Methylation of glycosylated sphingolipid modulates membrane lipid topography and pathogenicity of Cryptococcus neoformans

Cellular Microbiology

Volumn 14, Issue 4, 2012, Pages 500-516

  Singh, Arpita ^a,g   Wang, Haitao ^c   Silva, Liana C ^d   Na, Chongzheng ^c   Prieto, Manuel ^e   Futerman, Anthony H ^f   Luberto, Chiara ^a   Del Poeta, Maurizio ^a,b  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^c University of Notre Dame   (United States)

^d RESEARCH INSTITUTE FOR MEDICINES IMED ULISBOA   (Portugal)

^e INSTITUTO SUPERIOR TÉCNICO   (Portugal)

^f WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^g NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CERAMIDE; CERAMIDE GLUCOSYLTRANSFERASE; FUNGAL ENZYME; GLUCOSYLCERAMIDE; METHYLTRANSFERASE; SPHINGOLIPID C9 METHYLTRANSFERASE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATOMIC FORCE MICROSCOPY; CONTROLLED STUDY; CRYPTOCOCCOSIS; CRYPTOCOCCUS NEOFORMANS; FLUORESCENCE SPECTROSCOPY; FUNGAL CELL; FUNGAL VIRULENCE; FUNGUS GROWTH; FUNGUS MUTANT; GENE MUTATION; LUNG GRANULOMA; LUNG MYCOSIS; MEMBRANE DAMAGE; MENINGOENCEPHALITIS; METHYLATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; WILD TYPE;

ANIMALS; BRAIN; CELL MEMBRANE; CELL MEMBRANE PERMEABILITY; CENTRAL NERVOUS SYSTEM INFECTIONS; CRYPTOCOCCOSIS; CRYPTOCOCCUS NEOFORMANS; GENE EXPRESSION REGULATION, FUNGAL; GENES, FUNGAL; GLUCOSYLCERAMIDES; GRANULOMA; HOST-PATHOGEN INTERACTIONS; HYDROGEN-ION CONCENTRATION; LUNG; MEMBRANE LIPIDS; MENINGOENCEPHALITIS; METHYLATION; METHYLTRANSFERASES; MICE; MICE, INBRED CBA; MICROSCOPY, ATOMIC FORCE; MUTATION; SPECTROMETRY, FLUORESCENCE; SPHINGOLIPIDS; SPHINGOSINE; VIRULENCE;

FILOBASIDIELLA NEOFORMANS; FUNGI;

EID: 84862818711     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2011.01735.x     Document Type: Article

References (84)

