The polyene antimycotics nystatin and filipin disrupt the plasma membrane, whereas natamycin inhibits endocytosis in germinating conidia of Penicillium discolor

Journal of Applied Microbiology

Volumn 106, Issue 6, 2009, Pages 1908-1918

  Van Leeuwen, M R ^a   Golovina, E A ^b   Dijksterhuis, J ^a  

^a CBS KNAW FUNGAL BIODIVERSITY CENTRE   (Netherlands)

^b WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

Conidia; Endocytosis; Filipin; Germination; Natamycin; Nystatin; Penicillium discolor; Polyene antibiotics

Indexed keywords

CELL MEMBRANES; CROPS; FUNGI; MOLECULAR BIOLOGY; ORGANIC COMPOUNDS; SPOILAGE;

ANTIMYCOTICS; CONIDIUM; DOSE-DEPENDENT; ENDOCYTOSE; FILIPIN; NATAMYCIN; NYSTATIN; PENICILLIUM DISCOLOR; POLYENE ANTIBIOTICS; TIME DEPENDENT;

GERMINATION;

ANTIFUNGAL AGENT; FERRIC ION; FERRICYANIDE; FILIPIN; FLUORESCENT DYE; MARKER; NATAMYCIN; NYSTATIN; POLYENE;

ANTIBIOTICS; CELL ORGANELLE; FOOD; FUNGUS; GERMINATION; INFECTIOUS DISEASE; PERMEABILITY; SPORE;

AGRICULTURE; ANTIFUNGAL ACTIVITY; ARTICLE; CELL COMPARTMENTALIZATION; CELL MEMBRANE; CONIDIUM; CROP; DOSE RESPONSE; DRUG MECHANISM; ENDOCYTOSIS; ENDOSOME; FOOD SPOILAGE; FUNGAL CELL; INFECTION; MEMBRANE DAMAGE; MEMBRANE PERMEABILITY; NONHUMAN; PENICILLIUM;

FUNGI; PENICILLIUM DISCOLOR;

EID: 65549143259     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/j.1365-2672.2009.04165.x     Document Type: Article

References (38)

