Comparative lipidomics in clinical isolates of Candida albicans reveal crosstalk between mitochondria, cell wall integrity and azole resistance

PLoS ONE

Volumn 7, Issue 6, 2012, Pages

  Singh, Ashutosh ^a   Yadav, Vipin ^a   Prasad, Rajendra ^a  

^a JAWAHARLAL NEHRU UNIVERSITY   (India)

Author keywords

[No Author keywords available]

Indexed keywords

CERAMIDE DERIVATIVE; ERGOSTEROL; FLUCONAZOLE; GLYCEROPHOSPHOLIPID; LIPID; MANNOSYLINOSITOLPHOSPHORYLCERAMIDE DERIVATIVE; PHOSPHATIDYLGLYCEROL; PYRROLE DERIVATIVE; RNA DIRECTED DNA POLYMERASE; UNCLASSIFIED DRUG;

ANTIFUNGAL RESISTANCE; ARTICLE; CANDIDA ALBICANS; CELL MEMBRANE; CELL WALL; CONTROLLED STUDY; DRUG TOLERANCE; FUNGAL STRAIN; FUNGUS ISOLATION; LIPID ANALYSIS; LIPID METABOLISM; LIPIDOMICS; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; MOLECULAR INTERACTION; NONHUMAN; QUALITATIVE RESEARCH; QUANTITATIVE STUDY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANTIFUNGAL AGENTS; CANDIDA ALBICANS; CELL WALL; DRUG RESISTANCE, FUNGAL; FLUCONAZOLE; LIPIDS; MITOCHONDRIA; MITOCHONDRIAL MEMBRANES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

CANDIDA; CANDIDA ALBICANS;

EID: 84863001304     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0039812     Document Type: Article

References (68)

