Compositional and immunobiological analyses of extracellular vesicles released by Candida albicans

Cellular Microbiology

Volumn 17, Issue 3, 2015, Pages 389-407

  Vargas, Gabriele ^a   Rocha, Juliana D B ^a   Oliveira, Debora Leite ^a   Albuquerque, Priscila Costa ^a   Frases, Susana ^a   Santos, Suelen S ^b   Nosanchuk, Joshua Daniel ^a   Gomes, Andre Marco Oliveira ^c   Medeiros, Lia C A S ^a   Miranda, Kildare ^a   Sobreira, Tiago J P ^d   Nakayasu, Ernesto S ^e   Arigi, Emma A ^f   Casadevall, Arturo ^a   Guimaraes, Allan J ^g   Rodrigues, Marcio L ^a,h   Freire de Lima, Celio Geraldo ^a   Almeida, Igor C ^f   Nimrichter, Leonardo ^a  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

^c ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^d BRAZILIAN CENTER FOR RESEARCH IN ENERGY AND MATERIALS CNPEM   (Brazil)

^e PURDUE UNIVERSITY   (United States)

^f UNIVERSITY OF TEXAS AT EL PASO   (United States)

^g FLUMINENSE FEDERAL UNIVERSITY   (Brazil)

^h INSTITUTO OSWALDO CRUZ   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

CD86 ANTIGEN; ERGOSTEROL; GLUCOSYLCERAMIDE; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 12P40; LANOSTEROL; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MANNOPROTEIN; NITRIC OXIDE; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; FUNGAL PROTEIN; FUNGUS ANTIGEN; IMMUNOLOGIC FACTOR; LIPID; PROTEOME;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW DERIVED DENDRITIC CELL; BONE MARROW DERIVED MACROPHAGE; CANDIDA ALBICANS; CARBOHYDRATE METABOLISM; CONTROLLED STUDY; CYTOKINE PRODUCTION; EXTRACELLULAR VESICLE; FUNGAL STRUCTURES; FUNGAL VIRULENCE; GALLERIA MELLONELLA; IMMUNOBIOLOGY; IMMUNOBLOTTING; IMMUNOMODULATION; LARVA; LIGHT SCATTERING; LIPID METABOLISM; MOUSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEOMICS; THIN LAYER CHROMATOGRAPHY; TRANSMISSION ELECTRON MICROSCOPY; UPREGULATION; ANIMAL; CELL CULTURE; CHEMISTRY; CYTOLOGY; DENDRITIC CELL; ENDOCYTOSIS; IMMUNOLOGY; MACROPHAGE; METABOLISM; MOLECULAR WEIGHT; SECRETORY VESICLE; ULTRASTRUCTURE;

AJELLOMYCES CAPSULATUS; CANDIDA ALBICANS; FILOBASIDIELLA NEOFORMANS; GALLERIA MELLONELLA; MALASSEZIA SYMPODIALIS; MURINAE; PARACOCCIDIOIDES BRASILIENSIS; SPOROTHRIX SCHENCKII;

ANIMALS; ANTIGENS, FUNGAL; CANDIDA ALBICANS; CELLS, CULTURED; CHROMATOGRAPHY, THIN LAYER; DENDRITIC CELLS; ENDOCYTOSIS; FUNGAL PROTEINS; IMMUNOLOGIC FACTORS; INTERLEUKIN-12; LIPIDS; MACROPHAGES; MICE; MICROSCOPY, ELECTRON, TRANSMISSION; MOLECULAR WEIGHT; NITRIC OXIDE; PROTEOME; SECRETORY VESICLES; TRANSFORMING GROWTH FACTOR BETA;

EID: 84925052199     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/cmi.12374     Document Type: Article

References (109)

1. Abdullah, Z., Schlee, M., Roth, S., Mraheil, M.A., Barchet, W., Bottcher, J., etal. (2012) RIG-I detects infection with live Listeria by sensing secreted bacterial nucleic acids. EMBO J 31: 4153-4164.
