A Paracoccidioides brasiliensis glycan shares serologic and functional properties with cryptococcal glucuronoxylomannan

Fungal Genetics and Biology

Volumn 49, Issue 11, 2012, Pages 943-954

  Albuquerque, Priscila C ^a   Cordero, Radames J B ^b   Fonseca, Fernanda L ^a   Peres da Silva, Roberta ^c   Ramos, Caroline L ^a   Miranda, Kildare R ^a   Casadevall, Arturo ^b   Puccia, Rosana ^c   Nosanchuk, Joshua D ^b   Nimrichter, Leonardo ^a   Guimaraes, Allan J ^a   Rodrigues, Marcio L ^a,d  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^c FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^d INSTITUTO OSWALDO CRUZ   (Brazil)

Author keywords

Cryptococcus neoformans; Glucuronoxylomannan; Paracoccidioides brasiliensis; Polysaccharide

Indexed keywords

FUNGUS ANTIGEN; GALACTOSE; GLUCOSE; GLUCURONOXYLOMANNAN; GLYCAN; MANNOSE; MONOCLONAL ANTIBODY; POLYSACCHARIDE; RHAMNOSE; XYLOSE;

ANIMAL CELL; ANTIGEN BINDING; ARTICLE; CELL MEMBRANE; CELL WALL; CHEMICAL COMPOSITION; CONTROLLED STUDY; CRYPTOCOCCUS; CRYPTOCOCCUS NEOFORMANS; EXTRACELLULAR SPACE; FUNGAL METABOLISM; FUNGUS CAPSULE; FUNGUS MUTANT; GENETIC CODE; MACROPHAGE; MOLECULAR SIZE; MOUSE; MYCOSIS; NONHUMAN; PARACOCCIDIOIDES BRASILIENSIS; PARACOCCIDIOMYCOSIS; PATHOGENESIS; PHAGOCYTOSIS; PHYLOGENY; PRIORITY JOURNAL; PROTEIN DATABASE; SECRETORY VESICLE; SEQUENCE HOMOLOGY; SEROLOGY; SYNTHESIS;

ANIMALS; ANTIBODIES, MONOCLONAL; CELL LINE; CRYPTOCOCCOSIS; CRYPTOCOCCUS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FUNGAL PROTEINS; MICE; PARACOCCIDIOIDES; PARACOCCIDIOIDOMYCOSIS; PHAGOCYTOSIS; POLYSACCHARIDES;

FILOBASIDIELLA NEOFORMANS; FUNGI; MURINAE; PARACOCCIDIOIDES BRASILIENSIS;

EID: 84867907694     PISSN: 10871845     EISSN: 10960937     Source Type: Journal    
DOI: 10.1016/j.fgb.2012.09.002     Document Type: Article

References (89)

