The plant defensin RsAFP2 induces cell wall stress, septin mislocalization and accumulation of ceramides in Candida albicans

Molecular Microbiology

Volumn 84, Issue 1, 2012, Pages 166-180

  Thevissen, Karin ^a   De Mello Tavares, Patricia ^b   Xu, Deming ^c   Blankenship, Jill ^d   Vandenbosch, Davy ^e   Idkowiak Baldys, Jolanta ^f   Govaert, Gilmer ^a   Bink, Anna ^a   Rozental, Sonia ^b   De Groot, Piet W J ^g   Davis, Talya R ^h   Kumamoto, Carol A ^h   Vargas, Gabriele ^b   Nimrichter, Leonardo ^b   Coenye, Tom ^e   Mitchell, Aaron ^d   Roemer, Terry ^c   Hannun, Yusuf A ^f   Cammue, Bruno P A ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^c MERCK FROSST CENTRE FOR THERAPEUTIC RESEARCH   (Canada)

^d CARNEGIE MELLON UNIVERSITY   (United States)

^e GHENT UNIVERSITY   (Belgium)

^f MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^g UNIVERSITY OF CASTILLA LA MANCHA   (Spain)

^h TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEFENSIN; GLUCOSYLCERAMIDE; PROTEIN RSAFP2; SEPTIN; UNCLASSIFIED DRUG;

ARTICLE; CANDIDA ALBICANS; CELL STRESS; CELL WALL; CONTROLLED STUDY; FLUORESCENCE ACTIVATED CELL SORTING; FUNGAL CELL; FUNGAL STRAIN; FUNGUS GROWTH; FUNGUS HYPHAE; FUNGUS MUTANT; IMMUNOFLUORESCENCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN LOCALIZATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSMISSION ELECTRON MICROSCOPY;

CANDIDA ALBICANS; CELL WALL; DEFENSINS; GLUCOSYLCERAMIDES; HYPHAE; MICROSCOPY, ELECTRON, TRANSMISSION; PLANT PROTEINS; RAPHANUS; SEPTINS;

CANDIDA ALBICANS; RAPHANUS SATIVUS;

EID: 84863396190     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2012.08017.x     Document Type: Article

References (55)

