Fungal surface and innate immune recognition of filamentous fungi

Frontiers in Microbiology

Volumn 2, Issue DEC, 2011, Pages

  Figueiredo, Rodrigo T ^a   Carneiro, Leticia A M ^a   Bozza, Marcelo T ^a  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

Author keywords

Cytokines; Fungi; Inflammation; Innate immunity; Macrophages; PRRs; Signaling

Indexed keywords

FUNGI;

EID: 84862318340     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2011.00248     Document Type: Review

References (146)

1. Aimanianda, V., Bayry, J., Bozza, S., Kniemeyer, O., Perruccio, K., Elluru, S. R., Clavaud, C., Paris, S., Brakhage, A. A., Kaveri, S. V., Romani, L., and Latgé, J. P. (2009). Surface hydrophobin prevents immune recognition of airborne fungal spores. Nature 460, 1117-1121.
2. Akira, S., Uematsu, S., and Takeuchi, O. (2006). Pathogen recognition and innate immunity. Cell 124, 783-801.
3. Alexopoulou, L., Holt, A. C., Medzhitov, R., and Flavell, R. A. (2001). Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature 413, 732-738.
4. Ariizumi, K., Shen, G. L., Shikano, S., Ritter, R. III, Zukas, P., Edelbaum, D., Morita, A., and Takashima, A. (2000). Cloning of a second dendritic cell-associated C-type lectin (dectin-2) and its alternatively spliced isoforms. J. Biol. Chem. 275, 11957-11963.
5. Azad, A. K., Torrelles, J. B., and Schlesinger, L. S. (2008). Mutation in the DC-SIGN cytoplasmic triacidic cluster motif markedly attenuates receptor activity for phagocytosis and endocytosis of mannose-containing ligands by human myeloid cells. J. Leukoc. Biol. 84,1594-1603.
6. Barbosa, E M., Fonseca, E L., Figueiredo, R. T., Bozza, M. T., Casadevall, A., Nimrichter, L., and Rodrigues, M. L. (2007). Binding of glucuronoxylomannan to the CD 14 receptor in human A549 alveolar cells induces interleukin-8 production. Clin. Vaccine Immunol. 14, 94-98.
7. Bellocchio, S., Montagnoli, C., Bozza, S., Gaziano, R., Rossi, G., Mambula, S. S., Vecchi, A., Mantovani, A., Levitz, S. M., and Romani, L. (2004). The contribution of the Toll-like/IL-1 receptor superfamily to innate and adaptive immunity to fungal pathogens in vivo. J. Immunol. 172, 3059-3069.
8. Bi, L., Gojestani, S., Wu, W., Hsu, Y. M., Zhu, J., Ariizumi, K., and Lin, X. (2010). CARD9 mediates dectin-2-induced IkappaBalpha kinase ubiquitination leading to activation of NF-kappaB in response to stimulation by the hyphal form of Candida albicans. J. Biol. Chem. 285, 25969-25977.
9. Bittencourt, V. C., Figueiredo, R. T., da Silva, R. B., Mourão-Sá, D. S., Fernandez, P. L., Sassaki, G. L., Mul-loy, B., Bozza, M. T., and Barreto-Bergter, E. (2006). An alpha-glucan of Pseudallescheria boydii is involved in fungal phagocytosis and Toll-like receptor activation. J. Biol. Chem. 281,22614-22623.
10. Bochud, P. Y., Chien, J. W., Marr, K. A., Leisenring, W. M., Upton, A., Janer, M., Rodrigues, S. D., Li, S., Hansen, J. A., Zhao, L. P., Aderem, A., and Boeckh, M. (2008). Toll-like receptor 4 polymorphisms and aspergillosis in stem-cell transplantation. N. Engl. J. Med. 359, 1766-1777.