1. Richardson MD, (2005) Changing patterns and trends in systemic fungal infections. J Antimicrob Chemother 56: i5-i11.
2. Pfaller MA, Diekema DJ, (2007) Epidemiology of Invasive Candidiasis: a Persistent Public Health Problem. Clin Microbiol Rev 20: 133-163.
3. Clark TA, Hajjeh RA, (2002) Recent trends in the epidemiology of invasive mycoses. Curr Opin Infect Dis 15: 569-574.
4. Tortorano AM, Kibbler C, Peman J, Bernhardt H, Klingspor L, et al. (2006) Candidaemia in Europe: epidemiology and resistance. Int J Antimicrob Agents 27: 359-366.
5. Prasad R, Kapoor K, (2005) Multidrug resistance in yeast Candida. Int Rev Cytol 242: 215-248.
6. White TC, Marr KA, Bowden RA, (1998) Clinical, cellular, and molecular factors that contribute to antifungal drug resistance. Clin Microbiol Rev 11: 382-402.
7. Sanglard D, Coste A, Ferrari S, (2009) Antifungal drug resistance mechanisms in fungal pathogens from the perspective of transcriptional gene regulation. FEMS Yeast Res 9: 1029-1050.
8. Sanglard D, White TC, (2005) Chapter 14-Molecular Principles of Antifungal Drug Resistance. In: Heitman J, Filler SG, Edwards JE, Mitchell AP, editors. eds. Molecular principles of fungal pathogenesis. Washington, D.C.: ASM Press.197-212.
9. Pasrija R, Panwar SL, 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.
10. Mukhopadhyay K, Prasad T, Saini P, Pucadyil TJ, Chattopadhyay A, et al. (2004) Membrane Sphingolipid- Ergosterol interactions are important determinants of Multidrug Resistance in Candida albicans. Antimicrob Agents Chemother 48: 1778-1787.
11. Pasrija R, Prasad T, Prasad R, (2005) Membrane raft lipid constituents affect drug susceptibilities of Candida albicans. Biochem Soc Trans 33: 1219-1223.
12. Morschhauser J, (2002) The genetic basis of fluconazole resistance development in Candida albicans. Biochim Biophys Acta 1587: 240-248.
13. Marie C, White TC, (2009) Genetic Basis of Antifungal Drug Resistance. Curr Fungal Infect Rep 3: 163-169.
14. Kohli A, Mukhopadhyay K, Rattan A, Prasad R, (2002) In vitro low-level resistance to azoles in Candida albicans is associated with changes in membrane lipid fluidity and asymmetry. Antimicrob Agents Chemother 46: 1046-1052.
15. Mukhopadhyay K, Kohli A, Prasad R, (2002) Drug susceptibilities of yeast cells are affected by membrane lipid composition. Antimicrob Agents Chemother 46: 3695-3705.
16. Singh A, Prasad R, (2011) Comparative lipidomics of azole sensitive and resistant clinical isolates of Candida albicans reveals unexpected diversity in molecular lipid imprints. PLoS One 29 6(4): e19266.
17. White TC, (1997) Increased mRNA Levels of ERG16, CDR, and MDR1 Correlate with Increases in Azole Resistance in Candida albicans Isolates from a Patient Infected with Human Immunodeficiency Virus. Antimicrob Agents Chemother 41: 1482-1487.
18. Bligh EG, Dyer WJ, (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37: 911-917.
19. Han X, Gross RW, (1994) Electrospray ionization mass spectroscopic analysis of human erythrocyte plasma membrane phospholipids. Proc Natl Acad Sci USA 91: 10635- 10639.
20. Shevchenko A, Simons K, (2010) Lipidomics: coming to grips with lipid diversity. Nat Rev Mol Cell Biol 11: 593-598.
21. Singh A, Prasad T, Kapoor K, Mandal A, Roth M, et al. (2010) Phospholipidome of Candida: each species of Candida has distinctive phospholipid molecular species. OMICS 14: 665-677.
22. Schlame M, Rua D, Greenberg ML, (2000) The biosynthesis and functional role of cardiolipin. Prog Lipid Res 39: 257-288.
23. Oliver BG, Silver PM, Marie C, Hoot SJ, Leyde SE, et al. (2008) Tetracycline alters drug susceptibility in Candida albicans and other pathogenic fungi. Microbiol 154: 960-970.
24. Orij R, Postmus J, Beek AT, Brul S, Smits GJ, (2009) In vivo measurement of cytosolic and mitochondrial pH using a pH-sensitive GFP derivative in Saccharomyces cerevisiae reveals a relation between intracellular pH and growth. Microbiol 155: 268-278.
25. Dagley MJ, Gentle IE, Beilharz TH, Pettolino FA, Djordjevic JT, et al. (2011) Cell wall integrity is linked to mitochondria and phospholipid homeostasis in Candida albicans through the activity of the post-transcriptional regulator Ccr4-Pop2. Mol Microbiol 79: 968-989.