1. Aerts, A.M., François, I.E., Meert, E.M., Li, Q.T., Cammue, B.P., and 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.
2. Aerts, A.M., François, I.E., Cammue, B.P., and Thevissen, K. (2008) The mode of antifungal action of plant, insect and human defensins. Cell Mol Life Sci 65: 2069-2079.
3. Aerts, A.M., Carmona-Gutierrez, D., Lefevre, S., Govaert, G., François, I.E., Madeo, F., etal. (2009) The antifungal plant defensin RsAFP2 from radish induces apoptosis in a metacaspase independent way in Candida albicans. FEBS Lett 583: 2513-2516.
4. Babour, A., Bicknell, A.A., Tourtellotte, J., and Niwa, M. (2010) A surveillance pathway monitors the fitness of the endoplasmic reticulum to control its inheritance. Cell 142: 256-269.
5. Barreto-Bergter, E., Pinto, M.R., and Rodrigues, M.L. (2004) Structure and biological functions of fungal cerebrosides. An Acad Bras Cienc 76: 67-84.
6. Bielawski, J., Szulc, Z.M., Hannun, Y.A., and Bielawska, A. (2006) Simultaneous quantitative analysis of bioactive sphingolipids by high-performance liquid chromatography-tandem mass spectrometry. Methods 39: 82-91.
7. Bink, A., Govaert, G., François, I.E., Pellens, K., Meerpoel, L., Borgers, M., etal. (2010) A fungicidal piperazine-1-carboxamidine induces mitochondrial fission-dependent apoptosis in yeast. FEMS Yeast Res 10: 812-818.
8. Blankenship, J.R., Fanning, S., Hamaker, J.J., and Mitchell, A.P. (2010) An extensive circuitry for cell wall regulation in Candida albicans. PLoS Pathog 6: e1000752.
9. Boyce, K.J., Chang, H., D'Souza, C.A., and Kronstad, J.W. (2005) An Ustilago maydis septin is required for filamentous growth in culture and for full symptom development on maize. Eukaryot Cell 4: 2044-2056.
10. Cánovas, D., and Pérez-Martín, J. (2009) Sphingolipid biosynthesis is required for polar growth in the dimorphic phytopathogen Ustilago maydis. Fungal Genet Biol 46: 190-200.
11. Cowart, L.A., and Obeid, L.M. (2007) Yeast sphingolipids: recent developments in understanding biosynthesis, regulation, and function. Biochim Biophys Acta 1771: 421-431.
12. De Groot, P.W.J., De Boer, A.D., Cunningham, J., Dekker, H.L., De Jong, L., Hellingwerf, K.J., etal. (2004) Proteomic analysis of Candida albicans cell walls reveals covalently bound carbohydrate-active enzymes and adhesins. Eukaryot Cell 3: 955-965.
13. Drees, B.L., Sundin, B., Brazeau, E., Caviston, J.P., Chen, G.C., Guo, W., etal. (2001) A protein interaction map for cell polarity development. J Cell Biol 154: 549-571.
14. Ferket, K.K., Levery, S.B., Park, C., Cammue, B.P., and Thevissen, K. (2003) Isolation and characterization of Neurospora crassa mutants resistant to antifungal plant defensins. Fungal Genet Biol 40: 176-185.
15. Folch, K., Lees, M., and Soane Stanley, G.H. (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226: 497-509.
16. Fontaine, T., Magnin, T., Melhert, A., Lamont, D., Latge, J.P., and Ferguson, M.A. (2003) Structures of the glycosylphosphatidylinositol membrane anchors from Aspergillus fumigatus membrane proteins. Glycobiology 13: 169-177.
17. Fonzi, W.A., and Irwin, M.Y. (1993) Isogenic strain construction and gene mapping in Candida albicans. Genetics 134: 717-728.
18. François, I.E., De Bolle, M.F., Dwyer, G., Goderis, I.J., Wouters, P.F., Verhaert, P.D., etal. (2002) Transgenic expression in Arabidopsis of a polyprotein construct leading to production of two different antimicrobial proteins. Plant Physiol 128: 1346-1358.
19. François, I.E., Bink, A., Vandercappellen, J., Ayscough, K.R., Toulmay, A., Schneiter, R., etal. (2009) Membrane rafts are involved in intracellular miconazole accumulation in yeast cells. J Biol Chem 284: 32680-32685.