2. Albuquerque, P.C., Nakayasu, E.S., Rodrigues, M.L., Frases, S., Casadevall, A., Zancope-Oliveira, R.M., etal. (2008a) Vesicular transport in Histoplasma capsulatum: an effective mechanism for trans-cell wall transfer of proteins and lipids in ascomycetes. Cell Microbiol 10: 1695-1710.
3. Albuquerque, P.C., Nakayasu, E.S., Rodrigues, M.L., Frases, S., Casadevall, A., Zancope-Oliveira, R.M., etal. (2008b) Vesicular transport in Histoplasma capsulatum: an effective mechanism for trans-cell wall transfer of proteins and lipids in ascomycetes. Cell Microbiol 10: 1695-1710.
4. Anderson, J., Mihalik, R., and Soll, D.R. (1990) Ultrastructure and antigenicity of the unique cell wall pimple of the Candida opaque phenotype. J Bacteriol 172: 224-235.
5. Arendrup, M.C. (2010) Epidemiology of invasive candidiasis. Curr Opin Crit Care 16: 445-452.
6. Azie, N., Neofytos, D., Pfaller, M., Meier-Kriesche, H.U., Quan, S.P., and Horn, D. (2012) The PATH (Prospective Antifungal Therapy) Alliance(R) registry and invasive fungal infections: update 2012. Diagn Microbiol Infect Dis 73: 293-300.
7. Barbosa, F.M., Fonseca, F.L., Figueiredo, R.T., Bozza, M.T., Casadevall, A., Nimrichter, L., and Rodrigues, M.L. (2007) Binding of glucuronoxylomannan to the CD14 receptor in human A549 alveolar cells induces interleukin-8 production. Clin Vaccine Immunol 14: 94-98.
8. Barreto-Bergter, E., Pinto, M.R., and Rodrigues, M.L. (2004) Structure and biological functions of fungal cerebrosides. An Acad Bras Cienc 76: 67-84.
9. Batanghari, J.W., Deepe, G.S., Jr, Di Cera, E., and Goldman, W.E. (1998) Histoplasma acquisition of calcium and expression of CBP1 during intracellular parasitism. Mol Microbiol 27: 531-539.
10. Bayer-Santos, E., Aguilar-Bonavides, C., Rodrigues, S.P., Cordero, E.M., Marques, A.F., Varela-Ramirez, A., etal. (2013) Proteomic analysis of Trypanosoma cruzi secretome: characterization of two populations of extracellular vesicles and soluble proteins. J Proteome Res 12: 883-897.
11. Bayona, J.C., Nakayasu, E.S., Laverriere, M., Aguilar, C., Sobreira, T.J., Choi, H., etal. (2011) SUMOylation pathway in Trypanosoma cruzi: functional characterization and proteomic analysis of target proteins. Mol Cell Proteomics 10 (M110): 007369.
12. Bergin, D., Reeves, E.P., Renwick, J., Wientjes, F.B., and Kavanagh, K. (2005) Superoxide production in Galleria mellonella hemocytes: identification of proteins homologous to the NADPH oxidase complex of human neutrophils. Infect Immun 73: 4161-4170.
13. Bomberger, J.M., Maceachran, D.P., Coutermarsh, B.A., Ye, S., O'Toole, G.A., and Stanton, B.A. (2009) Long-distance delivery of bacterial virulence factors by Pseudomonas aeruginosa outer membrane vesicles. PLoS Pathog 5: e1000382.
14. Braga-Silva, L.A., and Santos, A.L. (2011) Aspartic protease inhibitors as potential anti-Candida albicans drugs: impacts on fungal biology, virulence and pathogenesis. Curr Med Chem 18: 2401-2419.
15. Braga-Silva, L.A., Mesquita, D.G., Ribeiro, M.D., Carvalho, S.M., Fracalanzza, S.E., and Santos, A.L. (2009) Trailing end-point phenotype antibiotic-sensitive strains of Candida albicans produce different amounts of aspartyl peptidases. Br J Med Biol Res 42: 765-770.