1. Araujo Gde S., et al. Capsules from pathogenic and non-pathogenic Cryptococcus spp. manifest significant differences in structure and ability to protect against phagocytic cells. PLoS One 2012, 7:e29561.
2. Barbosa F.M., et al. Glucuronoxylomannan-mediated interaction of Cryptococcus neoformans with human alveolar cells results in fungal internalization and host cell damage. Microbes Infect. 2006, 8:493-502.
3. Bertini S., et al. Expression of antibodies directed to Paracoccidioides brasiliensis glycosphingolipids during the course of paracoccidioidomycosis treatment. Clin. Vaccine Immunol. 2007, 14:150-156.
4. Carbonell L.M. Cell wall changes during the budding process of Paracoccidioides brasiliensis and Blastomyces dermatitidis. J. Bacteriol. 1967, 94:213-223.
5. Carbonell L.M., et al. Chemical morphology of glucan and chitin in the cell wall of the yeast phase of Paracoccidioides brasiliensis. J. Bacteriol. 1970, 101:636-642.
6. Casadevall A., Pirofski L.A. Polysaccharide-containing conjugate vaccines for fungal diseases. Trends Mol. Med. 2006, 12:6-9.
7. Casadevall A., et al. Monoclonal antibody based ELISAs for cryptococcal polysaccharide. J. Immunol. Methods 1992, 154:27-35.
8. Casadevall A., et al. Characterization of a murine monoclonal antibody to Cryptococcus neoformans polysaccharide that is a candidate for human therapeutic studies. Antimicrob. Agents Chemother. 1998, 42:1437-1446.
9. Chang Y.C., Kwon-Chung K.J. Isolation of the third capsule-associated gene, CAP60, required for virulence in Cryptococcus neoformans. Infect. Immun. 1998, 66:2230-2236.
10. Chang Y.C., Kwon-Chung K.J. Isolation, characterization, and localization of a capsule-associated gene, CAP10, of Cryptococcus neoformans. J. Bacteriol. 1999, 181:5636-5643.
11. Chang Y.C., et al. Further analysis of the CAP59 locus of Cryptococcus neoformans: structure defined by forced expression and description of a new ribosomal protein-encoding gene. Gene 1995, 167:179-183.
12. Chang Y.C., et al. The second capsule gene of Cryptococcus neoformans, CAP64, is essential for virulence. Infect. Immun. 1996, 64:1977-1983.
13. Chang Y.C., et al. Structure and biological activities of acapsular Cryptococcus neoformans 602 complemented with the CAP64 gene. Infect. Immun. 1997, 65:1584-1592.
14. Cleare W., Casadevall A. The different binding patterns of two immunoglobulin M monoclonal antibodies to Cryptococcus neoformans serotype A and D strains correlate with serotype classification and differences in functional assays. Clin. Diagn. Lab. Immunol. 1998, 5:125-129.
15. Cottrell T.R., et al. The pathogenic fungus Cryptococcus neoformans expresses two functional GDP-mannose transporters with distinct expression patterns and roles in capsule synthesis. Eukaryot. Cell 2007, 6:776-785.
16. De Jesus M., et al. Capsular localization of the Cryptococcus neoformans polysaccharide component galactoxylomannan. Eukaryot. Cell 2009, 8:96-103.
17. Dubois M., et al. A colorimetric method for the determination of sugars. Nature 1951, 168:167.
18. Eisenman H.C., et al. Vesicle-associated melanization in Cryptococcus neoformans. Microbiology 2009, 155:3860-3867.
19. Fava-Netto C. Estudos quantitativos sobre a fixação de complemento na blastomicose sul-americana, com antígeno polissacarídico. Arq. Cir. Clin. Exp. São Paulo 1955, 18:197-254.
20. Feldmesser M., Casadevall A. Mechanism of action of antibody to capsular polysaccharide in Cryptococcus neoformans infection. Front. Biosci. 1998, 3:d136-d151.
21. Fonseca F.L., et al. Structural and functional properties of the Trichosporon asahii glucuronoxylomannan. Fungal Genet. Biol. 2009, 46:496-505.
22. Fonseca F.L., et al. Role for chitin and chitooligomers in the capsular architecture of Cryptococcus neoformans. Eukaryot. Cell 2009, 8:1543-1553.
