Immunomodulatory effects of serotype B glucuronoxylomannan from Cryptococcus gattii correlate with polysaccharide diameter

Infection and Immunity

Volumn 78, Issue 9, 2010, Pages 3861-3870

  Fonseca, Fernanda L ^a   Nohara, Lilian L ^c   Cordero, Radames J B ^d   Frases, Susana ^b   Casadevall, Arturo ^d   Almeida, Igor C ^c   Nimrichter, Leonardo ^a   Rodrigues, Marcio L ^a  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^b INSTITUTO NACIONAL DE METROLOGIA   (Brazil)

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

^d ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCURONOXYLOMANNAN; HETERODIMER; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LUCIFERASE; MONOCLONAL ANTIBODY; MONOSACCHARIDE; NITRIC OXIDE; POLYSACCHARIDE; TOLL LIKE RECEPTOR 1; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 6; BACTERIAL POLYSACCHARIDE; TOLL LIKE RECEPTOR;

ANIMAL CELL; ANTIGEN RECOGNITION; ARTICLE; CELL STRAIN HEK293; CELLULAR IMMUNITY; CHEMICAL COMPOSITION; CONTROLLED STUDY; CRYPTOCOCCUS GATTII; CRYPTOCOCCUS NEOFORMANS; ELECTROPHORETIC MOBILITY; FUNGAL STRAIN; GENE CONSTRUCT; GENETIC TRANSFECTION; IMMUNOFLUORESCENCE TEST; IMMUNOMODULATION; LIGHT SCATTERING; MACROPHAGE; MOUSE; NONHUMAN; PHAGOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEROLOGY; ZETA POTENTIAL; ANIMAL; BIOSYNTHESIS; CELL LINE; CHEMISTRY; IMMUNOLOGY; METABOLISM; PHYSIOLOGY; SEROTYPING;

ANIMALS; CELL LINE; CRYPTOCOCCUS GATTII; MICE; NF-KAPPA B; NITRIC OXIDE; POLYSACCHARIDES; POLYSACCHARIDES, BACTERIAL; SEROTYPING; TOLL-LIKE RECEPTORS;

EID: 77956634319     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00111-10     Document Type: Article

References (54)