16. Brennan, M., Thomas, D.Y., Whiteway, M., and Kavanagh, K. (2002) Correlation between virulence of Candida albicans mutants in mice and Galleria mellonella larvae. FEMS Immunol Med Microbiol 34: 153-157.
17. Bruckmann, A., Kunkel, W., Augsten, K., Wetzker, R., and Eck, R. (2001) The deletion of CaVPS34 in the human pathogenic yeast Candida albicans causes defects in vesicle-mediated protein sorting and nuclear segregation. Yeast 18: 343-353.
18. Calderone, R., and Wadsworth, E. (1987) Characterization with crossed immunoelectrophoresis of some antigens differentiating a virulent Candida albicans from its derived, avirulent strain. Proc Soc Exp Biol Med 185: 325-334.
19. Chatterjee, D., and Chaudhuri, K. (2011) Association of cholera toxin with Vibrio cholerae outer membrane vesicles which are internalized by human intestinal epithelial cells. FEBS Lett 585: 1357-1362.
20. Cheng, S.C., Joosten, L.A., Kullberg, B.J., and Netea, M.G. (2012) Interplay between Candida albicans and the mammalian innate host defense. Infect Immun 80: 1304-1313.
21. Concia, E., Azzini, A.M., and Conti, M. (2009) Epidemiology, incidence and risk factors for invasive candidiasis in high-risk patients. Drugs 69 (Suppl. 1): 5-14.
22. Cotter, G., Doyle, S., and Kavanagh, K. (2000) Development of an insect model for the in vivo pathogenicity testing of yeasts. FEMS Immunol Med Microbiol 27: 163-169.
23. Crowe, J.D., Sievwright, I.K., Auld, G.C., Moore, N.R., Gow, N.A., and Booth, N.A. (2003) Candida albicans binds human plasminogen: identification of eight plasminogen-binding proteins. Mol Microbiol 47: 1637-1651.
24. De Jesus, M., Park, C.G., Su, Y., Goldman, D.L., Steinman, R.M., and Casadevall, A. (2008) Spleen deposition of Cryptococcus neoformans capsular glucuronoxylomannan in rodents occurs in red pulp macrophages and not marginal zone macrophages expressing the C-type lectin SIGN-R1. Med Mycol 46: 153-162.
25. Deatherage, B.L., and Cookson, B.T. (2012) Membrane vesicle release in bacteria, eukaryotes, and archaea: a conserved yet underappreciated aspect of microbial life. Infect Immun 80: 1948-1957.
26. Decote-Ricardo, D., Chagas, K.K., Rocha, J.D., Redner, P., Lopes, U.G., Cambier, J.C., etal. (2009) Modulation of in vitro murine B-lymphocyte response by curcumin. Phytomedicine 16: 982-988.
27. Dong, Z.M., Jackson, L., and Murphy, J.W. (1999) Mechanisms for induction of L-selectin loss from T lymphocytes by a cryptococcal polysaccharide, glucuronoxylomannan. Infect Immun 67: 220-229.
28. Dubreuil, J.D. (2012) The whole Shebang: the gastrointestinal tract, Escherichia coli enterotoxins and secretion. Curr Issues Mol Biol 14: 71-82.
29. Eisenman, H.C., Frases, S., Nicola, A.M., Rodrigues, M.L., and Casadevall, A. (2009) Vesicle-associated melanization in Cryptococcus neoformans. Microbiology 155: 3860-3867.
30. Folch, J., Lees, M., and Sloane Stanley, G.H. (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226: 497-509.
31. Gacser, A., Stehr, F., Kroger, C., Kredics, L., Schafer, W., and Nosanchuk, J.D. (2007) Lipase 8 affects the pathogenesis of Candida albicans. Infect Immun 75: 4710-4718.