1. Alspaugh, J.A., Pukkila-Worley, R., Harashima, T., Cavallo, L.M., Funnell, D., Cox, G.M., etal. (2002) Adenylyl cyclase functions downstream of the Galpha protein Gpa1 and controls mating and pathogenicity of Cryptococcus neoformans. Eukaryot Cell 1: 75-84.
2. Aresta-Branco, F., Cordeiro, A.M., Marinho, H.S., Cyrne, L., Antunes, F., and de Almeida, R.F. (2011) Gel domains in the plasma membrane of Saccharomyces cerevisiae: highly ordered, ergosterol-free, and sphingolipid-enriched lipid rafts. J Biol Chem 286: 5043-5054.
3. Bahn, Y.S., and Muhlschlegel, F.A. (2006) CO2 sensing in fungi and beyond. Curr Opin Microbiol 9: 572-578.
4. Bahn, Y.S., Cox, G.M., Perfect, J.R., and Heitman, J. (2005) Carbonic anhydrase and CO2 sensing during Cryptococcus neoformans growth, differentiation, and virulence. Curr Biol 15: 2013-2020.
5. Baorto, D.M., Gao, Z., Malaviya, R., Dustin, M.L., van der Merwe, A., Lublin, D.M., and Abraham, S.N. (1997) Survival of FimH-expressing enterobacteria in macrophages relies on glycolipid traffic. Nature 389: 636-639.
6. Barrow, D.A., and Lentz, B.R. (1985) Membrane structural domains. Resolution limits using diphenylhexatriene fluorescence decay. Biophys J 48: 221-234.
7. Bielawski, J., Pierce, J.S., Snider, J., Rembiesa, B., Szulc, Z.M., and Bielawska, A. (2009) Comprehensive quantitative analysis of bioactive sphingolipids by high-performance liquid chromatography-tandem mass spectrometry. Methods Mol Biol 579: 443-467.
8. Bligh, E.G., and Dyer, W.J. (1959) A rapid method for total lipid extraction and purification. Can J Biochem Physiol 37: 911-917.
9. Bogdanov, M., Umeda, M., and Dowhan, W. (1999) Phospholipid-assisted refolding of an integral membrane protein. Minimum structural features for phosphatidylethanolamine to act as a molecular chaperone. J Biol Chem 274: 12339-12345.
10. Brown, D.A. (2006) Lipid rafts, detergent-resistant membranes, and raft targeting signals. Physiology 21: 430-439.
11. Brown, D.A., and London, E. (1998) Functions of lipid rafts in biological membranes. Annu Rev Cell Dev Biol 14: 111-136.
12. Burns, A.R. (2007) Atomic force microscopy of lipid domains in supported model membranes. Methods Mol Biol 398: 263-282.
13. Casadevall, A., and Perfect, J.R. (1998) Cryptococcus Neoformans. Washington, DC, USA: ASM Press, 381-405, pp. 271-324.
14. Castro, B.M., de Almeida, R.F., Silva, L.C., Fedorov, A., and Prieto, M. (2007) Formation of ceramide/sphingomyelin gel domains in the presence of an unsaturated phospholipid: a quantitative multiprobe approach. Biophys J 93: 1639-1650.
15. Cleveland, J.P., Anczykowski, B., Schmid, A.E., and Elings, V.B. (1998) Energy dissipation in tapping-mode atomic force microscopy. Appl Phys Lett 72: 2613-2615.
16. Connell, S.D., and Smith, D.A. (2006) The atomic force microscope as a tool for studying phase separation in lipid membranes. Mol Membr Biol 23: 17-28.
17. Datta, K., Bartlett, K.H., Baer, R., Byrnes, E., Galanis, E., Heitman, J., etal. (2009) Spread of Cryptococcus gattii into Pacific Northwest region of the United States. Emerg Infect Dis 15: 1185-1191.
18. Fahy, E., Subramaniam, S., Brown, H.A., Glass, C.K., Merrill, A.H., Jr, Murphy, R.C., etal. (2005) A comprehensive classification system for lipids. J Lipid Res 46: 839-861.
19. Gaber, R.F., Copple, D.M., Kennedy, B.K., Vidal, M., and Bard, M. (1989) The yeast gene ERG6 is required for normal membrane function but is not essential for biosynthesis of the cell-cycle-sparking sterol. Mol Cell Biol 9: 3447-3456.
20. Garcia, J., Shea, J., Alvarez-Vasquez, F., Qureshi, A., Luberto, C., Voit, E.O., and Del Poeta, M. (2008) Mathematical modeling of pathogenicity of Cryptococcus neoformans. Mol Syst Biol 4: 183.
21. Giocondi, M.C., Yamamoto, D., Lesniewska, E., Milhiet, P.E., Ando, T., and Le Grimellec, C. (2010) Surface topography of membrane domains. Biochim Biophys Acta 1798: 703-718.
22. Hakomori, S. (1981) Glycosphingolipids in cellular interaction, differentiation, and oncogenesis. Annu Rev Biochem 50: 733-764.
23. Harder, T., Scheiffele, P., Verkade, P., and Simons, K. (1998) Lipid domain structure of the plasma membrane revealed by patching of membrane components. J Cell Biol 141: 929-942.