1. Bicanic, T., and T. S. Harrison. 2004. Cryptococcal meningitis. Br. Med. Bull. 72:99-118.
2. Biondo, C., A. Midiri, L. Messina, F. Tomasello, G. Garufi, M. R. Catania, M. Bombaci, C. Beninati, G. Teti, and G. Mancuso. 2005. MyD88 and TLR2, but not TLR4, are required for host defense against Cryptococcus neoformans. Eur. J. Immunol. 35:870-878.
3. Casadevall, A., W. Cleare, M. Feldmesser, A. Glatman-Freedman, D. L. Goldman, T. R. Kozel, N. Lendvai, J. Mukherjee, L. A. Pirofski, J. Rivera, A. L. Rosas, M. D. Scharff, P. Valadon, K. Westin, and Z. Zhong. 1998. Characterization of a murine monoclonal antibody to Cryptococcus neoformans polysaccharide that is a candidate for human therapeutic studies. Antimicrob. Agents Chemother. 42:1437-1446.
4. Casadevall, A., J. Mukherjee, and M. D. Scharff. 1992. Monoclonal antibody based ELISAs for cryptococcal polysaccharide. J. Immunol. Methods 154:27-35.
5. Chiapello, L. S., J. L. Baronetti, A. P. Garro, M. F. Spesso, and D. T. Masih. 2008. Cryptococcus neoformans glucuronoxylomannan induces macrophage apoptosis mediated by nitric oxide in a caspase-independent pathway. Int. Immunol. 20:1527-1541.
6. Collopy-Junior, I., F. F. Esteves, L. Nimrichter, M. L. Rodrigues, C. S. Alviano, and J. R. Meyer-Fernandes. 2006. An ectophosphatase activity in Cryptococcus neoformans. FEMS Yeast Res. 6:1010-1017.
7. Da Silva, C. A., D. Hartl, W. Liu, C. G. Lee, and J. A. Elias. 2008. TLR-2 and IL-17A in chitin-induced macrophage activation and acute inflammation. J. Immunol. 181:4279-4286.
8. De Jesus, M., S. K. Chow, R. J. Cordero, S. Frases, and A. Casadevall. 8 January 2010. Galactoxylomannans from Cryptococcus neoformans varieties neoformans and grubii are structurally and antigenically variable. Eukaryot. Cell. doi:10.1128/EC.00268-09.
9. Doering, T. L. 2000. How does Cryptococcus get its coat? Trends Microbiol. 8:547-553.
10. Fonseca, F. L., S. Frases, A. Casadevall, O. Fischman-Gompertz, L. Nimrichter, and M. L. Rodrigues. 2009. Structural and functional properties of the Trichosporon asahii glucuronoxylomannan. Fungal Genet. Biol. 46:496-505.
11. Frases, S., L. Nimrichter, N. B. Viana, A. Nakouzi, and A. Casadevall. 2008. Cryptococcus neoformans capsular polysaccharide and exopolysaccharide fractions manifest physical, chemical, and antigenic differences. Eukaryot. Cell 7:319-327.
12. Frases, S., B. Pontes, L. Nimrichter, N. B. Viana, M. L. Rodrigues, and A. Casadevall. 2009. Capsule of Cryptococcus neoformans grows by enlargement of polysaccharide molecules. Proc. Natl. Acad. Sci. U. S. A. 106:1228-1233.
13. García-Rivera, J., Y. C. Chang, K. J. Kwon-Chung, and A. Casadevall. 2004. Cryptococcus neoformans CAP59 (or Cap59p) is involved in the extracellular trafficking of capsular glucuronoxylomannan. Eukaryot. Cell 3:385-392.
14. Gautam, J. K., Ashish, L. D. Comeau, J. K. Krueger, and M. F. Smith, Jr. 2006. Structural and functional evidence for the role of the TLR2 DD loop in TLR1/TLR2 heterodimerization and signaling. J. Biol. Chem. 281:30132-30142.
15. Green, L. C., D. A. Wagner, J. Glogowski, P. L. Skipper, J. S. Wishnok, and S. R. Tannenbaum. 1982. Analysis of nitrate, nitrite, and [15N]nitrate in biological fluids. Anal. Biochem. 126:131-138.
16. Hajjar, A. M., D. S. O'Mahony, A. Ozinsky, D. M. Underhill, A. Aderem, S. J. Klebanoff, and C. B. Wilson. 2001. Functional interactions between toll-like receptor (TLR) 2 and TLR1 or TLR6 in response to phenol-soluble modulin. J. Immunol. 166:15-19.
17. Jin, M. S., S. E. Kim, J. Y. Heo, M. E. Lee, H. M. Kim, S. G. Paik, H. Lee, and J. O. Lee. 2007. Crystal structure of the TLR1-TLR2 heterodimer induced by binding of a tri-acylated lipopeptide. Cell 130:1071-1082.
18. Jin, M. S., and J. O. Lee. 2008. Structures of the toll-like receptor family and its ligand complexes. Immunity 29:182-191.