23. Fonseca F.L., et al. Immunomodulatory effects of serotype B glucuronoxylomannan from Cryptococcus gattii correlate with polysaccharide diameter. Infect. Immun. 2010, 78:3861-3870.
24. Frases S., et al. Capsule of Cryptococcus neoformans grows by enlargement of polysaccharide molecules. Proc. Natl. Acad. Sci. USA 2009, 106:1228-1233.
25. Fukazawa Y., et al. Cell wall polysaccharides of pathogenic yeasts. Curr. Top. Med. Mycol. 1995, 6:189-219.
26. Garcia-Rivera J., et al. Cryptococcus neoformans CAP59 (or Cap59p) is involved in the extracellular trafficking of capsular glucuronoxylomannan. Eukaryot. Cell 2004, 3:385-392.
27. Gomez B.L., et al. Detection of melanin-like pigments in the dimorphic fungal pathogen Paracoccidioides brasiliensis in vitro and during infection. Infect. Immun. 2001, 69:5760-5767.
28. Gonzalez A., et al. Paracoccidioides brasiliensis conidia recognize fibronectin and fibrinogen which subsequently participate in adherence to human type II alveolar cells: involvement of a specific adhesin. Microb. Pathog. 2008, 44:389-401.
29. Hogan L.H., Klein B.S. Altered expression of surface alpha-1,3-glucan in genetically related strains of Blastomyces dermatitidis that differ in virulence. Infect. Immun. 1994, 62:3543-3546.
30. Janbon G., et al. Cas1p is a membrane protein necessary for the O-acetylation of the Cryptococcus neoformans capsular polysaccharide. Mol. Microbiol. 2001, 42:453-467.
31. Kamerling J.P., et al. Characterization by gas-liquid chromatography-mass spectrometry and proton-magnetic-resonance spectroscopy of pertrimethylsilyl methyl glycosides obtained in the methanolysis of glycoproteins and glycopeptides. Biochem. J. 1975, 151:491-495.
32. Klimpel K.R., Goldman W.E. Cell walls from avirulent variants of Histoplasma capsulatum lack alpha-(1,3)-glucan. Infect. Immun. 1988, 56:2997-3000.
33. Klutts J.S., Doering T.L. Cryptococcal xylosyltransferase 1 (Cxt1p) from Cryptococcus neoformans plays a direct role in the synthesis of capsule polysaccharides. J. Biol. Chem. 2008, 283:14327-14334.
34. Kmetzsch L., et al. Role for Golgi reassembly and stacking protein (GRASP) in polysaccharide secretion and fungal virulence. Mol. Microbiol. 2011, 81:206-218.
35. Kozel T.R., Gotschlich E.C. The capsule of Cryptococcus neoformans passively inhibits phagocytosis of the yeast by macrophages. J. Immunol. 1982, 129:1675-1680.
36. Kozel T.R., et al. Antigenic and biological characteristics of mutant strains of Cryptococcus neoformans lacking capsular O acetylation or xylosyl side chains. Infect. Immun. 2003, 71:2868-2875.
37. Kumar P., et al. Emerging themes in cryptococcal capsule synthesis. Curr. Opin. Struct. Biol. 2011, 21:597-602.
38. Larsen R.A., et al. Phase I evaluation of the safety and pharmacokinetics of murine-derived anticryptococcal antibody 18B7 in subjects with treated cryptococcal meningitis. Antimicrob. Agents Chemother. 2005, 49:952-958.
39. Latge J.P. Galactofuranose containing molecules in Aspergillus fumigatus. Med. Mycol. 2009, 47(Suppl. 1):S104-S109.
40. Lopes L.C., et al. Glycoconjugates and polysaccharides from the Scedosporium/Pseudallescheria boydii complex: structural characterisation, involvement in cell differentiation, cell recognition and virulence. Mycoses 2011, 54(Suppl. 3):28-36.
41. Maxson M.E., et al. The volume and hydration of the Cryptococcus neoformans polysaccharide capsule. Fungal Genet. Biol. 2007, 44:180-186.
42. Maxson M.E., et al. Radial mass density, charge, and epitope distribution in the Cryptococcus neoformans capsule. Eukaryot. Cell 2007, 6:95-109.
43. Morejon K.M., et al. Paracoccidioidomycosis in patients infected with and not infected with human immunodeficiency virus: a case-control study. Am. J. Trop. Med. Hyg. 2009, 80:359-366.