24. Hechtberger, P., Zinser, E., Saf, R., Hummel, K., Paltauf, F., and Daum, G. (1994) Characterization, quantification and subcellular localization of inositol-containing sphingolipids of the yeast, Saccharomyces cerevisiae. Eur J Biochem 225: 641-649.
25. Heinz, E. (1996) Plant glycolipids: structure, isolation and analysis. In Advances in Lipid Methodology - 3. Christie, W.W. (ed.). Dundee, UK: The Oily Press, pp. 211-332.
26. Heung, L.J., Luberto, C., Plowden, A., Hannun, Y.A., and Del Poeta, M. (2004) The sphingolipid pathway regulates Pkc1 through the formation of diacylglycerol in Cryptococcus neoformans. J Biol Chem 279: 21144-21153.
27. Heung, L.J., Kaiser, A.E., Luberto, C., and Del Poeta, M. (2005) The role and mechanism of diacylglycerol-protein kinase C1 signaling in melanogenesis by Cryptococcus neoformans. J Biol Chem 280: 28547-28555.
28. Idnurm, A., Bahn, Y.S., Shen, W.C., Rutherford, J.C., and Muhlschlegel, F.A. (2011) Sensing extracellular signals in Cryptococcus neoformans. In Cryptococcus: from Human Pathogen to Model Yeast. Heitman, J., Kozel, T.R., Kwon-Chung, K.J., Perfect, J.R., and Casadevall, A. (eds). Washington, DC, USA: ASM Press, p. 175.
29. Kechichian, T.B., Shea, J., and Del Poeta, M. (2007) Depletion of alveolar macrophages decreases the dissemination of a glucosylceramide-deficient mutant of Cryptococcus neoformans in immunodeficient mice. Infect Immun 75: 4792-4798.
30. Kleinhans, F.W., Lees, N.D., Bard, M., Haak, R.A., and Woods, R.A. (1979) ESR determinations of membrane permeability in a yeast sterol mutant. Chem Phys Lipids 23: 143-154.
31. Lang, T., Bruns, D., Wenzel, D., Riedel, D., Holroyd, P., Thiele, C., and Jahn, R. (2001) SNAREs are concentrated in cholesterol-dependent clusters that define docking and fusion sites for exocytosis. EMBO J 20: 2202-2213.
32. Lazcano, O., Speights, V.O., Jr, Strickler, J.G., Bilbao, J.E., Becker, J., and Diaz, J. (1993) Combined histochemical stains in the differential diagnosis of Cryptococcus neoformans. Mod Pathol 6: 80-84.
33. Lees, N.D., Bard, M., Kemple, M.D., Haak, R.A., and Kleinhans, F.W. (1979) ESR determination of membrane order parameter in yeast sterol mutants. Biochim Biophys Acta 553: 469-475.
34. Leipelt, M., Warnecke, D., Zahringer, U., Ott, C., Muller, F., Hube, B., and Heinz, E. (2001) Glucosylceramide synthases, a gene family responsible for the biosynthesis of glucosphingolipids in animals, plants, and fungi. J Biol Chem 276: 33621-33629.
35. Lin, W.C., Blanchette, C.D., Ratto, T.V., and Longo, M.L. (2007) Lipid domains in supported lipid bilayer for atomic force microscopy. Methods Mol Biol 400: 503-513.
36. Lin, X., and Heitman, J. (2006) The biology of the Cryptococcus neoformans species complex. Annu Rev Microbiol 60: 69-105.
37. Lingwood, D., and Simons, K. (2010) Lipid rafts as a membrane-organizing principle. Science 327: 46-50.
38. Litvintseva, A.P., Thakur, R., Reller, L.B., and Mitchell, T.G. (2005) Prevalence of clinical isolates of Cryptococcus gattii serotype C among patients with AIDS in Sub-Saharan Africa. J Infect Dis 192: 888-892.
39. Luna, L.G. (1992) In Histopathologic methods and color atlas of special stains and tissue artifacts.
40. Lynch, D.V. (1993) Sphingolipids. In Lipid Metabolism in Plants. Moore, T.S.J. (ed.). Boca Raton, FL: CRC Press, pp. 285-308.
41. MacKinnon, R. (2003) Potassium channels. FEBS Lett 555: 62-65.
42. Mandala, S.M., Thornton, R.A., Frommer, B.R., Curotto, J.E., Rozdilsky, W., Kurtz, M.B., etal. (1995) The discovery of australifungin, a novel inhibitor of sphinganine N-acyltransferase from Sporormiella australis. Producing organism, fermentation, isolation, and biological activity. J Antibiot (Tokyo) 48: 349-356.
43. van Meer, G., and Hoetzl, S. (2010) Sphingolipid topology and the dynamic organization and function of membrane proteins. FEBS Lett 584: 1800-1805.
44. van der Meer-Janssen, Y.P., van Galen, J., Batenburg, J.J., and Helms, J.B. (2010) Lipids in host-pathogen interactions: pathogens exploit the complexity of the host cell lipidome. Prog Lipid Res 49: 1-26.