26. van Meer G, Voelker DR, Feigenson GW, (2008) Membrane lipids: where they are and how they behave. Nat Rev Mol Cell Biol 9: 112-124.
27. Simons K, (2004) Model Systems, Lipid Rafts, and Cell Membranes. Annu Rev Biophys Biomol Struct 33: 269-295.
28. Zhang Y-Q, Gamarra S, Garcia-Effron G, Park S, Perlin DS, et al. (2010) Requirement for Ergosterol in V-ATPase Function Underlies Antifungal Activity of Azole Drugs. PLoS Pathog 6(6): e1000939. doi:10.1371/journal.ppat.1000939.
29. Tate CG, (2001) Overexpression of mammalian integral membrane proteins for structural studies. FEBS Lett 504: 94-98.
30. Klappe K, Dijkhuis AJ, Hummel I, van Dam A, Ivanova PT, et al. (2010) Extensive sphingolipid depletion does not affect lipid raft integrity or lipid raft localization and efflux function of the ABC transporter MRP1. Biochem J 430: 519-529.
31. DiRusso CC, Black PN, (1999) Long-chain fatty acid transport in bacteria and yeast. Paradigms for defining the mechanism underlying this protein-mediated process. Mol Cell Biochem. 192: 41-52.
32. DiRusso CC, Black PN, (2004) Bacterial Long Chain Fatty Acid Transport: Gateway to a Fatty Acid-responsive Signaling System. J Biol Chem 279: 49563-49566.
33. Janmey PA, Kinnunen PKJ, (2006) Biophysical properties of lipids and dynamic membranes. Trends Cell Biol 16: 538-546.
34. Helmreich EJM, (2003) Environmental influences on signal transduction through membranes: a retrospective mini-review. Biophys Chem 100: 519-534.
35. Baylin A, Kim MK, Donovan-Palmer A, Siles X, Dougherty L, et al. (2005) Fasting Whole Blood as a Biomarker of Essential Fatty Acid Intake in Epidemiologic Studies: Comparison with Adipose Tissue and Plasma. Am J Epidemiol 162: 373-381.
36. Řezanka T, Sigler K, (2009) Odd-numbered very-long-chain fatty acids from the microbial, animal and plant kingdoms. Prog Lipid Res 48: 206-238.
37. Fievez V, Colman E, Castro-Montoya JM, Stefanov I, Vlaeminck B, (2011) Milk odd- and branched-chain fatty acids as biomarkers of rumen function-An update. doi.org/10.1016/j.anifeedsci.2011.12.008.
38. Millar AA, Wrischer M, Kunsta L, (1998) Accumulation of Very-Long-Chain Fatty Acids in Membrane Glycerolipids Is Associated with Dramatic Alterations in Plant Morphology. The Plant Cell 11: 1889-1902.
39. Zhong Q, Gvozdenovic-Jeremic J, Webster P, Zhou J, Greenberg ML, (2005) Loss of Function of KRE5 Suppresses Temperature Sensitivity of Mutants Lacking Mitochondrial Anionic Lipids. Mol Biol Cell 16: 665-675.
40. Ferrari S, Ischer F, Calabrese D, Posteraro B, Sanguinetti M, et al. (2009) Gain of Function Mutations in CgPDR1 of Candida glabrata Not Only Mediate Antifungal Resistance but Also Enhance Virulence. PLoS Pathog 5(1): e1000268. doi:10.1371/journal.ppat.1000268.
41. Ferrari S, Sanguinetti M, Bernardis FD, Torelli R, Posteraro B, et al. (2011) Loss of Mitochondrial Functions Associated with Azole Resistance in Candida glabrata Results in Enhanced Virulence in Mice. Antimicrob Agents Chemother 55: 1852-1860.
42. Osman C, Voelker DR, Langer T, (2011) Making heads or tails of phospholipids in mitochondria. J Cell Biol 192: 7-16.
43. Shingu-Vazquez M, Traven A, (2011) Mitochondria and Fungal Pathogenesis: Drug Tolerance, Virulence, and Potential for Antifungal Therapy. Eukaryot Cell 10: 1376-1383.
44. Cheng S, Clancy CJ, Nguyen KT, Clapp W, Nguyen MH, (2007) A Candida albicans petite mutant strain with uncoupled oxidative phosphorylation overexpresses MDR1 and has diminished susceptibility to fluconazole and voriconazole. Antimicrob Agents Chemother 51: 1855-1858.
45. Kaur R, Castano I, Cormack BP, (2004) Functional genomic analysis of fluconazole susceptibility in the pathogenic yeast Candida glabrata: roles of calcium signaling and mitochondria. Antimicrob Agents Chemother 48: 1600-1613.
46. Tsai HF, Krol AA, Sarti KE, Bennett JE, (2006) Candida glabrata PDR1, a transcriptional regulator of a pleiotropic drug resistance network, mediates azole resistance in clinical isolates and petite mutants. Antimicrob Agents Chemother 50: 1384-1392.
47. Zhang X, Moye-Rowley WS, (2001) Saccharomyces cerevisiae multidrug resistance gene expression inversely correlates with the status of the F(0) component of the mitochondrial ATPase. J Biol Chem 276: 47844-47852.
