Natamycin inhibits vacuole fusion at the priming phase via a specific interaction with ergosterol

Antimicrobial Agents and Chemotherapy

Volumn 54, Issue 6, 2010, Pages 2618-2625

  Te Welscher, Yvonne Maria ^a   Jones, Lynden ^b   Van Leeuwen, Martin Richard ^c   Dijksterhuis, Jan ^c   De Kruijff, Ben ^a   Eitzen, Gary ^b   Breukink, Eefjan ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

^b UNIVERSITY OF ALBERTA   (Canada)

^c STATISTICS NETHERLANDS   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ERGOSTEROL; FILIPIN; NATAMYCIN; NYSTATIN;

ARTICLE; CELL VACUOLE; CONTROLLED STUDY; DRUG EFFECT; DRUG MECHANISM; FUNGAL STRAIN; MEMBRANE FUSION; NONHUMAN; PRIORITY JOURNAL; TONOPLAST; YEAST;

ANTIFUNGAL AGENTS; BASE SEQUENCE; DNA PRIMERS; DNA, FUNGAL; ERGOSTEROL; FILIPIN; GENE DELETION; GENES, FUNGAL; MEMBRANE FUSION; MOLECULAR SEQUENCE DATA; NATAMYCIN; NYSTATIN; OXIDOREDUCTASES; PERMEABILITY; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; VACUOLES;

EID: 77952637659     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.01794-09     Document Type: Article

References (37)