11. Bretz, C., Gersuk, G., Knoblaugh, S., Chaudhary, N., Randolph-Habecker, J., Hackman, R. C., Staab, J., and Marr, K. A. (2008). MyD88 signaling contributes to early pulmonary responses to Aspergillus fumigatus. Infect. Immun. 76, 952-958.
12. Brown, G. D., and Gordon, S. (2001). A new receptor for β-glucans. Nature 413,36-37.
13. Brown, G. D., Herre, J., Williams, D. L., Willment, J. A., Marshall, A. S., Gordon, S. (2003). Dectin-1 mediates the biological effects of beta-glucans. J. Exp. Med. 197, 1119-1124.
14. Brown, G. D., Taylor, P. R., Reid, D. M., Willment, J. A., Williams, D. L., Martinez-Pomares, L., Wong, S. Y., Gordon, S. (2002) Dectin-1 is a major beta-glucan receptor on macrophages. J. Exp. Med. 196, 407-412.
15. Brunn, G. J., Bungum, M. K., Johnson, G. B., and Platt, J. L. (2005). Conditional signaling by Toll-like receptor 4. FASEBJ. 19,872-874.
16. Bugarcic, A., Hitchens, K., Beckhouse, A. G., Wells, C. A., Ashman, R. B., and Blanchard, H. (2008). Human and mouse macrophage-inducible C-type lectin (mincle) bind Candida albicans. Glycobiology 18,679-685.
17. Cambi, A., Gijzen, K., de Vries, J. M., Torensma, R., Joosten, B., Adema, G. J., Netea, M. G., Kullberg, B. J., Romani, L., and Figdor, C. G. (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.
18. Cambi, A., Netea, M. G., Mora-Montes, H. M., Gow, N. A., Hato, S. V., Lowman, D. W., Kullberg, B. J., Torensma, R., Williams, D. L., and Figdor, C. G. (2008). Dendritic cell interaction with Candida albicans critically depends on N-linked mannan. J. Biol. Chem. 283, 20590-20599.
19. Camilos, G., Luna, M., Lewism, R. E., Bodey, G. P., Chemaly, R., Tarrand, J. J., Safdar, A., Raad, I. I., and Kontoyiannis, D. P. (2006). Invasive fungal infections in patients with hematologic malignancies in a tertiary care cancer center: an autopsy study over a 15-year period (1989-2003). Haematologica 91, 986-989.
20. Campos, M. A., Almeida, I. C., Takeuchi, O., Akira, S., Valente, E. P., Procó-pio, D. O., Travassos, L. R., Smith, J. A., Golenbock, D. T., and Gazzinelli, R. T. (2001). Activation of Toll-like receptor-2byglycosylphosphatidyli-nositol anchors from a protozoan parasite.J. Immunol. 167,416-423.
21. Carneiro, L. A., Magalhaes, J. G., Tattoli, I., Philpott, D. J., and Travassos, L. H. (2008). Nod-like proteins in inflammation and disease. J. Pathol. 214, 136-148.
22. Chaffin, W L., López-Ribot, J. L., Casanova, M., Gozalbo, D., and Martínez, J. P. (1998). Cell wall and secreted proteins of Candida albicans: identification, function, and expression. Microbiol. Mol. Biol. Rev. 62,130-180.
23. Costachel, C., Coddeville, B., Latgé, J. P., and Fontaine, T. (2005). Glycosylphosphatidylinositol-anchored fungal polysaccharide in Aspergillus fumigatus. J. Biol. Chem. 280,39835-39842.
24. Dan, J. M., Kelly, R. M., Lee, C. K., and Levitz, S. M. (2008). Role of the mannose receptor in a murine model of Cryptococcus neoformans infection. Infec. Immun. 76, 2362-2367.
25. Davis, B. K., Wen, H., and Ting, J. P. (2011). The inflammasome NLRs in immunity, inflammation, and associated diseases. Annu. Rev. Immunol. 29, 707-735.