48. Chen YL, Montedonico AE, Kauffman S, Dunlap JR, Menn FM, et al. (2010) Phosphatidylserine synthase and phosphatidylserine decarboxylase are essential for cell wall integrity and virulence in Candida albicans. Mol Microbiol 75: 1112-1132.
49. Kornmann B, Currie E, Collins SR, Schuldiner M, Nunnari J, et al. (2009) An ER-mitochondria tethering complex revealed by a synthetic biology screen. Science 325: 477-481.
50. Osman C, Haag M, Potting C, Rodenfels J, Dip PV, et al. (2009) The genetic interactome of prohibitins: coordinated control of cardiolipin and phosphatidylethanolamine by conserved regulators in mitochondria. J Cell Biol. 184: 583-596.
51. Tamura Y, Endo T, Iijima M, Sesaki H, (2009) Ups1p and Ups2p antagonistically regulate cardiolipin metabolism in mitochondria. J Cell Biol 185: 1029-1045.
52. Thomas E, Panwar SL, Ansari HR, (2011) PEL1 (Phosphatidylglycerol Phosphate Synthase) is required for mitochondrial function and affects drug susceptibility in C. albicans. In: Human Fungal Pathogens Molecular Mechanism of Host-Pathogen Interactions and Virulence, 4th FEBS Advanced Lecture Course, La Colle sur Loup, France. Abstract P3-15C.
53. Gohil VM, Thompson MN, Greenberg ML, (2005) Synthetic Lethal Interaction of the Mitochondrial Phosphatidylethanolamine and Cardiolipin Biosynthetic Pathways in Saccharomyces cerevisiae. J Biol Chem 280: 35410-35416.
54. Mileykovskaya E, Sun Q, Margolin W, Dowhan W, (1998) Localization and Function of Early Cell Division Proteins in Filamentous Escherichia coli Cells Lacking Phosphatidylethanolamine. J Bacteriol 180: 4252-4257.
55. Li G, Chen S, Thompson MN, Greenberg ML, (2007) New insights into the regulation of cardiolipin biosynthesis in yeast: Implications for Barth syndrome. Biochim Biophys Acta - Mol Cell Biol Lipids 1771: 432-441.
56. Shahi P, Moye-Rowley WS, (2009) Coordinate control of lipid composition and drug transport activities is required for normal multidrug resistance in fungi. Biochim Biophys Acta 1794: 852-859.
57. Birner R, Daum G, (2003) Biogenesis and cellular dynamics of aminoglycerophospholipids. Int Rev Cytol 225: 273-323.
58. Burgermeister M, Birner-Grunberger R, Nebauer R, Daum G, (2004) Contribution of different pathways to the supply of phosphatidylethanolamine and phosphatidylcholine to mitochondrial membranes of the yeast Saccharomyces cerevisiae. Biochim Biophys Acta 1686: 161-168.
59. Voelker DR, (2000) Interorganelle transport of aminoglycerophospholipids. Biochim Biophys Acta 1486: 97-107.
60. Hallstrom TC, Moye-Rowley WS, (2000) Multiple signals from dysfunctional mitochondria activate the pleiotropic drug resistance pathway in Saccharomyces cerevisiae. J Biol Chem 275: 37347-37356.
61. Batova M, Borecka-Melkusova S, Simockova M, Dzugasova V, Goffa E, et al. (2008) Functional characterization of the CgPGS1 gene reveals a link between mitochondrial phospholipid homeostasis and drug resistance in Candida glabrata. Curr Genet 53: 313-322.
62. Gulshan K, Schmidt JA, Shahi P, Moye-Rowley WS, (2008) Evidence for the bifunctional nature of mitochondrial phosphatidylserine decarboxylase: role in Pdr3-dependent retrograde regulation of PDR5 expression. Mol Cell Biol 28: 5851-5864.
63. Devaiah SP, Roth MR, Baughman E, Li M, Tamura P, et al. (2006) Quantitative profiling of polar glycerolipid species from organs of wild-type Arabidopsis and a phospholipase Dalpha1 knockout mutant. Phytochemistry 67: 1907-1924.
64. Welti R, Li W, Li M, Sang Y, Biesiada H, et al. (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.
65. Moore A, Donahue CJ, Bauer KD, Mather JP, (1998) Simultaneous measurement of cell cycle and apoptotic cell death. Meth Cell Biol 57: 265-278.
66. Liu TT, Znaidi S, Barker KS, Xu L, Homayouni R, et al. (2007) Genome-Wide Expression and Location Analyses of the Candida albicans Tac1p Regulon. Eukaryot Cell 6: 2122-2138.
67. Franz R, Ruhnke M, Morschhauser J, (1999) Molecular aspects of fluconazole resistance development in Candida albicans. Mycoses 42: 453-458.
68. Karababa M, Coste AT, Rognon B, Bille J, Sanglard D, (2004) Comparison of Gene Expression Profiles of Candida albicans Azole-Resistant Clinical Isolates and Laboratory Strains Exposed to Drugs Inducing Multidrug Transporters. Antimicrob Agents Chemother 48: 3064-3079.