32. Gehrmann, U., Qazi, K.R., Johansson, C., Hultenby, K., Karlsson, M., Lundeberg, L., etal. (2011) Nanovesicles from Malassezia sympodialis and host exosomes induce cytokine responses - novel mechanisms for host-microbe interactions in atopic eczema. PLoS ONE 6: e21480.
33. Gil, M.L., Dagan, S., Eren, R., and Gozalbo, D. (2006) Evaluation of the usefulness of anti-glyceraldehyde-3-phosphate dehydrogenase antibodies as a treatment for invasive candidiasis in a murine model. Antonie Van Leeuwenhoek 89: 345-350.
34. Gow, N.A., and Hube, B. (2012a) Importance of the Candida albicans cell wall during commensalism and infection. Curr Opin Microbiol 15: 406-412.
35. Gow, N.A., van de Veerdonk, F.L., Brown, A.J., and Netea, M.G. (2012b) Candida albicans morphogenesis and host defence: discriminating invasion from colonization. Nat Rev Microbiol 10: 112-122.
36. Grechi, J., Marinho-Carvalho, M., Zancan, P., Cinelli, L.P., Gomes, A.M., Rodrigues, M.L., etal. (2011) Glucuronoxylomannan from Cryptococcus neoformans down-regulates the enzyme 6-phosphofructo-1-kinase of macrophages. J Biol Chem 286: 14820-14829.
37. Green, L.C., Wagner, D.A., Glogowski, J., Skipper, P.L., Wishnok, J.S., and Tannenbaum, S.R. (1982) Analysis of nitrate, nitrite, and [15N]nitrate in biological fluids. Anal Biochem 126: 131-138.
38. Guimaraes, A.J., Nakayasu, E.S., Sobreira, T.J., Cordero, R.J., Nimrichter, L., Almeida, I.C., and Nosanchuk, J.D. (2011) Histoplasma capsulatum heat-shock 60 orchestrates the adaptation of the fungus to temperature stress. PLoS ONE 6: e14660.
39. Hazen, K.C. (1995) New and emerging yeast pathogens. Clin Microbiol Rev 8: 462-478.
40. Heinsbroek, S.E., Brown, G.D., and Gordon, S. (2005) Dectin-1 escape by fungal dimorphism. Trends Immunol 26: 352-354.
41. Hoffmann, J.A. (1995) Innate immunity of insects. Curr Opin Immunol 7: 4-10.
42. Huang, S.H., Wu, C.H., Chang, Y.C., Kwon-Chung, K.J., Brown, R.J., and Jong, A. (2012) Cryptococcus neoformans-derived microvesicles enhance the pathogenesis of fungal brain infection. PLoS ONE 7: e48570.
43. Jones, C.M., Goldfarb, R.H., and Holden, H.T. (1983) Macrophage cell lines behave as activated macrophages in the production and regulation of plasminogen activator. Cancer Invest 1: 207-213.
44. Jouault, T., Sarazin, A., Martinez-Esparza, M., Fradin, C., Sendid, B., and Poulain, D. (2009) Host responses to a versatile commensal: PAMPs and PRRs interplay leading to tolerance or infection by Candida albicans. Cell Microbiol 11: 1007-1015.
45. Kaparakis, M., Turnbull, L., Carneiro, L., Firth, S., Coleman, H.A., Parkington, H.C., etal. (2010) Bacterial membrane vesicles deliver peptidoglycan to NOD1 in epithelial cells. Cell Microbiol 12: 372-385.
46. Karkowska-Kuleta, J., Kedracka-Krok, S., Rapala-Kozik, M., Kamysz, W., Bielinska, S., Karafova, A., and Kozik, A. (2011) Molecular determinants of the interaction between human high molecular weight kininogen and Candida albicans cell wall: identification of kininogen-binding proteins on fungal cell wall and mapping the cell wall-binding regions on kininogen molecule. Peptides 32: 2488-2496.
47. Kelly, J., and Kavanagh, K. (2010) Proteomic analysis of proteins released from growth-arrested Candida albicans following exposure to caspofungin. Med Mycol 48: 598-605.