26. Debierre-Grockiego, F., Campos, M. A., Azzouz, N., Schmidt, J., Bieker, U., Resende, M. G., Mansur, D. S., Wein-gart, R., Schmidt, R. R., Golenbock, D. T., Gazzinelli, R. T., and Schwarz, R. T. J. (2007). Activation of TLR2 and TLR4 by glycosylphosphatidylinositols derived from Toxoplasma gondii.J. Immunol. 179, 1129-1137.
27. Delfino, D., Cianci, L., Lupis, E., Celeste, A., Petrelli, M. L., Curro, E, Cusumano, V., and Teti, G. (1997). Interleukin-6 production by human monocytes stimulated with Cryptococcus neoformans components. Infect. Immun. 65,2454-2456.
28. Di Carlo, F.J., and Fiore,J.V. (1958). On the composition of zymosan. Science 127, 756-757.
29. Diebold, S. S., Kaisho, T., Hemmi, H., Akira,S.,andReise Sousa, C. (2004). Innate antiviral responses by means of TLR7-mediated recognition of single-stranded RNA. Science 303, 1529-1531.
30. Dubourdeau, M., Athman, R., Balloy, V., Huerre, M., Chignard, M., Philpott, D. J., Latgé, J. P., and Ibrahim-Granet, O. (2006). Aspergillus fumigatus induces innate immune responses in alveolar macrophages through the MAPK pathway independently of TLR2 and TLR4. J. Immunol. 177,3994-4001.
31. Enoch, D. A., Ludlam, H. A., and Brown, N. M. (2006). Invasive fungal infections: a review of epidemiology and management options. J. Med. Microbiol. 55, 809-818.
32. Ezekowitz, R. A., Sastry, K., Bailly, P., Warner, A. (1990) Molecular characterization of the human macrophage mannose receptor: demonstration of multiple carbohydrate recognition-like domains and phagocytosis of yeasts in Cos-1 cells.J. Exp. Med. 172, 1785-1794.
33. Figueiredo, R. T., Fernandez, P. L., Dutra, F. F., González, Y., Lopes, L. C., Bittencourt, V. C., Sassaki, G. L., Barreto-Bergter, E., and Bozza, M. T. (2010). TLR4 recognizes Pseudallescheria boydii conidia and purified rhamnomannans. J. Biol. Chem. 285,40714-40723.
34. Figueiredo, R. T., Fernandez, P. L., Mourão-Sá, D. S., Porto, B. N., Dutra, F. F., Alves, L. S., Oliveira, M. F., Oliveira, P. L., Graça-Souza, A. V., and Bozza, M. T. (2007). Characterization of heme as activator of Toll-like receptor 4. J. Biol. Chem. 282,20221-20229.
35. Fonseca, F. L., Nohara, L. L., Cordero, R. J., Frases, S., Casadevall, A., Almeida, I. C., Nimrichter, L., and Rodrigues, M. L. (2010). Immunomodulatory effects of serotype B glucuronoxy-lomannan from Cryptococcus gattii correlate with polysaccharide diameter. Infect. Immun. 78, 3861-3870.
36. Fontaine, T., Magnin, T., Melhert, A., Lamont, D., Latgé, J. P., and Ferguson, M. A. (2003). Structures of the glycosylphosphatidylinositol membrane anchors from Aspergillus fumigatus membrane proteins. Gly-cobiology 13,169-177.
37. Fontaine, T., Simenel, C., Dubreucq, G., Adam, O., Delepierre, M., Lemoine, J., Vorgias, C. E., Diaquin, M., and Latgé, J. P. (2000). Molecular organization of the alkali-insoluble fraction of Aspergillus fumigatus cell wall. J. Biol. Chem. 275, 41528.
38. 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, 107-117.
39. Gantner, B. N., Simmons, R. M., and Underhill, D. M. (2005). Dectin-1 mediates macrophage recognition of Candida albicans yeast but not filaments. EMBO J. 24,1277-1286.