1. Baars, T. L., S. Petri, C. Peters, and A. Mayer. 2007. Role of the V-ATPase in regulation of the vacuolar fission-fusion equilibrium. Mol. Biol. Cell 18: 3873-3882.
2. Banta, L. M., J. S. Robinson, D. J. Klionsky, and S. D. Emr. 1988. Organelle assembly in yeast: characterization of yeast mutants defective in vacuolar biogenesis and protein sorting. J. Cell Biol. 107:1369-1383.
3. Bolard, J. 1986. How do the polyene macrolide antibiotics affect the cellular membrane properties? Biochim. Biophys. Acta 864:257-304.
4. Brachmann, C. B., A. Davies, G. J. Cost, E. Caputo, J. Li, P. Hieter, and J. D. Boeke. 1998. Designer deletion strains derived from Saccharomyces cerevisiae S288C: a useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast 14:115-132.
5. Breukink, E., I. Wiedemann, C. van Kraaij, O. P. Kuipers, H. Sahl, and B. de Kruijff. 1999. Use of the cell wall precursor lipid II by a pore-forming peptide antibiotic. Science 286:2361-2364.
6. Brown, D. A., and E. London. 1998. Functions of lipid rafts in biological membranes. Annu. Rev. Cell Dev. Biol. 14:111-136.
7. Burger, K. N. 2000. Greasing membrane fusion and fission machineries. Traffic 1:605-613.
8. Clejan, S., and R. Bittman. 1985. Rates of amphotericin B and filipin association with sterols. A study of changes in sterol structure and phospholipid composition of vesicles. J. Biol. Chem. 260:2884-2889.
9. Conradt, B., A. Haas, and W. Wickner. 1994. Determination of four biochemically distinct, sequential stages during vacuole inheritance in vitro. J. Cell Biol. 126:99-110.
10. de Kruijff, B., and R. A. Demel. 1974. Polyene antibiotic-sterol interactions in membranes of Acholeplasma laidlawii cells and lecithin liposomes. 3. Molecular structure of the polyene antibiotic-cholesterol complexes. Biochim. Biophys. Acta 339:57-70.
11. de Kruijff, B., W. J. Gerritsen, A. Oerlemans, P. W. van Dijck, R. A. Demel, and L. L. van Deenen. 1974. Polyene antibiotic-sterol interactions in membranes of Acholeplasma laidlawii cells and lecithin liposomes. II. Temperature dependence of the polyene antibiotic-sterol complex formation. Biochim. Biophys. Acta 339:44-56.
12. D'Hondt, K., A. Heese-Peck, and H. Riezman. 2000. Protein and lipid requirements for endocytosis. Annu. Rev. Genet. 34:255-295.
13. Eitzen, G., N. Thorngren, and W. Wickner. 2001. Rho1p and Cdc42p act after Ypt7p to regulate vacuole docking. EMBO J. 20:5650-5656. (Pubitemid 33010042)
14. Ghannoum, M. A., and L. B. Rice. 1999. Antifungal agents: mode of action, mechanisms of resistance, and correlation of these mechanisms with bacterial resistance. Clin. Microbiol. Rev. 12:501-517.
15. Haas, A. 1995. A quantitative assay to measure homotypic vacuole fusion in vitro. Methods Cell Sci. 17:283-294.
16. Hasper, H. E., N. E. Kramer, J. L. Smith, J. D. Hillman, C. Zachariah, O. P. Kuipers, B. de Kruijff, and E. Breukink. 2006. An alternative bactericidal mechanism of action for lantibiotic peptides that target lipid II. Science 313:1636-1637.
17. Heese-Peck, A., H. Pichler, B. Zanolari, R. Watanabe, G. Daum, and H. Riezman. 2002. Multiple functions of sterols in yeast endocytosis. Mol. Biol. Cell 13:2664-2680.
18. Isgandarova, S., L. Jones, D. Forsberg, A. Loncar, J. Dawson, K. Tedrick, and G. Eitzen. 2007. Stimulation of actin polymerization by vacuoles via Cdc42p-dependent signaling. J. Biol. Chem. 282:30466-30475.
19. Jin, H., J. M. McCaffery, and E. Grote. 2008. Ergosterol promotes pheromone signaling and plasma membrane fusion in mating yeast. J. Cell Biol. 180:813-826. (Pubitemid 351397780)
20. Kane, P. M. 2006. The where, when, and how of organelle acidification by the yeast vacuolar H+-ATPase. Microbiol. Mol. Biol. Rev. 70:177-191.
21. Kato, M., and W. Wickner. 2001. Ergosterol is required for the Sec18/ATP-dependent priming step of homotypic vacuole fusion. EMBO J. 20:4035-4040. (Pubitemid 32751820)
22. Kitajima, Y., T. Sekiya, and Y. Nozawa. 1976. Freeze-fracture ultrastructural alterations induced by filipin, pimaricin, nystatin and amphotericin B in the plasma membranes of Epidermophyton, Saccharomyces and red complex-induced membrane lesions. Biochim. Biophys. Acta 455:452-465.
23. Mayer, A. 2002. Membrane fusion in eukaryotic cells. Annu. Rev. Cell Dev. Biol. 18:289-314.
24. Munn, A. L., A. Heese-Peck, B. J. Stevenson, H. Pichler, and H. Riezman. 1999. Specific sterols required for the internalization step of endocytosis in yeast. Mol. Biol. Cell 10:3943-3957.
25. Ostrowicz, C. W., C. T. Meiringer, and C. Ungermann. 2008. Yeast vacuole fusion: a model system for eukaryotic endomembrane dynamics. Autophagy 4:5-19.
26. Peters, C., M. J. Bayer, S. Buhler, J. S. Andersen, M. Mann, and A. Mayer. 2001. Trans-complex formation by proteolipid channels in the terminal phase of membrane fusion. Nature 409:581-588.
27. Peters, C., and A. Mayer. 1998. Ca2+/calmodulin signals the completion of docking and triggers a late step of vacuole fusion. Nature 396:575-580.
28. Rodriguez, R. J., C. Low, C. D. Bottema, and L. W. Parks. 1985. Multiple functions for sterols in Saccharomyces cerevisiae. Biochim. Biophys. Acta 837:336-343.
29. Salaun, C., D. J. James, and L. H. Chamberlain. 2004. Lipid rafts and the regulation of exocytosis. Traffic 5:255-264.
30. Simons, K., and E. Ikonen. 1997. Functional rafts in cell membranes. Nature 387:569-572.
31. Tedrick, K., T. Trischuk, R. Lehner, and G. Eitzen. 2004. Enhanced membrane fusion in sterol-enriched vacuoles bypasses the Vrp1p requirement. Mol. Biol. Cell 15:4609-4621.
32. te Welscher, Y. M., H. H. ten Napel, M. Masia Balague, C. M. Souza, H. Riezman, B. de Kruijff, and E. Breukink. 2008. Natamycin blocks fungal growth by binding specifically to ergosterol without permeabilizing the membrane. J. Biol. Chem. 283:6393-6401.
33. Ungermann, C., W. Wickner, and Z. Xu. 1999. Vacuole acidification is required for trans-SNARE pairing, LMA1 release, and homotypic fusion. Proc. Natl. Acad. Sci. U. S. A. 96:11194-11199.
34. Van Leeuwen, M. R., E. A. Golovina, and J. Dijksterhuis. 2009. The polyene antimycotics nystatin and filipin disrupt the plasma membrane, whereas natamycin inhibits endocytosis in germinating conidia of Penicillium discolor. J. Appl. Microbiol. 106:1908-1918.
35. Van Leeuwen, M. R., W. Smant, W. de Boer, and J. Dijksterhuis. 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 germ tube formation. J. Microbiol. Methods 74:64-73.
36. Wickner, W. 2002. Yeast vacuoles and membrane fusion pathways. EMBO J. 21:1241-1247.
37. Wickner, W., and A. Haas. 2000. Yeast homotypic vacuole fusion: a window on organelle trafficking mechanisms. Annu. Rev. Biochem. 69:247-275.