Lipidomics of Candida albicans biofilms reveals phase-dependent production of phospholipid molecular classes and role for lipid rafts in biofilm formation

References

1. Abu-Elteen K. H., Whittaker P. A. ( 1997-1998). Effect of sub-inhibitory concentration of chlorhexidine on lipid and sterol composition of Candida albicans. Mycopathologia 140:69–76 [View Article][PubMed]
   [Google Scholar]
2. Aeed P. A., Young C. L., Nagiec M. M., Elhammer A. P. ( 2009). Inhibition of inositol phosphorylceramide synthase by the cyclic peptide aureobasidin A. Antimicrob Agents Chemother 53:496–504 [View Article][PubMed]
   [Google Scholar]
3. Ansari S., Prasad R. ( 1993). Effect of miconazole on the structure and function of plasma membrane of Candida albicans. FEMS Microbiol Lett 114:93–98 [View Article][PubMed]
   [Google Scholar]
4. Brügger B., Erben G., Sandhoff R., Wieland F. T., Lehmann W. D. ( 1997). Quantitative analysis of biological membrane lipids at the low picomole level by nano-electrospray ionization tandem mass spectrometry. Proc Natl Acad Sci U S A 94:2339–2344 [View Article][PubMed]
   [Google Scholar]
5. Cerantola V., Guillas I., Roubaty C., Vionnet C., Uldry D., Knudsen J., Conzelmann A. ( 2009). Aureobasidin A arrests growth of yeast cells through both ceramide intoxication and deprivation of essential inositolphosphorylceramides. Mol Microbiol 71:1523–1537 [View Article][PubMed]
   [Google Scholar]
6. Chandra J., McCormick T. S., Imamura Y., Mukherjee P. K., Ghannoum M. A. ( 2007). Interaction of Candida albicans with adherent human peripheral blood mononuclear cells increases C. albicans biofilm formation and results in differential expression of pro- and anti-inflammatory cytokines. Infect Immun 75:2612–2620 [View Article][PubMed]
   [Google Scholar]
7. Chandra J., Mukherjee P. K., Ghannoum M. A. ( 2008). In vitro growth and analysis of Candida biofilms. Nat Protoc 3:1909–1924 [View Article][PubMed]
   [Google Scholar]
8. Chen Y. L., Montedonico A. E., Kauffman S., Dunlap J. R., Menn F. M., Reynolds T. B. ( 2010). Phosphatidylserine synthase and phosphatidylserine decarboxylase are essential for cell wall integrity and virulence in Candida albicans. Mol Microbiol 75:1112–1132 [View Article][PubMed]
   [Google Scholar]
9. Devaiah S. P., Roth M. R., Baughman E., Li M., Tamura P., Jeannotte R., Welti R., Wang X. ( 2006). Quantitative profiling of polar glycerolipid species from organs of wild-type Arabidopsis and a phospholipase Dalpha1 knockout mutant. Phytochemistry 67:1907–1924 [View Article][PubMed]
   [Google Scholar]
10. Dickson R. C., Nagiec E. E., Wells G. B., Nagiec M. M., Lester R. L. ( 1997). Synthesis of mannose-(inositol-P)2-ceramide, the major sphingolipid in Saccharomyces cerevisiae, requires the IPT1 (YDR072c) gene. J Biol Chem 272:29620–29625 [View Article][PubMed]
    [Google Scholar]
11. Dudani A. K., Prasad R. ( 1985). Differences in amino acid transport and phospholipid contents during the cell cycle of Candida albicans. Folia Microbiol (Praha) 30:493–500 [View Article][PubMed]
    [Google Scholar]
12. Ghannoum M. A., Burns G. R., Elteen K. A., Radwan S. S. ( 1986). Experimental evidence for the role of lipids in adherence of Candida spp. to human buccal epithelial cells. Infect Immun 54:189–193[PubMed]
