Immune sensing of Candida albicans requires cooperative recognition of mannans and glucans by lectin and Toll-like receptors

Journal of Clinical Investigation

Volumn 116, Issue 6, 2006, Pages 1642-1650

  Netea, Mihai G ^a   Gow, Neil A R ^b   Munro, Carol A ^b   Bates, Steven ^b   Collins, Claire ^b   Ferwerda, Gerben ^a   Hobson, Richard P ^b   Bertram, Gwyneth ^b   Hughes, H Bleddyn ^b   Jansen, Trees ^a   Jacobs, Liesbeth ^a   Buurman, Ed T ^b   Gijzen, Karlijn ^a   Williams, David L ^c   Torensma, Ruurd ^a   McKinnon, Alistair ^b   MacCallum, Donna M ^b   Odds, Frank C ^b   Van Der Meer, Jos W M ^a   Brown, Alistair J P ^b   Kullberg, Bart Jan ^a   more..

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b UNIVERSITY OF ABERDEEN   (United Kingdom)

^c East Tennessee State University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GLUCAN; DECTIN 1; GLUCAN; LECTIN; MANNAN; MANNOSE RECEPTOR; MEMBRANE PROTEIN; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANDIDA ALBICANS; CANDIDIASIS; CELL WALL; CONTROLLED STUDY; CYTOKINE PRODUCTION; HUMAN; HUMAN CELL; IN VIVO STUDY; MACROPHAGE; MONOCYTE; MONONUCLEAR CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; VIRULENCE;

ANIMALS; CANDIDA ALBICANS; CANDIDIASIS; CARBOHYDRATE CONFORMATION; CARBOHYDRATE SEQUENCE; CELL WALL; CYTOKINES; GLUCANS; HUMANS; LEUKOCYTES, MONONUCLEAR; MANNANS; MICE; MICE, INBRED C57BL; MOLECULAR SEQUENCE DATA; RECEPTORS, MITOGEN; TOLL-LIKE RECEPTORS;

EID: 33745207594     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI27114     Document Type: Article

References (51)