45. Merrill, A.H., Jr, Sullards, M.C., Wang, E., Voss, K.A., and Riley, R.T. (2001) Sphingolipid metabolism: roles in signal transduction and disruption by fumonisins. Environ Health Perspect 109 (Suppl. 2): 283-289.
46. Mogensen, E.G., Janbon, G., Chaloupka, J., Steegborn, C., Fu, M.S., Moyrand, F., etal. (2006) Cryptococcus neoformans senses CO2 through the carbonic anhydrase Can2 and the adenylyl cyclase Cac1. Eukaryot Cell 5: 103-111.
47. Mukherjee, J., Pirofski, L.A., Scharff, M.D., and Casadevall, A. (1993) Antibody-mediated protection in mice with lethal intracerebral Cryptococcus neoformans infection. Proc Natl Acad Sci USA 90: 3636-3640.
48. Muller, D.J. (2008) AFM: a nanotool in membrane biology. Biochemistry 47: 7986-7998.
49. Niemeyer, M.I., Cid, L.P., Barros, L.F., and Sepulveda, F.V. (2001) Modulation of the two-pore domain acid-sensitive K+ channel TASK-2 (KCNK5) by changes in cell volume. J Biol Chem 276: 43166-43174.
50. Niemeyer, M.I., Gonzalez-Nilo, F.D., Zuniga, L., Gonzalez, W., Cid, L.P., and Sepulveda, F.V. (2007) Neutralization of a single arginine residue gates open a two-pore domain, alkali-activated K+ channel. Proc Natl Acad Sci USA 104: 666-671.
51. Noble, S.M., French, S., Kohn, L.A., Chen, V., and Johnson, A.D. (2010) Systematic screens of a Candida albicans homozygous deletion library decouple morphogenetic switching and pathogenicity. Nat Genet 42: 590-598.
52. Oura, T., and Kajiwara, S. (2010) Candida albicans sphingolipid C9-methyltransferase is involved in hyphal elongation. Microbiology 156: 1234-1243.
53. Park, B.J., Wannemuehler, K.A., Marston, B.J., Govender, N., Pappas, P.G., and Chiller, T.M. (2009) Estimation of the current global burden of cryptococcal meningitis among persons living with HIV/AIDS. AIDS 23: 525-530.
54. Park, B.J., Lockhart, S.R., Brandt, M.E., and Chiller, T.M. (2011) Public health importance of cryptococcal disease: epidemiology, burden and control. In Cryptococcus: from Human Pathogen to Model Yeast. Heitman, J., Kozel, T.R., Kwon-Chung, K.J., Perfect, J.R., and Casadevall, A. (eds). Washington, DC, USA: ASM Press, pp. 585-593.
55. Pelling, A.E., Li, Y., Shi, W., and Gimzewski, J.K. (2005) Nanoscale visualization and characterization of Myxococcus xanthus cells with atomic force microscopy. Proc Natl Acad Sci USA 102: 6484-6489.
56. Pralle, A., Keller, P., Florin, E.L., Simons, K., and Horber, J.K. (2000) Sphingolipid-cholesterol rafts diffuse as small entities in the plasma membrane of mammalian cells. J Cell Biol 148: 997-1008.
57. Pruett, S.T., Bushnev, A., Hagedorn, K., Adiga, M., Haynes, C.A., Sullards, M.C., etal. (2008) Biodiversity of sphingoid bases ('sphingosines') and related amino alcohols. J Lipid Res 49: 1621-1639.
58. Ramamoorthy, V., Cahoon, E.B., Thokala, M., Kaur, J., Li, J., and Shah, D.M. (2009) Sphingolipid C-9 methyltransferases are important for growth and virulence but not for sensitivity to antifungal plant defensins in Fusarium graminearum. Eukaryot Cell 8: 217-229.
59. Reyes Mateo, C., Brochon, J.C., Pilar Lillo, M., and Ulises Acuna, A. (1993) Lipid clustering in bilayers detected by the fluorescence kinetics and anisotropy of trans-parinaric acid. Biophys J 65: 2237-2247.
60. Rhome, R., McQuiston, T., Kechichian, T., Bielawska, A., Hennig, M., Drago, M., etal. (2007) Biosynthesis and immunogenicity of glucosylceramide in Cryptococcus neoformans and other human pathogens. Eukaryot Cell 6: 1715-1726.
61. Rhome, R., Singh, A., Kechichian, T., Drago, M., Morace, G., Luberto, C., and Del Poeta, M. (2011) Surface localization of Glucosylceramide during Cryptococcus neoformans infection allows targeting as a potential antifungal. PLoS ONE 6: e15572.
62. Rittershaus, P.C., Kechichian, T.B., Allegood, J.C., Merrill, A.H., Jr, Hennig, M., Luberto, C., and Del Poeta, M. (2006) Glucosylceramide synthase is an essential regulator of pathogenicity of Cryptococcus neoformans. J Clin Invest 116: 1651-1659.
63. Rodrigues, M.L., Travassos, L.R., Miranda, K.R., Franzen, A.J., Rozental, S., de Souza, W., etal. (2000) Human antibodies against a purified glucosylceramide from Cryptococcus neoformans inhibit cell budding and fungal growth. Infect Immun 68: 7049-7060.