40. Gersuk, G. M., Underhill, D. M., Zhu, L., and Marr, K. A. (2006). Dectin-1 and TLRs permit macrophages to distinguish between different Aspergillus fumigatus cellular states. J. Immunol. 176, 3717-3724.
41. Goodridge, H. S., Reyes, C. N., Becker, C. A., Katsumoto, T. R., Ma, J., Wolf, A. J., Bose, N., Chan, A. S., Magee, A. S., Danielson, M. E., Weiss, A., Vasilakos, J. P., and Underhill, D. M. (2011). Activation of the innate immune receptor dectin-1 upon formation of a phagocytic synapse. Nature 472,471-475.
42. Goodridge, H. S., Simmons, R. M., and Underhill, D. M. (2007). Dectin-1 stimulation by Candida albicans yeast or zymosan triggers NFAT activation in macrophages and dendritic cells. J. Immunol. 178, 3107-3115.
43. Groll, A. H., and Walsh, T. J. (2001). Uncommon opportunistic fungi: newnosocomial threats. Clin. Microbiol. Infect. 7, 8-24.
44. Gross, O., Gewies, A., Finger, K., Schäfer, M., Sparwasser, T., Peschel, C, Forster, I., and Ruland, J. (2006). Card9 controls a non-TLR signalling pathway for innate anti-fungal immunity. Nature 442, 651-656.
45. Gross, O., Poeck, H., Bscheider, M., Dostert, C., Hannesschläger, N., Endres, S., Hartmann, G., Tardivel, A., Schweighoffer, E., Tybulewicz, V., Mocsai, A., Tschopp, J., and Ruland, J. (2009). Syk kinase signalling couples to the Nlrp3 inflammasome for anti-fungal host defence. Nature 459, 433-437.
46. Hara, H., Ishihara, C., Takeuchi, A., Imanishi, T., Xue, L., Morris, S. W., Inui, M., Takai, T., Shibuya, A., Saijo, S., Iwakura, Y., Ohno, N., Koseki, H., Yoshida, H., Penninger, J. M., and Saito, T. (2007). The adaptor protein CARD9 is essential for the activation of myeloid cells through ITAM-associated and Toll-like receptors. Nat. Immunol. 8, 619-629.
47. Hayashi, F., Smith, K. D., Ozinsky, A., Hawn, T. R., Yi, E. C., Goodlett, D R., Eng, J. K., Akira, S., Underhill, D. M., and Aderem, A. (2001). The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature 410, 1099-1103.
48. Heil, F., Hemmi, H., Hochrein, H., Ampenberger, F., Kirschning, C., Akira, S., Lipford, G., Wagner, H., and Bauer, S. (2004). Species-specific recognition of single-stranded RNA via Toll-like receptor 7 and 8. Science 303, 1526-1529.
49. Hemmi, H., Kaisho, T., Takeuchi, O., Sato, S., Sanjo, H., Hoshino, K., Horiuchi, T., Tomizawa, H., Takeda, K., and Akira, S. (2002). Small anti-viral compounds activate immune cells via the TLR7 MyD88-dependent signaling pathway. Nat. Immunol. 3, 196-200.
50. Hemmi, H., Takeuchi, O., Kawai, T., Kaisho, T., Sato, S., Sanjo, H., Matsumoto, M., Hoshino, K., Wagner, H., Takeda, K., and Akira, S. (2000). A Toll-like receptor recognizes bacterial DNA. Nature 408, 740-745.
51. Herre, J., Marshall, A. S., Caron, E., Edwards, A. D., Williams, D. L., Schweighoffer, E., Tybulewicz, V., Reis E Sousa, C., Gordon, S., and Brown, G. D. (2004). Dectin-1 uses novel mechanisms for yeast phagocytosis in macrophages. Blood 104, 4038-4045.
52. Hise, A. G., Tomalka, J., Ganesan, S., Patel, K., Hall, B. A., Brown, G. D., and Fitzgerald, K. A. (2009). An essential role for the NLRP3 inflammasome in host defense against the human fungal pathogen Candida albicans. Cell Host Microbe 5, 487-497.
