.F. (2007) Parallel evaluation of antimicrobial peptides derived from the synthetic PAF26 and the human LL37. Biochem Biophys Res Commun 356: 107-113.
42. López-García, B., Gandía, M., Muñoz, A., Carmona, L., and Marcos, J.F. (2010) A genomic approach highlights common and diverse effects and determinants of susceptibility on the yeast Saccharomyces cerevisiae exposed to distinct antimicrobial peptides. BMC Microbiol 10: 289.
43. Lupetti, A., Paulusma-Annema, A., Welling, M.M., Dogterom-Ballering, H., Brouwer, C.P.J.M., Senesi, S., etal. (2003) Synergistic activity of the N-terminal peptide of human lactoferrin and fluconazole against Candida species. Antimicrob Agents Chemother 47: 262-267.
44. Mania, D., Hilpert, K., Ruden, S., Fischer, R., and Takeshita, N. (2010) Screening for antifungal peptides and their modes of action in Aspergillus nidulans. Appl Environ Microbiol 76: 7102-7108.
45. Marcos, J.F., and Gandía, M. (2009) Antimicrobial peptides: to membranes and beyond. Expert Opin Drug Discov 4: 659-671.
46. Marcos, J.F., Muñoz, A., Pérez-Payá, E., Misra, S., and Lopez-García, B. (2008) Identification and rational design of novel antimicrobial peptides for plant protection. Annu Rev Phytopathol 46: 273-301.
47. Mayor, S., and Pagano, R.E. (2007) Pathways of clathrin-independent endocytosis. Nat Rev Mol Cell Biol 8: 603-612.
48. Mochon, A.B., and Liu, H.P. (2008) The antimicrobial peptide Histatin-5 causes a spatially restricted disruption on the Candida albicans surface, allowing rapid entry of the peptide into the cytoplasm. PLoS Pathog 4: e1000190.
49. Montesinos, E. (2007) Antimicrobial peptides and plant disease control. FEMS Microbiol Lett 270: 1-11.
50. Moreno, A.B., Martínez del Pozo, A., and San Segundo, B. (2006) Biotechnologically relevant enzymes and proteins - antifungal mechanism of the Aspergillus giganteus AFP against the rice blast fungus Magnaporthe grisea. Appl Microbiol Biotechnol 72: 883-895.
51. Muñoz, A., López-García, B., and Marcos, J.F. (2006) Studies on the mode of action of the antifungal hexapeptide PAF26. Antimicrob Agents Chemother 50: 3847-3855.
52. Nelson, G., Kozlova-Zwinderman, O., Collis, A.J., Knight, M.R., Fincham, J.R.S., Stanger, C.P., etal. (2004) Calcium measurement in living filamentous fungi expressing codon-optimized aequorin. Mol Microbiol 52: 1437-1450.
53. Nicolas, P. (2009) Multifunctional host defense peptides: intracellular-targeting antimicrobial peptides. FEBS J 276: 6483-6496.
54. Oberparleiter, C., Kaiserer, L., Haas, H., Ladurner, P., Andratsch, M., and Marx, F. (2003) Active internalization of the Penicillium chrysogenum antifungal protein PAF in sensitive Aspergilli. Antimicrob Agents Chemother 47: 3598-3601.
55. Palma-Guerrero, J., Huang, I.C., Jansson, H.B., Salinas, J., Lopez-Llorca, L.V., and Read, N.D. (2009) Chitosan permeabilizes the plasma membrane and kills cells of Neurospora crassa in an energy dependent manner. Fungal Genet Biol 46: 585-594.
56. Park, C.B., Yi, K.S., Matsuzaki, K., Kim, M.S., and Kim, S.C. (2000) Structure-activity analysis of buforin II, a histone H2A-derived antimicrobial peptide: the proline hinge is responsible for the cell-penetrating ability of buforin II. Proc Natl Acad Sci USA 97: 8245-8250.