20. Franzen, A.J., Cunha, M.M., Batista, E.J., Seabra, S.H., De Souza, W., and Rozental, S. (2006) Effects of tricyclazole (5-methyl-1, 2, 4-triazol(3, 4) benzothiazole), a specific DHN-melanin inhibitor, on the morphology of Fonsecaea pedrosoi conidia and sclerotic cells. Microsc Res Tech 69: 729-737.
21. Funato, K., and Riezman, H. (2001) Vesicular and nonvesicular transport of ceramide from ER to the Golgi apparatus in yeast. J Cell Biol 155: 949-959.
22. Herath, K., Harris, G., Jayasuriya, H., Zink, D., Smith, S., Vicente, F., etal. (2009) Isolation, structure and biological activity of phomafungin, a cyclic lipodepsipeptide from a widespread tropical Phoma sp. Bioorg Med Chem 17: 1361-1369.
23. Hou, Z., Xue, C., Peng, Y., Katan, T., Kistler, H.C., and Xu, J.R. (2002) A mitogen-activated protein kinase gene (MGV1) in Fusarium graminearum is required for female fertility, heterokaryon formation, and plant infection. Mol Plant Microbe Interact 15: 1119-1127.
24. Kumamoto, C.A. (2005) A contact-activated kinase signals Candida albicans invasive growth and biofilm development. Proc Natl Acad Sci USA 102: 5576-5581.
25. Leipelt, M., Warnecke, D., Zähringer, U., Ott, C., Müller, F., Hube, B., and Heinz, E. (2001) Glucosylceramide synthases, a gene family responsible for the biosynthesis of glucosphingolipids in animals, plants, and fungi. J Biol Chem 276: 33621-33629.
26. 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.
27. Mandala, S.M., Frommer, B.R., Thornton, R.A., Kurtz, M.B., Young, N.M., Cabello, M.A., etal. (1994) Inhibition of serine palmitoyl-transferase activity by lipoxamycin. J Antibiot (Tokyo) 47: 376-379.
28. Mavor, A.L., Thewes, S., and Hube, B. (2005) Systemic fungal infections caused by Candida species: epidemiology, infection process and virulence attributes. Curr Drug Targets 6: 863-874.
29. Nailis, H., Coenye, T., Van Nieuwerburgh, F., Deforce, D., and Nelis, H.J. (2006) Development and evaluation of different normalization strategies for gene expression studies in Candida albicans biofilms by real-time PCR. BMC Mol Biol 7: 25.
30. Nailis, H., Vandenbroucke, R., Tilleman, K., Deforce, D., Nelis, H., and Coenye, T. (2009) Monitoring ALS1 and ALS3 gene expression during in vitro Candida albicans biofilm formation under continuous flow conditions. Mycopathologia 167: 9-17.
31. Noble, S.M., French, S., Kohn, L.A., Chen, V., and Johnson, A.D. (2010) Systematic screens of a Candida albicans homozygous deletion library decouple morphogenetic switching and pathogenicity. Nat Genet 42: 590-598.
32. Pardini, G., De Groot, P.W.J., Coste, A.T., Karababa, M., Klis, F.M., de Koster, C.G., and Sanglard, D. (2006) The CRH family coding for cell wall glycosylphosphatidylinositol proteins with a predicted transglycosidase domain affects cell wall organization and virulence of Candida albicans. J Biol Chem 281: 40399-40411.
33. Park, C., Bennion, B., François, I.E., Ferket, K.K., Cammue, B.P., Thevissen, K., and Levery, S.B. (2005) Neutral glycolipids of the filamentous fungus Neurospora crassa: altered expression in plant defensin-resistant mutants. J Lipid Res 46: 759-768.
34. Park, H.O., Bi, E., Pringle, J.R., and Herskowitz, I. (1997) Two active states of the Ras-related Bud1/Rsr1 protein bind to different effectors to determine yeast cell polarity. Proc Natl Acad Sci USA 94: 4463-4468.
35. Parsons, A.B., Brost, R.L., Ding, H., Li, Z., Zhang, C., Sheikh, B., etal. (2004) Integration of chemical-genetic and genetic interaction data links bioactive compounds to cellular target pathways. Nat Biotechnol 22: 62-69.
36. Ramamoorthy, V., Zhao, X., Snyder, A.K., Xu, J.R., and Shah, D.M. (2007) Two mitogen-activated protein kinase signalling cascades mediate basal resistance to antifungal plant defensins in Fusarium graminearum. Cell Microbiol 9: 1491-1506.