48. Kim, J., and Sudbery, P. (2011) Candida albicans, a major human fungal pathogen. J Microbiol 49: 171-177.
49. Kmetzsch, L., Joffe, L.S., Staats, C.C., de Oliveira, D.L., Fonseca, F.L., Cordero, R.J., etal. (2011) Role for Golgi reassembly and stacking protein (GRASP) in polysaccharide secretion and fungal virulence. Mol Microbiol 81: 206-218.
50. Kuehn, M.J., and Kesty, N.C. (2005) Bacterial outer membrane vesicles and the host-pathogen interaction. Genes Dev 19: 2645-2655.
51. Long, K.H., Gomez, F.J., Morris, R.E., and Newman, S.L. (2003) Identification of heat shock protein 60 as the ligand on Histoplasma capsulatum that mediates binding to CD18 receptors on human macrophages. J Immunol 170: 487-494.
52. Lopez-Ribot, J.L., Gozalbo, D., Sepulveda, P., Casanova, M., and Martinez, J.P. (1995) Preliminary characterization of the material released to the culture medium by Candida albicans yeast and mycelial cells. Antonie Van Leeuwenhoek 68: 195-201.
53. Luo, Z.Q. (2012) Legionella secreted effectors and innate immune responses. Cell Microbiol 14: 19-27.
54. Lutz, M.B., Kukutsch, N., Ogilvie, A.L., Rossner, S., Koch, F., Romani, N., and Schuler, G. (1999) An advanced culture method for generating large quantities of highly pure dendritic cells from mouse bone marrow. J Immunol Methods 223: 77-92.
55. Marcos, C.M., de Fatima da Silva, J., de Oliveira, H.C., Moraes da Silva, R.A., Mendes-Giannini, M.J., and Fusco-Almeida, A.M. (2012) Surface-expressed enolase contributes to the adhesion of Paracoccidioides brasiliensis to host cells. FEMS Yeast Res 12: 557-570.
56. Mayer, F.L., Wilson, D., and Hube, B. (2013) Candida albicans pathogenicity mechanisms. Virulence 4: 119-128.
57. Momose, I., Terashima, M., Nakashima, Y., Sakamoto, M., Ishino, H., Nabika, T., etal. (2000) Phorbol ester synergistically increases interferon regulatory factor-1 and inducible nitric oxide synthase induction in interferon-gamma-treated RAW 264.7 cells. Biochim Biophys Acta 1498: 19-31.
58. Monari, C., Bevilacqua, S., Piccioni, M., Pericolini, E., Perito, S., Calvitti, M., etal. (2009) A microbial polysaccharide reduces the severity of rheumatoid arthritis by influencing Th17 differentiation and proinflammatory cytokines production. J Immunol 183: 191-200.
59. Naglik, J.R., Challacombe, S.J., and Hube, B. (2003a) Candida albicans secreted aspartyl proteinases in virulence and pathogenesis. Microbiol Mol Biol Rev 67: 400-428, table of contents.
60. Naglik, J.R., Rodgers, C.A., Shirlaw, P.J., Dobbie, J.L., Fernandes-Naglik, L.L., Greenspan, D., etal. (2003b) Differential expression of Candida albicans secreted aspartyl proteinase and phospholipase B genes in humans correlates with active oral and vaginal infections. J Infect Dis 188: 469-479.
61. Nakayasu, E.S., Sobreira, T.J., Torres, R., Jr, Ganiko, L., Oliveira, P.S., Marques, A.F., and Almeida, I.C. (2012) Improved proteomic approach for the discovery of potential vaccine targets in Trypanosoma cruzi. J Proteome Res 11: 237-246.
62. Naslavsky, N., Stein, R., Yanai, A., Friedlander, G., and Taraboulos, A. (1997) Characterization of detergent-insoluble complexes containing the cellular prion protein and its scrapie isoform. J Biol Chem 272: 6324-6331.