    [Google Scholar]
13. Ghannoum M. A., Swairjo I., Soll D. R. ( 1990). Variation in lipid and sterol contents in Candida albicans white and opaque phenotypes. J Med Vet Mycol 28:103–115 [View Article][PubMed]
    [Google Scholar]
14. Hallstrom T. C., Lambert L., Schorling S., Balzi E., Goffeau A., Moye-Rowley W. S. ( 2001). Coordinate control of sphingolipid biosynthesis and multidrug resistance in Saccharomyces cerevisiae. J Biol Chem 276:23674–23680 [View Article][PubMed]
    [Google Scholar]
15. Hitchcock C. A., Barrett-Bee K. J., Russell N. J. ( 1986). The lipid composition of azole-sensitive and azole-resistant strains of Candida albicans. J Gen Microbiol 132:2421–2431[PubMed]
    [Google Scholar]
16. Hitchcock C. A., Barrett-Bee K. J., Russell N. J. ( 1987). The lipid composition and permeability to azole of an azole- and polyene-resistant mutant of Candida albicans. J Med Vet Mycol 25:29–37 [View Article][PubMed]
    [Google Scholar]
17. Ibrahim A. S., Ghannoum M. A., Prasad R. ( 1996). Chromatographic analysis of lipids. Manual on Membrane Lipids52 Prasad R. New York: Springer-Verlag;
    [Google Scholar]
18. Koul A., Chandra J., Prasad R. ( 1995). Status of membrane lipids and amino acid transport in morphological mutants of Candida albicans. Biochem Mol Biol Int 35:1215–1222[PubMed]
    [Google Scholar]
19. Lattif A. A., Chandra J., Chang J., Liu S., Zhou G., Chance M. R., Ghannoum M. A., Mukherjee P. K. ( 2008). Proteomic and pathway analyses reveal phase-dependent over-expression of proteins associated with carbohydrate metabolic pathways in Candida albicans biofilms. The Open Proteomics Journal 1:5–26 [View Article]
    [Google Scholar]
20. Lomb M., Fryberg M., Oehlschlager A. C., Unrau A. M. ( 1975). Sterol and fatty acid composition of polyene macrolide antibiotic resistant Torulopsis glabrata. Can J Biochem 53:1309–1315 [View Article][PubMed]
    [Google Scholar]
21. Mago N., Khuller G. K. ( 1989). Influence of lipid composition on the sensitivity of Candida albicans to antifungal agents. Indian J Biochem Biophys 26:30–33[PubMed]
    [Google Scholar]
22. Martin S. W., Konopka J. B. ( 2004). Lipid raft polarization contributes to hyphal growth in Candida albicans. Eukaryot Cell 3:675–684 [View Article][PubMed]
    [Google Scholar]
23. Mukherjee P. K., Chandra J., Kuhn D. M., Ghannoum M. A. ( 2003). Mechanism of fluconazole resistance in Candida albicans biofilms: phase-specific role of efflux pumps and membrane sterols. Infect Immun 71:4333–4340 [View Article][PubMed]
    [Google Scholar]
24. Mukherjee P. K., Zhou G., Munyon R., Ghannoum M. A. ( 2005). Candida biofilm: a well-designed protected environment. Med Mycol 43:191–208 [View Article][PubMed]
    [Google Scholar]
25. Nagiec M. M., Nagiec E. E., Baltisberger J. A., Wells G. B., Lester R. L., Dickson R. C. ( 1997). Sphingolipid synthesis as a target for antifungal drugs. Complementation of the inositol phosphorylceramide synthase defect in a mutant strain of Saccharomyces cerevisiae by the AUR1 gene. J Biol Chem 272:9809–9817 [View Article][PubMed]
    [Google Scholar]
26. Pasrija R., Panwar S. L., Prasad R. ( 2008). Multidrug transporters CaCdr1p and CaMdr1p of Candida albicans display different lipid specificities: both ergosterol and sphingolipids are essential for targeting of CaCdr1p to membrane rafts. Antimicrob Agents Chemother 52:694–704 [View Article][PubMed]