37. Rodrigues, M.L., Travassos, L.R., Miranda, K.R., Franzen, A.J., Rozental, S., de Souza, W., etal. (2000) Human antibodies against a purified glucosylceramide from Cryptococcus neoformans inhibit cell budding and fungal growth. Infect Immun 68: 7049-7060.
38. Sass, V., Schneider, T., Wilmes, M., Körner, C., Tossi, A., Novikova, N., etal. (2010) Human beta-defensin 3 inhibits cell wall biosynthesis in Staphylococci. Infect Immun 78: 2793-2800.
39. Schmitt, P., Wilmes, M., Pugnière, M., Aumelas, A., Bachère, E., Sahl, H.G., etal. (2010) Insight into invertebrate defensin mechanism of action: oyster defensins inhibit peptidoglycan biosynthesis by binding to lipid II. J Biol Chem 285: 29208-29216.
40. Schneider, T., Kruse, T., Wimmer, R., Wiedemann, I., Sass, V., Pag, U., etal. (2010) Plectasin, a fungal defensin, targets the bacterial cell wall precursor Lipid II. Science 328: 1168-1172.
41. Sudbery, P.E. (2001) The germ tubes of Candida albicans hyphae and pseudohyphae show different patterns of septin ring localization. Mol Microbiol 41: 19-31.
42. Tavares, P.M., Thevissen, K., Cammue, B.P., François, I.E., Barreto-Bergter, E., Taborda, C.P., etal. (2008) In vitro activity of the antifungal plant defensin RsAFP2 against Candida isolates and its in vivo efficacy in prophylactic murine models of candidiasis. Antimicrob Agents Chemother 52: 4522-4525.
43. Terras, F.R., Schoofs, H.M., De Bolle, M.F., Van Leuven, F., Rees, S.B., Vanderleyden, J., etal. (1992) Analysis of two novel classes of plant antifungal proteins from radish (Raphanus sativus L.) seeds. J Biol Chem 267: 15301-15309.
44. 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.
45. Thevissen, K., Terras, F.R., and Broekaert, W.F. (1999) Permeabilization of fungal membranes by plant defensins inhibits fungal growth. Appl Environ Microbiol 65: 5451-5458.
46. Thevissen, K., Warnecke, D.C., François, I.E., Leipelt, M., Heinz, E., Ott, C., etal. (2004) Defensins from insects and plants interact with fungal glucosylceramides. J Biol Chem 279: 3900-3905.
47. Thevissen, K., Ayscough, K.R., Aerts, A.M., Du, W., De Brucker, K., Meert, E.M., etal. (2007a) Miconazole induces changes in actin cytoskeleton prior to reactive oxygen species induction in yeast. J Biol Chem 282: 21592-21597.
48. Thevissen, K., Kristensen, H.H., Thomma, B.P., Cammue, B.P., and François, I.E. (2007b) Therapeutic potential of antifungal plant and insect defensins. Drug Discov Today 12: 966-971.
49. Thorpe, G.W., Fong, C.S., Alic, N., Higgins, V.J., and Dawes, I.W. (2004) Cells have distinct mechanisms to maintain protection against different reactive oxygen species: oxidative-stress-response genes. Proc Natl Acad Sci USA 101: 6564-6569.
50. Toenjes, K.A., Munsee, S.M., Ibrahim, A.S., Jeffrey, R., Edwards, J.E., Jr, and Johnson, D.I. (2005) Small-molecule inhibitors of the budded-to-hyphal-form transition in the pathogenic yeast Candida albicans. Antimicrob Agents Chemother 49: 963-972.
51. Toenjes, K.A., Stark, B.C., Brooks, K.M., and Johnson, D.I. (2009) Inhibitors of cellular signalling are cytotoxic or block the budded-to-hyphal transition in the pathogenic yeast Candida albicans. J Med Microbiol 58 (Part 6): 779-790.
52. 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.
53. van der Weerden, N.L., Hancock, R.E., and Anderson, M.A. (2010) Permeabilization of fungal hyphae by the plant defensin NaD1 occurs through a cell wall dependent process. J Biol Chem 285: 37513-37520.
54. Wheeler, R.T., Kombe, D., Agarwala, S.D., and Fink, G.R. (2008) Dynamic, morphotype-specific Candida albicans β-glucan exposure during infection and drug treatment. PLoS Pathog 4: e1000227.
55. Xu, D., Jiang, B., Ketela, T., Lemieux, S., Veillette, K., Martel, N., etal. (2007) Genome-wide fitness test and mechanism-of-action studies of inhibitory compounds in Candida albicans. PLoS Pathog 3: e92.