44. Moyrand F., et al. Isolation and characterization of capsule structure mutant strains of Cryptococcus neoformans. Mol. Microbiol. 2002, 45:837-849.
45. Mukherjee J., et al. Protective murine monoclonal antibodies to Cryptococcus neoformans. Infect. Immun. 1992, 60:4534-4541.
46. Mukherjee J., et al. Protective and nonprotective monoclonal antibodies to Cryptococcus neoformans originating from one B cell. J. Exp. Med. 1995, 181:405-409.
47. Nimrichter L., et al. Self-aggregation of Cryptococcus neoformans capsular glucuronoxylomannan is dependent on divalent cations. Eukaryot. Cell 2007, 6:1400-1410.
48. Nogueira S.V., et al. Paracoccidioides brasiliensis enolase is a surface protein that binds plasminogen and mediates interaction of yeast forms with host cells. Infect. Immun. 2010, 78:4040-4050.
49. Oliveira D.L., et al. Cryptococcus neoformans cryoultramicrotomy and vesicle fractionation reveals an intimate association between membrane lipids and glucuronoxylomannan. Fungal Genet. Biol. 2009, 46:956-963.
50. Oliveira D.L., et al. Extracellular vesicles from Cryptococcus neoformans modulate macrophage functions. Infect. Immun. 2010, 78:1601-1609.
51. Oliveira D.L., et al. Characterization of yeast extracellular vesicles: evidence for the participation of different pathways of cellular traffic in vesicle biogenesis. PLoS One 2010, 5:e11113.
52. Panepinto J., et al. Sec6-dependent sorting of fungal extracellular exosomes and laccase of Cryptococcus neoformans. Mol. Microbiol. 2009, 71:1165-1176.
53. Pirofski L.A. Polysaccharides, mimotopes and vaccines for fungal and encapsulated pathogens. Trends Microbiol. 2001, 9:445-451.
54. Prado M., et al. Mortality due to systemic mycoses as a primary cause of death or in association with AIDS in Brazil: a review from 1996 to 2006. Mem. Inst. Oswaldo Cruz 2009, 104:513-521.
55. Puccia R., et al. Exocellular proteolytic activity of Paracoccidioides brasiliensis: cleavage of components associated with the basement membrane. Med. Mycol. 1998, 36:345-348.
56. Queiroz-Telles F., Escuissato D.L. Pulmonary paracoccidioidomycosis. Semin. Respir. Crit. Care Med. 2011, 32:764-774.
57. Ramos C.L., et al. Chitin-like molecules associate with Cryptococcus neoformans glucuronoxylomannan to form a glycan complex with previously unknown properties. Eukaryot. Cell 2012.
58. Rappleye C.A., et al. RNA interference in Histoplasma capsulatum demonstrates a role for alpha-(1,3)-glucan in virulence. Mol. Microbiol. 2004, 53:153-165.
59. Reese A.J., Doering T.L. Cell wall alpha-1,3-glucan is required to anchor the Cryptococcus neoformans capsule. Mol. Microbiol. 2003, 50:1401-1409.
60. Reese A.J., et al. Loss of cell wall alpha(1-3) glucan affects Cryptococcus neoformans from ultrastructure to virulence. Mol. Microbiol. 2007, 63:1385-1398.
61. Rodrigues M.L., et al. Human antibodies against a purified glucosylceramide from Cryptococcus neoformans inhibit cell budding and fungal growth. Infect. Immun. 2000, 68:7049-7060.
62. Rodrigues M.L., et al. Sialylglycoconjugates and sialyltransferase activity in the fungus Cryptococcus neoformans. Glycoconj. J. 2002, 19:165-173.
63. Rodrigues M.L., et al. Cleavage of human fibronectin and other basement membrane-associated proteins by a Cryptococcus neoformans serine proteinase. Microb. Pathog. 2003, 34:65-71.
64. Rodrigues M.L., et al. Vesicular polysaccharide export in Cryptococcus neoformans is a eukaryotic solution to the problem of fungal trans-cell wall transport. Eukaryot. Cell 2007, 6:48-59.
65. Rodrigues M.L., et al. Binding of the wheat germ lectin to Cryptococcus neoformans suggests an association of chitinlike structures with yeast budding and capsular glucuronoxylomannan. Eukaryot. Cell 2008, 7:602-609.