1. Araujo-Bazán, L., Peñalva, M.A. Espeso, E.A. (2008) Preferential localization of the endocytic internalization machinery to hyphal tips underlies polarization of the actin cytoskeleton in Aspergillus nidulans. Mol Microbiol 67, 891 905.
2. Atkinson, H.A., Daniels, A. 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. (Pubitemid 35373795)
3. Baginski, M., Resat, H. McCammon, J.A. (1997) Molecular properties of amphotericin B membrane channel: a molecular dynamics simulation. Mol Pharmacol 52, 560 570. (Pubitemid 27443977)
4. Bolard, J. (1986) How do polyene macrolide antibiotics affect the cellular membrane properties? Biochim Biophys Acta 864, 257 304. (Pubitemid 17228111)
5. Brik, H. (1981) Natamycin. In Analytical Profiles of Drug Substances, Vol 10 ed. Florey, K. pp. 514 561. San Diego : Academic Press.
6. Brul, S. Coote, P. (1999) Preservative agents in foods. Mode of action and microbial resistance mechanism. Int J Food Microbiol 50, 1 17. (Pubitemid 29376427)
7. Chitarra, G.S., Abee, T., Rombouts, F.M. Dijksterhuis, J. (2005) 1-Octen-3-ol inhibits conidia germination of Penicillium paneum despite of mild effects on membrane permeability, respiration, intracellular pH, and changes the protein composition. FEMS Microbiol Ecol 54, 67 75. (Pubitemid 41149004)
8. D'Hondt, K., Heese-Peck, A. Riezman, H. (2000) Protein and lipid requirements for endocytosis. Annu Rev Genet 34, 255 295. (Pubitemid 32065923)
9. De Kruijff, B. Demel, R.A. (1974) Polyene antibiotic-sterol interactions in membranes of Acholeplasma laidlawii cells and lecithin liposomes. III. Molecular structure of the polyene antibiotic-cholesterol complexes. Biochim Biophys Acta 339, 57 70.
10. De Kruijff, B., Gerritsen, W.J., Oerlemans, A., Demel, R.A. Van Deenen, L.L.M. (1974) Polyene antibiotic-sterol interactions in membranes of Acholeplasma laidlawii cells and lecithin liposomes. I. Specificity of the membrane permeability changes induced by the polyene antibiotics. Biochim Biophys Acta 339, 30 43.
11. Dijksterhuis, J., Nijsse, J., Hoekstra, F.A. Golovina, E.A. (2007) High viscosity and anisotropy characterize the cytoplasm of fungal dormant stress-resistant spores. Eukaryot Cell 6, 157 170. (Pubitemid 46303284)
12. Fischer-Parton, S., Parton, R.M., Hickey, P.C., Dijksterhuis, J., Atkinson, H.A. 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. (Pubitemid 30415388)
13. Frisvad, J.C., Samson, R.A., Rassing, B., van der Horst, M.I., Rijn, F.T.J. Stark, J. (1997) Penicillium discolor, a new species from cheese, nuts and vegetables. Antonie Van Leeuwenhoek 72, 119 126. (Pubitemid 27412183)
14. Fuchs, U., Hause, G., Schuchardt, I. Steinberg, G. (2006) Endocytosis is essential for pathogenic development in the corn smut fungus Ustilago maydis. Plant Cell 18, 2066 2081. (Pubitemid 44260197)
15. Ghaunnoum, M.A. Rice, L.B. (1999) Antifungal agents: mode of action, mechanisms of resistance, and correlation of these mechanisms with bacterial resistance. Clin Microbiol Rev 12, 501 517. (Pubitemid 29484744)
16. Hamilton-Miller, J.M.T. (1973) Chemistry and biology of the polyene macrolide antibiotics. Bacteriol Rev 37, 166 196.
17. Heese-Peck, A., Pichler, H., Zanolari, B., Watanabe, R., Daum, G. Riezman, H. (2002) Multiple functions of sterols in yeast endocytosis. Mol Biol Cell 13, 2664 2680.
18. Higuchi, Y., Nakahama, T., Shoji, J., Arioka, M. Kitamoto, K. (2006) Visualization of the endocytic pathway in the filamentous fungus Aspergillus oryzae using an EGFP-fused plasma membrane protein. Biochem Biophys Res Commun 340, 784 791. (Pubitemid 43053898)
19. Kato, M. Wickner, W. (2001) Ergosterol is required for the Sec18/ATP-dependent priming step of homotypic vacuole fusion. EMBO J 20, 4035 4040. (Pubitemid 32751820)
20. Kotler-Brajtburg, J., Medoff, G., Kobayashi, G.S., Boggs, S., Schlessinger, D., Pandey, C. Rinehart, K.L. (1979) Classification of polyene antibiotics according to chemical structure and biological effects. Antimicrob Agents Chemother 15, 716 722. (Pubitemid 9160351)
21. Miller, R.W. (1978) Osmotically induced removal of water from fungal cells as determined by a spin probe technique. Plant Physiol 62, 741 745.
22. Miller, R.W. Barran, L.R. (1977) The effect of ionic surface-active agents on macroconidial plasma membrane of Fusarium sulphureum. Can J Microbiol 23, 1373 1383. (Pubitemid 8205385)
23. Momany, M. (2002) Polarity in filamentous fungi: establishment, maintenance and new axes. Curr Opin Microbiol 5, 580 585. (Pubitemid 35434547)
24. Munn, A.L., Heese-Peck, A., Stevenson, B.J., Pichler, H. Riezman, H. (1999) Specific sterols required for the internalization step of endocytosis in yeast. Mol Biol Cell 10, 3943 3957. (Pubitemid 29534036)
25. Mysyakina, I.S. Funtikova, N.S. (2007) The role of sterols in morphogenetic processes and dimorphism in fungi. Microbiology 76, 1 13. (Pubitemid 46352561)
26. Russell, N.J., Kerridge, D. Gale, E.F. (1975) Polyene sensitivity during germination of conidia of Aspergillus fumigatus. J Gen Microbiol 87, 351 358.
27. Russell, N.J., Kerridge, D. Bokor, J.T. (1977) Sterol metabolism during germination of conidia of Aspergillus fumigatus. J Gen Microbiol 101, 197 206. (Pubitemid 8161832)
28. Stark, J. (2007) Cheese and fermented sausages. In Food Mycology: A Multifaceted Approach to Fungi and Food ed. Dijksterhuis, J. Samson, R.A. pp. 319 331. Boca Raton : CRC press, Taylor & Francis group.
29. Struyk, A.P., Hoette, I., Drost, G., Waisvisz, J.M., Van Eek, T. Hoogerheide, J.C. (1957-1958) Pimaricin, a new antifungal compound. Antibiot Annu 5, 878 885.
30. Taheri-Talesh, N., Horio, T., Araujo-Bazán, L., Dou, X., Espeso, E.A., Peñalva, M.A., Osmani, S.A. Oakley, B.R. (2008) The tip growth apparatus of Aspergillus nidulans. Mol Biol Cell 19, 1439 1449.
31. Takeshita, N., Higashitsuji, Y., Konzack, S. Fischer, R. (2008) Apical sterol-rich membranes are essential for localizing cell end markers that determine growth directionality in the filamentous fungus Aspergillus nidulans. Mol Biol Cell 19, 339 351.
32. Te Welscher, Y.M., Ten Napel, H.H., Masià Balagué, M., Souza, C.M., Riezman, H., De Kruijff, B. Breukink, E. (2008) Natamycin blocks fungal growth by binding specifically to ergosterol without permeabilizing the membrane. J Biol Chem 283, 6393 6401.
33. Teerlink, T., De Kruijff, B. Demel, R.A. (1980) The action of pimaricin, etruscomycin and amphotericin B on liposomes with varying sterol content. Biochim Biophys Acta 599, 484 492.
34. Thanh, N.V., Rombouts, F.M. Nout, M.J. (2007) Viability and physiological state transitions Rhizopus oligosporus sporangiospores in tempe starter culture. Antonie Van Leeuwenhoek 91, 35 44.
35. Upadhyay, S. Shaw, B.D. (2008) The role of actin, fimbrin and endocytosis in growth of hyphae in Aspergillus nidulans. Mol Microbiol 68, 690 705.
36. Van Leeuwen, M.R., Smant, W., De Boer, W. Dijksterhuis, J. (2008) Filipin is a reliable in situ marker of ergosterol in the plasma membrane of germinating conidia (spores) of Penicillium discolor and stains intensively at the site of germtube formation. J Microbiol Methods 74, 64 73.
37. Vida, T.A. Emr, S.D. (1995) A new vital stain for visualizing vacuolar membrane dynamics and endocytosis in yeast. J Cell Biol 128, 779 792.
38. Wedlich-Söldner, R., Bölker, M., Kahman, R. Steinberg, G. (2000) A putative endosomal t-SNARE links exo- and endocytosis in the Phytopathogenic fungus Ustilago maydis. EMBO J 19, 1974 1986. (Pubitemid 30237573)