1. Pfaller, M.A., et al. 1999. International surveillance of blood stream infections due to Candida species in the European SENTRY Program: species distribution and antifungal susceptibility including the investigational triazole and echinocandin agents. Diagn. Microbiol. Infect. Dis. 35:19-25.
2. Edmond, M.B., et al. 1999. Nosocomial bloodstream infections in United States hospitals: a three-year analysis. Clin. Infect. Dis. 29:239-244.
3. Van 't Wout, J.W., Linde, I., Leijh, P.C.J., and Van Furth, R. 1988. Contribution of granulocytes and monocytes to resistance against experimental disseminated Candida albicans infections. Eur. J. Clin. Microbiol. Infect. Dis. 7:736-741.
4. Kullberg, B.J., Van 't Wout, J.W., and Van Furth, R. 1990. Role of granulocytes in enhanced host resistance to Candida albicans induced by recombinant interleukin-1. Infect. Immun. 58:3319-3324.
5. Marodi, L., Korchak, H.M., and Johnston, R.B., Jr. 1991. Mechanisms of host defense against Candida species. 1. Phagocytosis by monocytes and monocyte-derived macrophages. J. Immunol. 146:2783-2789.
6. Qian, Q., Jutila, M.A., Van Rooijen, N., and Cutler, J.E. 1994. Elimination of mouse splenic macrophages correlates with increased susceptibility to experimental disseminated candidiasis. J. Immunol. 152:5000-5008.
7. Djeu, J.Y. 1990. Role of tumor necrosis factor and colony-stimulating factors in phagocyte function against Candida albicans. Diagn. Microbiol. Infect. Dis. 13:383-386.
8. Kullberg, B.J., Van 't Wout, J.W., Hoogstraten, C., and Van Furth, R. 1993. Recombinant interferon-γ enhances resistance to acute disseminated Candida albicans infection in mice. J. Infect. Dis. 168:436-443.
9. Netea, M.G., et al. 1999. The increased susceptibility of TNFαLTα double knock-out mice to systemic candidiasis is due to defective recruitment and phagocytosis by neutrophils. J. Immunol. 163:1498-1505.
10. Kaposzta, R., Tree, P., Marodi, L., and Gordon, S. 1998. Characteristics of invasive candidiasis in gamma interferon- and interleukin-4-deficient mice: role of macrophages in host defense against Candida albicans. Infect. Immun. 66:1708-1717.
11. Tonnetti, L., et al. 1995. Interleukin-4 and -10 exacerbate candidiasis in mice. Eur. J. Immunol. 25:1559-1565.
12. Romani, L. 2004. Immunity to fungal infections. Nat. Rev. Immunol. 4:1-13.
13. Netea, M.G., Van der Graaf, C., Van der Meer, J.W.M., and Kullberg, B.J. 2004. Toll-like receptors and the host defense against microbial pathogens: bringing specificity to the innate-immune system. J. Leukoc. Biol. 75:749-755.
14. Netea, M.G., et al. 2002. The role of toll-like receptor (TLR) 2 and TLR4 in the host defense against disseminated candidiasis. J. Infect. Dis. 185:1483-1489.
15. Netea, M.G., et al. 2004. Toll-like receptor 2 inhibits cellular responses against Candida albicans through pathways mediated by IL-10 and CD4+CD25+ regulatory T cells. J. Immunol. 172:3712-3718.
16. Bellocchio, S., et al. 2004. The contribution of Toll-like/IL-1 receptor superfamily to innate and adaptive immunity to fungal pathogens in vivo. J. Immunol. 172:3059-3069.
17. Villamon, E., et al. 2004. Toll-like receptor-2 is essential in murine defenses against Candida albicans infections. Microbes Infect. 6:1-7.
18. Yamamoto, Y., Klein, T.W., and Friedman, H. 1997. Involvement of mannose receptor in cytokine interleukin-1beta (IL-1beta), IL-6, and granulocyte-macrophage colony-stimulating factor responses, but not in chemokine macrophage inflammatory protein 1beta (MIP-1beta), MIP-2, and KC responses, caused by attachment of Candida albicans to macrophages. Infect. Immun. 65:1077-1082.
19. Cambi, A., et al. 2003. The C-type lectin DC-SIGN (CD209) is an antigen-uptake receptor for Candida albicans on dendritic cells. Eur. J. Immunol. 33:532-538.
20. Klis, F.M., de Groot, P., and Hellingwerf, K. 2001. Molecular organization of the cell wall of Candida albicans. Med. Mycol. 39(Suppl. 1):1-8.
21. Vecchiarelli, A., Puliti, M., Torosantucci, A., Cassone, A., and Bistoni, F. 1991. In vitro production of tumor necrosis factor by murine splenic macrophages stimulated with mannoprotein constituents of Candida albicans cell wall. Cell Immunol. 134:65-76.
22. Tada, H., et al. 2002. Saccharomyces cerevisiae- and Candida albicans-derived mannan induced production of tumor necrosis factor alpha by human monocytes in a CD14- and Toll-like receptor 4-dependent manner. Microbiol. Immunol. 2002:503-512.
23. Jouault, T., et al. 2003. Candida albicans phospholipomannan is sensed through toll-like receptors. J. Infect. Dis. 188:165-172.
24. Gantner, B.N., Simmons, R.M., Canavera, S.J., Akira, S., and Underhill, D.M. 2003. Collaborative induction of inflammatory responses by dectin-1 and Toll-like receptor 2. J. Exp. Med. 197:1107-1117.
25. Brown, G.D., et al. 2003. Dectin-1 mediates the biological effects of beta-glucans. J. Exp. Med. 197:1119-1124.