19. Kidd, S. E., F. Hagen, R. L. Tscharke, M. Huynh, K. H. Bartlett, M. Fyfe, L. Macdougall, T. Boekhout, K. J. Kwon-Chung, and W. Meyer. 2004. A rare genotype of Cryptococcus gattii caused the cryptococcosis outbreak on Vancouver Island (British Columbia, Canada). Proc. Natl. Acad. Sci. U. S. A. 101:17258-17263.
20. Kozel, T. R., S. M. Levitz, F. Dromer, M. A. Gates, P. Thorkildson, and G. Janbon. 2003. Antigenic and biological characteristics of mutant strains of Cryptococcus neoformans lacking capsular O acetylation or xylosyl side chains. Infect. Immun. 71:2868-2875.
21. Krishnegowda, G., A. M. Hajjar, J. Zhu, E. J. Douglass, S. Uematsu, S. Akira, A. S. Woods, and D. C. Gowda. 2005. Induction of proinflammatory responses in macrophages by the glycosylphosphatidylinositols of Plasmodium falciparum: cell signaling receptors, glycosylphosphatidylinositol (GPI) structural requirement, and regulation of GPI activity. J. Biol. Chem. 280: 8606-8616.
22. Kumar, H., T. Kawai, and S. Akira. 2009. Toll-like receptors and innate immunity. Biochem. Biophys. Res. Commun. 388:621-625.
23. Kwon-Chung, K. J., and A. Varma. 2006. Do major species concepts support one, two or more species within Cryptococcus neoformans? FEMS Yeast Res. 6:574-587.
24. Larsen, R. A., P. G. Pappas, J. Perfect, J. A. Aberg, A. Casadevall, G. A. Cloud, R. James, S. Filler, and W. E. Dismukes. 2005. Phase I evaluation of the safety and pharmacokinetics of murine-derived anticryptococcal antibody 18B7 in subjects with treated cryptococcal meningitis. Antimicrob. Agents Chemother. 49:952-958.
25. Lee, C. G. 2009. Chitin, chitinases and chitinase-like proteins in allergic inflammation and tissue remodeling. Yonsei Med. J. 50:22-30.
26. Lee, C. G., C. A. Da Silva, J. Y. Lee, D. Hartl, and J. A. Elias. 2008. Chitin regulation of immune responses: an old molecule with new roles. Curr. Opin. Immunol. 20:684-689.
27. Levitz, S. M. 2002. Receptor-mediated recognition of Cryptococcus neoformans. Nippon Ishinkin Gakkai Zasshi 43:133-136.
28. Levitz, S. M. 2004. Interactions of Toll-like receptors with fungi. Microbes Infect. 6:1351-1355.
29. Liang, S., K. B. Hosur, S. Lu, H. F. Nawar, B. R. Weber, R. I. Tapping, T. D. Connell, and G. Hajishengallis. 2009. Mapping of a microbial protein domain involved in binding and activation of the TLR2/TLR1 heterodimer. J. Immunol. 182:2978-2985.
30. McClelland, E. E., P. Bernhardt, and A. Casadevall. 2005. Coping with multiple virulence factors: which is most important? PLoS Pathog. 1:e40.
31. McFadden, D., O. Zaragoza, and A. Casadevall. 2006. The capsular dynamics of Cryptococcus neoformans. Trends Microbiol. 14:497-505.
32. Merkle, R. K., and I. Poppe. 1994. Carbohydrate composition analysis of glycoconjugates by gas-liquid chromatography/mass spectrometry. Methods Enzymol. 230:1-15.
33. Mitchell, D. H., T. C. Sorrell, A. M. Allworth, C. H. Heath, A. R. McGregor, K. Papanaoum, M. J. Richards, and T. Gottlieb. 1995. Cryptococcal disease of the CNS in immunocompetent hosts: influence of cryptococcal variety on clinical manifestations and outcome. Clin. Infect. Dis. 20:611-616.
34. Monari, C., F. Bistoni, A. Casadevall, E. Pericolini, D. Pietrella, T. R. Kozel, and A. Vecchiarelli. 2005. Glucuronoxylomannan, a microbial compound, regulates expression of costimulatory molecules and production of cytokines in macrophages. J. Infect. Dis. 191:127-137.
35. Monari, C., F. Bistoni, and A. Vecchiarelli. 2006. Glucuronoxylomannan exhibits potent immunosuppressive properties. FEMS Yeast Res. 6:537-542.
36. Monari, C., E. Pericolini, G. Bistoni, A. Casadevall, T. R. Kozel, and A. Vecchiarelli. 2005. Cryptococcus neoformans capsular glucuronoxylomannan induces expression of Fas ligand in macrophages. J. Immunol. 174:3461-3468.
37. Mukherjee, J., G. Nussbaum, M. D. Scharff, and A. Casadevall. 1995. Protective and nonprotective monoclonal antibodies to Cryptococcus neoformans originating from one B cell. J. Exp. Med. 181:405-409.