    [Google Scholar]
27. Pesti M., Horváth L., Vígh L., Farkas T. ( 1985). Lipid content and ESR determination of plasma membrane order parameter in Candida albicans sterol mutants. Acta Microbiol Hung 32:305–313[PubMed]
    [Google Scholar]
28. Prasad T., Saini P., Gaur N. A., Vishwakarma R. A., Khan L. A., Haq Q. M., Prasad R. ( 2005). Functional analysis of CaIPT1, a sphingolipid biosynthetic gene involved in multidrug resistance and morphogenesis of Candida albicans. Antimicrob Agents Chemother 49:3442–3452 [View Article][PubMed]
    [Google Scholar]
29. Reynolds T. B. ( 2009). Strategies for acquiring the phospholipid metabolite inositol in pathogenic bacteria, fungi and protozoa: making it and taking it. Microbiology 155:1386–1396 [View Article][PubMed]
    [Google Scholar]
30. Siafakas A. R., Wright L. C., Sorrell T. C., Djordjevic J. T. ( 2006). Lipid rafts in Cryptococcus neoformans concentrate the virulence determinants phospholipase B1 and Cu/Zn superoxide dismutase. Eukaryot Cell 5:488–498 [View Article][PubMed]
    [Google Scholar]
31. Singh M., Jayakumar A., Prasad R. ( 1978). The effect of altered lipid composition on the transport of various amino acids in Candida albicans. Arch Biochem Biophys 191:680–686 [View Article][PubMed]
    [Google Scholar]
32. Singh A., Prasad T., Kapoor K., Mandal A., Roth M., Welti R., Prasad R. ( 2010). Phospholipidome of Candida: each species of Candida has distinctive phospholipid molecular species. OMICS 14:665–677 [View Article][PubMed]
    [Google Scholar]
33. Thevissen K., Cammue B. P., Lemaire K., Winderickx J., Dickson R. C., Lester R. L., Ferket K. K., Van Even F., Parret A. H., Broekaert W. F. ( 2000). A gene encoding a sphingolipid biosynthesis enzyme determines the sensitivity of Saccharomyces cerevisiae to an antifungal plant defensin from dahlia (Dahlia merckii). Proc Natl Acad Sci U S A 97:9531–9536 [View Article][PubMed]
    [Google Scholar]
34. Thevissen K., Francois I. E., Aerts A. M., Cammue B. P. ( 2005). Fungal sphingolipids as targets for the development of selective antifungal therapeutics. Curr Drug Targets 6:923–928 [View Article][PubMed]
    [Google Scholar]
35. Toulmay A., Schneiter R. ( 2007). Lipid-dependent surface transport of the proton pumping ATPase: a model to study plasma membrane biogenesis in yeast. Biochimie 89:249–254 [View Article][PubMed]
    [Google Scholar]
36. Wachtler V., Balasubramanian M. K. ( 2006). Yeast lipid rafts? – an emerging view. Trends Cell Biol 16:1–4 [View Article][PubMed]
    [Google Scholar]
37. Welti R., Li W., Li M., Sang Y., Biesiada H., Zhou H. E., Rajashekar C. B., Williams T. D., Wang X. ( 2002). Profiling membrane lipids in plant stress responses. Role of phospholipase D alpha in freezing-induced lipid changes in Arabidopsis. J Biol Chem 277:31994–32002 [View Article][PubMed]
    [Google Scholar]
38. Yeater K. M., Chandra J., Cheng G., Mukherjee P. K., Zhao X., Rodriguez-Zas S. L., Kwast K. E., Ghannoum M. A., Hoyer L. L. ( 2007). Temporal analysis of Candida albicans gene expression during biofilm development. Microbiology 153:2373–2385 [View Article][PubMed]
    [Google Scholar]