57. Peñalva, M.A. (2010) Endocytosis in filamentous fungi: Cinderella gets her reward. Curr Opin Microbiol 13: 1-9.
58. Plásek, J., and Sigler, K. (1996) Slow fluorescent indicators of membrane potential: a survey of different approaches to probe response analysis. J Photochem Photobiol B 33: 101-124.
59. Read, N.D., and Kalkman, E.R. (2003) Does endocytosis occur in fungal hyphae? Fungal Genet Biol 39: 199-203.
60. Richard, J.P., Melikov, K., Vives, E., Ramos, C., Verbeure, B., Gait, M.J., etal. (2003) Cell-penetrating peptides - a reevaluation of the mechanism of cellular uptake. J Biol Chem 278: 585-590.
61. Rydlo, T., Miltz, J., and Mor, A. (2006) Eukaryotic antimicrobial peptides: promises and premises in food safety. J Food Sci 71: R125-R135.
62. Schmidt, N., Mishra, A., Lai, G.H., and Wong, G.C.L. (2010) Arginine-rich cell-penetrating peptides. FEBS Lett 584: 1806-1813.
63. Sebbage, V. (2009) Cell-penetrating peptides and their therapeutic applications. Biosci Horiz 2: 64-72.
64. Seligmann, B.E., Gallin, E.K., Martin, D.L., Shain, W., and Gallin, J.I. (1980) Interaction of chemotactic factors with human polymorphonuclear leukocytes: studies using a membrane potential-sensitive cyanine dye. J Membr Biol 52: 257-272.
65. Sims, P.J., Waggoner, A.S., Wang, C.H., and Hoffman, J.F. (1974) Studies on the mechanism by which cyanine dyes measure membrane potential in red blood cells and phosphatidylcholine vesicles. Biochemistry 13: 3315-3330.
66. Smythe, E., and Ayscough, K.R. (2006) Actin regulation in endocytosis. J Cell Sci 119: 4589-4598.
67. Sun, J.N.N., Li, W.S., Jang, W.S., Nayyar, N., Sutton, M.D., and Edgerton, M. (2008) Uptake of the antifungal cationic peptide Histatin 5 by Candida albicans Ssa2p requires binding to non-conventional sites within the ATPase domain. Mol Microbiol 70: 1246-1260.
68. Thevissen, K., Ghazi, A., De Samblanx, G.W., Brownlee, C., Osborn, R.W., and Broekaert, W.F. (1996) Fungal membrane responses induced by plant defensins and thionins. J Biol Chem 271: 15018-15025.
69. Toret, C.P., and Drubin, D.G. (2006) The budding yeast endocytic pathway. J Cell Sci 119: 4585-4587.
70. Veerman, E.C.I., Valentijn-Benz, M., Nazmi, K., Ruissen, A.L.A., Walgreen-Weterings, E., van Marle, J., etal. (2007) Energy depletion protects Candida albicans against antimicrobial peptides by rigidifying its cell membrane. J Biol Chem 282: 18831-18841.
71. Vogel, H.J. (1956) A convenient growth medium for Neurospora. Microb Genet Bull 13: 42-46.
72. van der Weerden, N.L., Lay, F.T., and Anderson, M.A. (2008) The plant defensin, NaD1, enters the cytoplasm of Fusarium oxysporum hyphae. J Biol Chem 283: 14445-14452.
73. Yount, N.Y., Bayer, A.S., Xiong, Y.Q., and Yeaman, M.R. (2006) Advances in antimicrobial peptide immunobiology. Biopolymers 84: 435-458.
74. Zasloff, M. (2002) Antimicrobial peptides of multicellular organisms. Nature 415: 389-395.
75. Zhu, J., Luther, P.W., Leng, Q., and Mixson, A.J. (2006) Synthetic histidine-rich peptides inhibit Candida species and other fungi in vitro: role of endocytosis and treatment implications. Antimicrob Agents Chemother 50: 2797-2805.