38. Mukherjee, J., M. D. Scharff, and A. Casadevall. 1992. Protective murine monoclonal antibodies to Cryptococcus neoformans. Infect. Immun. 60:4534-4541.
39. Nakamura, K., K. Miyagi, Y. Koguchi, Y. Kinjo, K. Uezu, T. Kinjo, M. Akamine, J. Fujita, I. Kawamura, M. Mitsuyama, Y. Adachi, N. Ohno, K. Takeda, S. Akira, A. Miyazato, M. Kaku, and K. Kawakami. 2006. Limited contribution of Toll-like receptor 2 and 4 to the host response to a fungal infectious pathogen, Cryptococcus neoformans. FEMS Immunol. Med. Microbiol. 47:148-154.
40. Nimrichter, L., S. Frases, L. P. Cinelli, N. B. Viana, A. Nakouzi, L. R. Travassos, A. Casadevall, and M. L. Rodrigues. 2007. Self-aggregation of Cryptococcus neoformans capsular glucuronoxylomannan is dependent on divalent cations. Eukaryot. Cell 6:1400-1410.
41. Nosanchuk, J. D., and A. Casadevall. 1997. Cellular charge of Cryptococcus neoformans: contributions from the capsular polysaccharide, melanin, and monoclonal antibody binding. Infect. Immun. 65:1836-1841.
42. Nussbaum, G., W. Cleare, A. Casadevall, M. D. Scharff, and P. Valadon. 1997. Epitope location in the Cryptococcus neoformans capsule is a determinant of antibody efficacy. J. Exp. Med. 185:685-694.
43. Perfect, J. R., and A. Casadevall. 2002. Cryptococcosis. Infect. Dis. Clin. North Am. 16:837-874.
44. Roeder, A., C. J. Kirschning, R. A. Rupec, M. Schaller, and H. C. Korting. 2004. Toll-like receptors and innate antifungal responses. Trends Microbiol. 12:44-49.
45. Schindler, U., and V. R. Baichwal. 1994. Three NF-κB binding sites in the human E-selectin gene required for maximal tumor necrosis factor alphainduced expression. Mol. Cell. Biol. 14:5820-5831.
46. Shoham, S., C. Huang, J. M. Chen, D. T. Golenbock, and S. M. Levitz. 2001. Toll-like receptor 4 mediates intracellular signaling without TNF-α release in response to Cryptococcus neoformans polysaccharide capsule. J. Immunol. 166:4620-4626.
47. Sorgi, C. A., A. Secatto, C. Fontanari, W. M. Turato, C. Belanger, A. I. de Medeiros, S. Kashima, S. Marleau, D. T. Covas, P. T. Bozza, and L. H. Faccioli. 2009. Histoplasma capsulatum cell wall β-glucan induces lipid body formation through CD18, TLR2, and dectin-1 receptors: correlation with leukotriene B4 generation and role in HIV-1 infection. J. Immunol. 182:4025-4035.
48. Speed, B., and D. Dunt. 1995. Clinical and host differences between infections with the two varieties of Cryptococcus neoformans. Clin. Infect. Dis. 21:28-34.
49. Sweetser, M. T., T. Hoey, Y. L. Sun, W. M. Weaver, G. A. Price, and C. B. Wilson. 1998. The roles of nuclear factor of activated T cells and ying-yang 1 in activation-induced expression of the interferon-gamma promoter in T cells. J. Biol. Chem. 273:34775-34783.
50. Triantafilou, M., F. G. Gamper, R. M. Haston, M. A. Mouratis, S. Morath, T. Hartung, and K. Triantafilou. 2006. Membrane sorting of toll-like receptor (TLR)-2/6 and TLR2/1 heterodimers at the cell surface determines heterotypic associations with CD36 and intracellular targeting. J. Biol. Chem. 281:31002-31011.
51. Vecchiarelli, A. 2007. Fungal capsular polysaccharide and T-cell suppression: the hidden nature of poor immunogenicity. Crit. Rev. Immunol. 27:547-557.
52. Yauch, L. E., M. K. Mansour, and S. M. Levitz. 2005. Receptor-mediated clearance of Cryptococcus neoformans capsular polysaccharide in vivo. Infect. Immun. 73:8429-8432.
53. Yauch, L. E., M. K. Mansour, S. Shoham, J. B. Rottman, and S. M. Levitz. 2004. Involvement of CD14, toll-like receptors 2 and 4, and MyD88 in the host response to the fungal pathogen Cryptococcus neoformans in vivo. Infect. Immun. 72:5373-5382.
54. Zaragoza, O., M. L. Rodrigues, M. De Jesus, S. Frases, E. Dadachova, and A. Casadevall. 2009. The capsule of the fungal pathogen Cryptococcus neoformans. Adv. Appl. Microbiol. 68:133-216.