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

Microbiology

Volumn 157, Issue 11, 2011, Pages 3232-3242

  Lattif, Ali Abdul ^a   Mukherjee, Pranab K ^a   Chandra, Jyotsna ^a   Roth, Mary R ^b   Welti, Ruth ^b   Rouabhia, Mahmoud ^c   Ghannoum, Mahmoud A ^a  

^a UNIVERSITY HOSPITALS OF CLEVELAND   (United States)

^b KANSAS STATE UNIVERSITY   (United States)

^c Faculté des Sciences et de Génie   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AUREOBASIDIN A; INOSITOL PHOSPHOTRANSFERASE; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLETHANOLAMINE; PHOSPHOLIPID; PHOSPHOTRANSFERASE; SPHINGOLIPID; THERMOZYMOCIDIN; UNCLASSIFIED DRUG;

ARTICLE; BIOFILM; BIOSYNTHESIS; CANDIDA ALBICANS; CONTROLLED STUDY; ELECTROSPRAY MASS SPECTROMETRY; FUNGAL CELL; FUNGUS ISOLATION; GENE DISRUPTION; LIPID ANALYSIS; LIPID COMPOSITION; LIPID RAFT; LIPIDOMICS; NONHUMAN; PLANKTON; PRIORITY JOURNAL; SCANNING ELECTRON MICROSCOPY; THIN LAYER CHROMATOGRAPHY;

BIOFILMS; CANDIDA ALBICANS; DEPSIPEPTIDES; FATTY ACIDS, MONOUNSATURATED; FUNGAL PROTEINS; GLYCOSPHINGOLIPIDS; MEMBRANE MICRODOMAINS; PHOSPHOLIPIDS; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; SPHINGOLIPIDS;

CANDIDA; CANDIDA ALBICANS;

EID: 80155127200     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.051086-0     Document Type: Article

References (38)

1. Abu-Elteen, K. H. & Whittaker, P. A. (1997-1998). Effect of subinhibitory concentration of chlorhexidine on lipid and sterol composition of Candida albicans. Mycopathologia 140, 69-76.
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.
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.
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.
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.
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.
7. Chandra, J., Mukherjee, P. K. & Ghannoum, M. A. (2008). In vitro growth and analysis of Candida biofilms. Nat Protoc 3, 1909-1924.
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.
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.
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.
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.
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.
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.
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.
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.
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.
17. Ibrahim, A. S., Ghannoum, M. A. & Prasad, R. (1996). Chromatographic analysis of lipids. In Manual on Membrane Lipids, p. 52. Edited by R. Prasad. New York: Springer-Verlag.
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.
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.
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.
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.
22. Martin, S. W. & Konopka, J. B. (2004). Lipid raft polarization contributes to hyphal growth in Candida albicans. Eukaryot Cell 3, 675-684.
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.
24. Mukherjee, P. K., Zhou, G., Munyon, R. & Ghannoum, M. A. (2005). Candida biofilm: a well-designed protected environment. Med Mycol 43, 191-208.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
36. Wachtler, V. & Balasubramanian, M. K. (2006). Yeast lipid rafts? - an emerging view. Trends Cell Biol 16, 1-4.
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.
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.