26. Bates, S., et al. 2005. Candida albicans Pmr1p, a secretory pathway P-type Ca2+/Mn2+-ATPase, is required for glycosylation and virulence. J. Biol. Chem. 280:23408-23415.
27. Munro, C.A., et al. 2005. Mnt1p and Mnt2p of Candida albicans are partially redundant alpha-1,2-mannosyltransferases that participate in O-linked mannosylation and are required for adhesion and virulence. J. Biol. Chem. 280:1051-1060.
28. Hobson, R.P., et al. 2004. Loss of cell wall mannosylphosphate in Candida albicans does not influence macrophage recognition. J. Biol. Chem. 279:39628-39635.
29. Bates, S., et al. 2006. Outer chain N-glycans are required for cell wall integrity and virulence of Candida albicans. J. Biol. Chem. 281:90-98.
30. Singleton, D.R., Masuoka, J., and Hazen, K.C. 2005. Surface hydrophobicity changes of two Candida albicans serotype B mnn4 delta mutants. Eukaryotic Cell. 4:639-648.
31. Gantner, B.N., Simmons, R.M., and Underhill, D.M. 2005. Dectin-1 mediates macrophage recognition of Candida albicans yeasts but not filaments. EMBO J. 24:1277-1286.
32. Jouault, T., Bernigaud, A., Lepage, G., Trinel, P.A., and Poulain, D. 1994. The Candida albicans phospholipomannan induces in vitro production of tumour necrosis factor-alpha from human and murine macrophages. Immunology. 83:268-273.
33. Jouault, T., et al. 1995. β-1,2-linked oligomannosides from Candida albicans act as signals for tumor necrosis factor alpha production. Infect. Immun. 63:2378-2381.
34. Torosantucci, A., Chiani, P., and Cassone, A. 2000. Differential chemokine response of human monocytes to yeast and fungal forms of Candida albicans and its relation to the beta-1,6 glucan of the fungal cell wall. J. Leukoc. Biol. 68:923-932.
35. Poulain, D., and Jouault, T. 2004. Candida albicans cell wall glycans, host receptors and responses: elements for a decisive cross-talk. Curr. Opin. Microbiol. 7:342-349.
36. Gow, N.A., Brown, A.J., and Odds, F.C. 2002. Fungal morphogenesis and host invasion. Curr. Opin. Microbiol. 5:366-371.
37. Serbina, V., et al. 2003. Sequential MyD88-independent and -dependent activation of innate immune responses to intracellular bacterial infection. Immunity. 19:891-898.
38. Cutler, J.E. 2001. N-glycosylation of yeast, with emphasis on Candida albicans. Med. Mycol. 39S:75-86.
39. Newman, S.L., and Holly, A. 2001. Candida albicans is phagocytosed, killed, and processed for antigen presentation by human dendritic cells. Infect. Immun. 69:6813-6822.
40. Porcaro, I., Vidal, M., Jouvert, S., Stahl, P.D., and Giaimis, J. 2003. Mannose receptor contribution to Candida albicans phagocytosis by murine E-clone J774 macrophages. J. Leukoc. Biol. 74:206-215.
41. Underhill, D.M., and Ozinsky, A. 2002. Toll-like receptors: key mediators of microbe detection. Curr. Opin. Immunol. 14:103-110.
42. Brown, G.D., et al. 2002. Dectin-1 is a major beta-glucan receptor on macrophages. J. Exp. Med. 196:407-412.
43. Rogers, N.C., et al. 2005. Syk-dependent cytokine induction by Dectin-1 reveals a novel pattern recognition pathway for C type lectins. Immunity. 22:507-517.
44. Fonzi, W.A., and Irwin, M.Y. 1993. Isogenic strain construction and gene mapping in Candida albicans. Genetics. 134:717-728.
45. Brand, A., MacCallum, D.M., Brown, A.P.J., Gow, N.A.R., and Odds, F.C. 2004. Ectopic expression of URA3 can influence the virulence phenotypes and proteome of Candida albicans but can be overcome by targeted re-integration of URA3 at the RPS10 locus. Eukaryot. Cell. 3:900-909.
46. Kogan, G., Pavliak, V., and Masler, L. 1988. Structural studies of mannans from the cell walls of the pathogenic yeasts Candida albicans serotypes A and B and Candida parapsilosis. Carbohydr. Res. 172:243-253.
47. Mueller, A., et al. 2000. The influence of glucan polymer structure and solution conformation on binding to (1→3)-beta-D-glucan receptors in a human monocyte-like cell line. Glycobiology. 10:339-346.
48. Lowman, D.W., Ferguson, D.A., and Williams, D.L. 2003. Structural characterization of (1→3)-beta-D-glucans isolated from blastospore and hyphal forms of Candida albicans. Carbohydr. Res. 338:1491-1496.
49. Endres, S., Ghorbani, R., Lonnemann, G., Van der Meer, J.W.M., and Dinarello, C.A. 1988. Measurement of immunoreactive interleukin-1 beta from human mononuclear cells: optimization of recovery, intrasubject consistency, and comparison with interleukin-1 alpha and tumor necrosis factor. Clin. Immunol. Immunopathol. 49:424-438.
50. Drenth, J.P.H., et al. 1995. Endurance run increases circulating IL-6 and IL-1ra but downregulates ex vivo TNF-α and IL-1β production. J. Appl. Physiol. 79:1497-1503.
51. Netea, M.G., et al. 1996. Low-density-lipoprotein receptor deficient mice are protected against lethal endotoxinemia and severe Gram-negative infections. J. Clin. Invest. 97:1366-1372.