66. Rodrigues M.L., et al. Extracellular vesicles produced by Cryptococcus neoformans contain protein components associated with virulence. Eukaryot. Cell 2008, 7:58-67.
67. Rodrigues M.L., et al. Fungal polysaccharides: biological activity beyond the usual structural properties. Front. Microbiol. 2011, 2:171.
68. Rodrigues M.L., et al. Vesicular transport systems in fungi. Future Microbiol. 2011, 6:1371-1381.
69. San-Blas G., San-Blas F. Paracoccidioides brasiliensis: cell wall structure and virulence. A review. Mycopathologia 1977, 62:77-86.
70. San-Blas G., San-Blas F. Variability of cell wall composition in Paracoccidioides brasiliensis: a study of two strains. Sabouraudia 1982, 20:31-40.
71. San-Blas G., Vernet D. Induction of the synthesis of cell wall alpha-1,3-glucan in the yeastlike form of Paracoccidioides brasiliensis strain IVIC Pb9 by fetal calf serum. Infect. Immun. 1977, 15:897-902.
72. San-Blas G., et al. Fungal morphogenesis and virulence. Med. Mycol. 2000, 38(Suppl. 1):79-86.
73. Soares R.M., et al. Identification of sialic acids on the cell surface of hyphae and yeast forms of the human pathogen Paracoccidioides brasiliensis. FEMS Microbiol. Lett. 1993, 108:31-34.
74. Soares R.M., et al. Anionogenic groups and surface sialoglycoconjugate structures of yeast forms of the human pathogen Paracoccidioides brasiliensis. Microbiology 1998, 144(Pt. 2):309-314.
75. Sommer U., et al. An alpha-1,3-mannosyltransferase of Cryptococcus neoformans. J. Biol. Chem. 2003, 278:47724-47730.
76. Tavares P.M., et al. In vitro activity of the antifungal plant defensin RsAFP2 against Candida isolates and its in vivo efficacy in prophylactic murine models of candidiasis. Antimicrob. Agents Chemother. 2008, 52:4522-4525.
77. Taylor C.M., Roberts I.S. Capsular polysaccharides and their role in virulence. Contrib. Microbiol. 2005, 12:55-66.
78. Teles F.R., Martins M.L. Laboratorial diagnosis of paracoccidioidomycosis and new insights for the future of fungal diagnosis. Talanta 2011, 85:2254-2264.
79. Torosantucci A., et al. A novel glyco-conjugate vaccine against fungal pathogens. J. Exp. Med. 2005, 202:597-606.
80. Vaishnav V.V., et al. Structural characterization of the galactoxylomannan of Cryptococcus neoformans Cap67. Carbohydr. Res. 1998, 306:315-330.
81. Vallejo M.C., et al. The pathogenic fungus Paracoccidioides brasiliensis exports extracellular vesicles containing highly immunogenic alpha-Galactosyl epitopes. Eukaryot. Cell 2011, 10:343-351.
82. Vallejo M.C., et al. Lipidomic analysis of extracellular vesicles from the pathogenic phase of Paracoccidioides brasiliensis. PLoS One 2012, 7:e39463.
83. Vallejo M.C., et al. Vesicle and vesicle-free extracellular proteome of Paracoccidioides brasiliensis: comparative analysis with other pathogenic fungi. J. Proteome Res. 2012, 11:1676-1685.
84. Vliegenthart J.F., Kamerling J.P. Mass spectrometry of carbohydrates. Biochem. Soc. Trans. 1975, 3:460-462.
85. Wang Y., et al. Cryptococcus neoformans melanin and virulence: mechanism of action. Infect. Immun. 1995, 63:3131-3136.
86. Yoneda A., Doering T.L. A eukaryotic capsular polysaccharide is synthesized intracellularly and secreted via exocytosis. Mol. Biol. Cell 2006, 17:5131-5140.
87. Yoneda A., Doering T.L. An unusual organelle in Cryptococcus neoformans links luminal pH and capsule biosynthesis. Fungal Genet. Biol. 2009, 46:682-687.
88. Zancope-Oliveira R.M., et al. Immunochemical analysis of the H and M glycoproteins from Histoplasma capsulatum. Clin. Diagn. Lab. Immunol. 1994, 1:563-568.
89. Zaragoza O., et al. The capsule of the fungal pathogen Cryptococcus neoformans. Adv. Appl. Microbiol. 2009, 68:133-216.