63. Netea, M.G., and Marodi, L. (2010) Innate immune mechanisms for recognition and uptake of Candida species. Trends Immunol 31: 346-353.
64. Newport, G., Kuo, A., Flattery, A., Gill, C., Blake, J.J., Kurtz, M.B., etal. (2003) Inactivation of Kex2p diminishes the virulence of Candida albicans. J Biol Chem 278: 1713-1720.
65. Nicola, A.M., Frases, S., and Casadevall, A. (2009) Lipophilic dye staining of Cryptococcus neoformans extracellular vesicles and capsule. Eukaryot Cell 8: 1373-1380.
66. Nimrichter, L., Rodrigues, M.L., Rodrigues, E.G., and Travassos, L.R. (2005) The multitude of targets for the immune system and drug therapy in the fungal cell wall. Microbes Infect 7: 789-798. [Epub 2005 Mar].
67. Nisini, R., Romagnoli, G., Gomez, M.J., La Valle, R., Torosantucci, A., Mariotti, S., etal. (2001) Antigenic properties and processing requirements of 65-kilodalton mannoprotein, a major antigen target of anti-Candida human T-cell response, as disclosed by specific human T-cell clones. Infect Immun 69: 3728-3736.
68. 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.
69. Nucci, M., Queiroz-Telles, F., Tobon, A.M., Restrepo, A., and Colombo, A.L. (2010) Epidemiology of opportunistic fungal infections in Latin America. Clin Infect Dis 51: 561-570.
70. Odorizzi, G., Katzmann, D.J., Babst, M., Audhya, A., and Emr, S.D. (2003) Bro1 is an endosome-associated protein that functions in the MVB pathway in Saccharomyces cerevisiae. J Cell Sci 116: 1893-1903.
71. Oliveira, D.L., Nimrichter, L., Miranda, K., Frases, S., Faull, K.F., Casadevall, A., and Rodrigues, M.L. (2009) Cryptococcus neoformans cryoultramicrotomy and vesicle fractionation reveals an intimate association between membrane lipids and glucuronoxylomannan. Fungal Genet Biol 46: 956-963.
72. Oliveira, D.L., Freire-de-Lima, C.G., Nosanchuk, J.D., Casadevall, A., Rodrigues, M.L., and Nimrichter, L. (2010a) Extracellular vesicles from Cryptococcus neoformans modulate macrophage functions. Infect Immun 78: 1601-1609.
73. Oliveira, D.L., Nakayasu, E.S., Joffe, L.S., Guimaraes, A.J., Sobreira, T.J., Nosanchuk, J.D., etal. (2010b) Characterization of yeast extracellular vesicles: evidence for the participation of different pathways of cellular traffic in vesicle biogenesis. PLoS ONE 5: e11113.
74. O'Leary, S., O'sullivan, M.P., and Keane, J. (2011) IL-10 blocks phagosome maturation in mycobacterium tuberculosis-infected human macrophages. Am J Respir Cell Mol Biol 45: 172-180.
75. Pappas, P.G., Rex, J.H., Sobel, J.D., Filler, S.G., Dismukes, W.E., Walsh, T.J., and Edwards, J.E. (2004) Guidelines for treatment of candidiasis. Clin Infect Dis 38: 161-189.
76. Pfaller, M.A., and Diekema, D.J. (2007) Epidemiology of invasive candidiasis: a persistent public health problem. Clin Microbiol Rev 20: 133-163.
77. Pietrella, D., Mazzolla, R., Lupo, P., Pitzurra, L., Gomez, M.J., Cherniak, R., and Vecchiarelli, A. (2002) Mannoprotein from Cryptococcus neoformans promotes T-helper type 1 anticandidal responses in mice. Infect Immun 70: 6621-6627.
78. Pietrella, D., Bistoni, G., Corbucci, C., Perito, S., and Vecchiarelli, A. (2006) Candida albicans mannoprotein influences the biological function of dendritic cells. Cell Microbiol 8: 602-612.