64. Roth, B.L., Poot, M., Yue, S.T., and Millard, P.J. (1997) Bacterial viability and antibiotic susceptibility testing with SYTOX green nucleic acid stain. Appl Environ Microbiol 63: 2421-2431.
65. Saito, K., Takakuwa, N., Ohnishi, M., and Oda, Y. (2006) Presence of glucosylceramide in yeast and its relation to alkali tolerance of yeast. Appl Microbiol Biotechnol 71: 515-521.
66. Sandhoff, R. (2010) Very long chain sphingolipids: tissue expression, function and synthesis. FEBS Lett 584: 1907-1913.
67. Scheuring, S., Boudier, T., and Sturgis, J.N. (2007) From high-resolution AFM topographs to atomic models of supramolecular assemblies. J Struct Biol 159: 268-276.
68. Schlicker, C., Hall, R.A., Vullo, D., Middelhaufe, S., Gertz, M., Supuran, C.T., etal. (2009) Structure and inhibition of the CO2-sensing carbonic anhydrase Can2 from the pathogenic fungus Cryptococcus neoformans. J Mol Biol 385: 1207-1220.
69. Schuck, S., Honsho, M., Ekroos, K., Shevchenko, A., and Simons, K. (2003) Resistance of cell membranes to different detergents. Proc Natl Acad Sci USA 100: 5795-5800.
70. Shea, J.M., Kechichian, T.B., Luberto, C., and Del Poeta, M. (2006) The cryptococcal enzyme inositol phosphosphingolipid-phospholipase C confers resistance to the antifungal effects of macrophages and promotes fungal dissemination to the central nervous system. Infect Immun 74: 5977-5988.
71. Sheehan, D.C., and Hrapchak, B.B. (1980) Connective Tissue and Muscle Fiber Stains London, The C.V. Mosby Company. pp. 196-197.
72. Siafakas, A.R., Wright, L.C., Sorrell, T.C., and 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.
73. Singh, A., Qureshi, A., and Del Poeta, M. (2011) Quantitation of cellular components if Cryptococcus neoformans for system biology analysis. Methods Mol Biol 734: 317-333.
74. Sklar, L.A., Hudson, B.S., Petersen, M., and Diamond, J. (1977) Conjugated polyene fatty acids on fluorescent probes: spectroscopic characterization. Biochemistry 16: 813-819.
75. Sonnino, S., Aureli, M., Loberto, N., Chigorno, V., and Prinetti, A. (2010) Fine tuning of cell functions through remodeling of glycosphingolipids by plasma membrane-associated glycohydrolases. FEBS Lett 584: 1914-1922.
76. Ternes, P., Sperling, P., Albrecht, S., Franke, S., Cregg, J.M., Warnecke, D., and Heinz, E. (2006) Identification of fungal sphingolipid C9-methyltransferases by phylogenetic profiling. J Biol Chem 281: 5582-5592.
77. Thevissen, K., Terras, F.R., and Broekaert, W.F. (1999) Permeabilization of fungal membranes by plant defensins inhibits fungal growth. Appl Environ Microbiol 65: 5451-5458.
78. Toffaletti, D.L., Rude, T.H., Johnston, S.A., Durack, D.T., and Perfect, J.R. (1993) Gene transfer in Cryptococcus neoformans by use of biolistic delivery of DNA. J Bacteriol 175: 1405-1411.
79. Tran, D., Carpentier, J.L., Sawano, F., Gorden, P., and Orci, L. (1987) Ligands internalized through coated or noncoated invaginations follow a common intracellular pathway. Proc Natl Acad Sci USA 84: 7957-7961.
80. Vanegas, J.M., Faller, R., and Longo, M.L. (2010) Influence of ethanol on lipid/sterol membranes: phase diagram construction from AFM imaging. Langmuir 26: 10415-10418.
81. Walther, T.C. (2010) Keeping sphingolipid levels nORMal. Proc Natl Acad Sci USA 107: 5701-5702.
82. Warth, R., Barriere, H., Meneton, P., Bloch, M., Thomas, J., Tauc, M., etal. (2004) Proximal renal tubular acidosis in TASK2 K+ channel-deficient mice reveals a mechanism for stabilizing bicarbonate transport. Proc Natl Acad Sci USA 101: 8215-8220.
83. Xu, X., Bittman, R., Duportail, G., Heissler, D., Vilcheze, C., and London, E. (2001) Effect of the structure of natural sterols and sphingolipids on the formation of ordered sphingolipid/sterol domains (rafts). Comparison of cholesterol to plant, fungal, and disease-associated sterols and comparison of sphingomyelin, cerebrosides, and ceramide. J Biol Chem 276: 33540-33546.
84. Yellen, G. (2002) The voltage-gated potassium channels and their relatives. Nature 419: 35-42.