79. Pitarch, A., Diez-Orejas, R., Molero, G., Pardo, M., Sanchez, M., Gil, C., and Nombela, C. (2001) Analysis of the serologic response to systemic Candida albicans infection in a murine model. Proteomics 1: 550-559.
80. Pitarch, A., Abian, J., Carrascal, M., Sanchez, M., Nombela, C., and Gil, C. (2004) Proteomics-based identification of novel Candida albicans antigens for diagnosis of systemic candidiasis in patients with underlying hematological malignancies. Proteomics 4: 3084-3106.
81. Pitarch, A., Jimenez, A., Nombela, C., and Gil, C. (2006) Decoding serological response to Candida cell wall immunome into novel diagnostic, prognostic, and therapeutic candidates for systemic candidiasis by proteomic and bioinformatic analyses. Mol Cell Proteomics 5: 79-96.
82. van der Poel, S., Wolthoorn, J., van den Heuvel, D., Egmond, M., Groux-Degroote, S., Neumann, S., etal. (2011) Hyperacidification of trans-Golgi network and endo/lysosomes in melanocytes by glucosylceramide-dependent V-ATPase activity. Traffic 12: 1634-1647.
83. Puccia, R., Schenkman, S., Gorin, P.A., and Travassos, L.R. (1986) Exocellular components of Paracoccidioides brasiliensis: identification of a specific antigen. Infect Immun 53: 199-206.
84. 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.
85. Rivera, J., Cordero, R.J., Nakouzi, A.S., Frases, S., Nicola, A., and Casadevall, A. (2010) Bacillus anthracis produces membrane-derived vesicles containing biologically active toxins. Proc Natl Acad Sci U S A 107: 19002-19007.
86. Rodrigues, M.L., Nimrichter, L., Oliveira, D.L., Frases, S., Miranda, K., Zaragoza, O., etal. (2007) Vesicular polysaccharide export in Cryptococcus neoformans is a eukaryotic solution to the problem of fungal trans-cell wall transport. Eukaryot Cell 6: 48-59.
87. Rodrigues, M.L., Nakayasu, E.S., Oliveira, D.L., Nimrichter, L., Nosanchuk, J.D., Almeida, I.C., and Casadevall, A. (2008) Extracellular vesicles produced by Cryptococcus neoformans contain protein components associated with virulence. Eukaryot Cell 7: 58-67.
88. Rodrigues, M.L., Franzen, A.J., Nimrichter, L., and Miranda, K. (2013) Vesicular mechanisms of traffic of fungal molecules to the extracellular space. Curr Opin Microbiol 16: 414-420.
89. Romani, L. (2000) Innate and adaptive immunity in Candida albicans infections and saprophytism. J Leukoc Biol 68: 175-179.
90. Roy, N., Barman, S., Ghosh, A., Pal, A., Chakraborty, K., Das, S.S., etal. (2010) Immunogenicity and protective efficacy of Vibrio cholerae outer membrane vesicles in rabbit model. FEMS Immunol Med Microbiol 60: 18-27.
91. Ruchel, R., Uhlemann, K., and Boning, B. (1983) Secretion of acid proteinases by different species of the genus Candida. Zentralbl Bakteriol Mikrobiol Hyg A 255: 537-548.
92. Sandini, S., Stringaro, A., Arancia, S., Colone, M., Mondello, F., Murtas, S., etal. (2011) The MP65 gene is required for cell wall integrity, adherence to epithelial cells and biofilm formation in Candida albicans. BMC Microbiol 11: 106.
93. Schnaar, R.L. (1994) Isolation of glycosphingolipids. Methods Enzymol 230: 348-370.
94. Silverman, J.M., Chan, S.K., Robinson, D.P., Dwyer, D.M., Nandan, D., Foster, L.J., and Reiner, N.E. (2008) Proteomic analysis of the secretome of Leishmania donovani. Genome Biol 9: R35.
95. Silverman, J.M., Clos, J., de Oliveira, C.C., Shirvani, O., Fang, Y., Wang, C., etal. (2010a) An exosome-based secretion pathway is responsible for protein export from Leishmania and communication with macrophages. J Cell Sci 123: 842-852.
96. Silverman, J.M., Clos, J., Horakova, E., Wang, A.Y., Wiesgigl, M., Kelly, I., etal. (2010b) Leishmania exosomes modulate innate and adaptive immune responses through effects on monocytes and dendritic cells. J Immunol 185: 5011-5022.
97. Sorgo, A.G., Heilmann, C.J., Dekker, H.L., Brul, S., de Koster, C.G., and Klis, F.M. (2010) Mass spectrometric analysis of the secretome of Candida albicans. Yeast 27: 661-672.
98. Sprong, H., Degroote, S., Claessens, T., van Drunen, J., Oorschot, V., Westerink, B.H., etal. (2001) Glycosphingolipids are required for sorting melanosomal proteins in the Golgi complex. J Cell Biol 155: 369-380.
99. Stanley, E.R., and Heard, P.M. (1977) Factors regulating macrophage production and growth. Purification and some properties of the colony stimulating factor from medium conditioned by mouse L cells. J Biol Chem 252: 4305-4312.
100. Thomas, D.P., Lopez-Ribot, J.L., and Lee, S.A. (2009) A proteomic analysis of secretory proteins of a pre-vacuolar mutant of Candida albicans. J Proteomics 73: 342-351.
101. Tian, T., Wang, Y., Wang, H., Zhu, Z., and Xiao, Z. (2010) Visualizing of the cellular uptake and intracellular trafficking of exosomes by live-cell microscopy. J Cell Biochem 111: 488-496.
102. Torosantucci, A., Gomez, M.J., Bromuro, C., Casalinuovo, I., and Cassone, A. (1991) Biochemical and antigenic characterization of mannoprotein constituents released from yeast and mycelial forms of Candida albicans. J Med Vet Mycol 29: 361-372.
103. Trocoli Torrecilhas, A.C., Tonelli, R.R., Pavanelli, W.R., da Silva, J.S., Schumacher, R.I., de Souza, W., etal. (2009) Trypanosoma cruzi: parasite shed vesicles increase heart parasitism and generate an intense inflammatory response. Microbes Infect 11: 29-39.
104. Vallejo, M.C., Matsuo, A.L., Ganiko, L., Medeiros, L.C., Miranda, K., Silva, L.S., etal. (2011) The pathogenic fungus Paracoccidioides brasiliensis exports extracellular vesicles containing highly immunogenic alpha-Galactosyl epitopes. Eukaryot Cell 10: 343-351.
105. Vallejo, M.C., Nakayasu, E.S., Longo, L.V., Ganiko, L., Lopes, F.G., Matsuo, A.L., etal. (2012a) Lipidomic analysis of extracellular vesicles from the pathogenic phase of Paracoccidioides brasiliensis. PLoS ONE 7: e39463.
106. Vallejo, M.C., Nakayasu, E.S., Matsuo, A.L., Sobreira, T.J., Longo, L.V., Ganiko, L., etal. (2012b) Vesicle and vesicle-free extracellular proteome of Paracoccidioides brasiliensis: comparative analysis with other pathogenic fungi. J Proteome Res 11: 1676-1685.
107. van de Veerdonk, F.L., Kullberg, B.J., and Netea, M.G. (2012) Adjunctive immunotherapy with recombinant cytokines for the treatment of disseminated candidiasis. Clin Microbiol Infect 18: 112-119.
108. Vyas, K.A., Patel, H.V., Vyas, A.A., and Schnaar, R.L. (2001) Segregation of gangliosides GM1 and GD3 on cell membranes, isolated membrane rafts, and defined supported lipid monolayers. Biol Chem 382: 241-250.
109. Youseff, B.H., Holbrook, E.D., Smolnycki, K.A., and Rappleye, C.A. (2012) Extracellular superoxide dismutase protects Histoplasma yeast cells from host-derived oxidative stress. PLoS Pathog 8: e1002713.