53. Hohl, T. M., Van Epps, H. L., Rivera, A., Morgan, L. A., Chen, P. L., Feldmesser, M., and Pamer, E. G. (2005). Aspergillus fumigatus triggers inflammatory responses by stage-specific beta-glucan display. PLoS Pathog. 1, e30. doi:10.1371/journal.ppat.0010030
54. Hoshino, K., Takeuchi, O., Kawai, T., Sanjo, H., Ogawa, T., Takeda, Y., Takeda, K., and Akira, S. (1999). Cutting edge: Toll-like receptor 4 (TLR4)-deficient mice are hypore-sponsive to lipopolysaccharide: evidence for TLR4 as the Lps gene product. J. Immunol. 162, 3749-3752.
55. Hsu, T. L., Cheng, S. C., Yang, W. B., Chin, S. W., Chen, B. H., Huang, M. T., Hsieh, S. L., and Wong, C. H. (2009). Profiling carbohydrate-receptor interaction with recombinant innate immunity receptor-Fc fusion proteins. J. Biol. Chem. 284, 34479-34489.
56. Jin, M. S., Kim, S. E., Heo, J. Y., Lee, M. E., Kim, H. M., Paik, S. G., Lee, H., and Lee, J. O. (2007). Crystal structure of the TLR1-TLR2 heterodimer induced by binding of a tri-acylated lipopeptide. Cell 130,1071-1082.
57. Jouault, T., Ibata-Ombetta, S., Takeuchi, O., Trinel, P. A., Sacchetti, P., Lefebvre, P., Akira, S., and Poulain, D. (2003). Candida albicans phospholipomannan is sensed through Toll-like receptors. J. Infect. Dis. 188, 165-172.
58. Kang, J. Y., Nan, X., Jin, M. S., Youn, S. J., Ryu, Y H., Mah, S., Han, S. H., Lee, H., Paik, S. G., and Lee, J. O. (2009). Recognition of lipopeptide patterns by Toll-like receptor 2-Toll-like receptor 6 heterodimer. Immunity 31, 873-884.
59. Kankkunen, P., Teirilä, L., Rinta-haka, J., Alenius, H., Wolff, H., and Matikainen, S. (2010). (1,3)-beta-glucans activate both dectin-1 and NLRP3 inflammasome in human macrophages. J. Immunol. 184,6335-6342.
60. Kawai, T., and Akira, S. (2011). Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity 34, 637-650.
61. Kerrigan, A. M., and Brown, G. D. (2009). C-type lectins and phagocytosis. Immunobiology 214, 562-575.
62. Kerrigan, A. M., and Brown, G. D. (2010). Syk-coupled C-type lectin receptors that mediate cellular activation via single tyrosine based activation motifs. Immunol. Rev. 234, 335-352.
63. Kesh, S., Mensah, N. Y., Peterlongo, P., Jaffe, D., Hsu, K., Van Den Brink, M., O'reilly, R., Pamer, E., Satagopan, J., and Papanicolaou, G. A. (2005). TLR1 and TLR6 polymorphisms are associated with susceptibility to invasive aspergillosis after allogeneic stem cell transplantation. Ann. N Y. Acad. Sci. 1062, 95-103.
64. Krishnegowda, G., Hajjar, A. M., Zhu, J., Douglass, E. J., Uematsu, S., Akira, S., Woods, A. S., and Gowda, D. C. (2005). Induction of proinflammatory responses in macrophages by the glycosylphos-phatidylinositols of Plasmodium falciparum: cell signaling receptors, glycosylphosphatidylinositol (GPI) structural requirement, and regulation of GPI activity. J. Biol. Chem. 280,8606-8016.
65. Kruskal, B. A., Sastry, K., Warner, A. B., Mathieu, C. E., and Ezekowitz, R. A. (1992). Phagocytic chimeric receptors require both transmembrane and cytoplasmic domains from the mannose receptor. J. Exp. Med. 176, 1673-1680.
66. Kumar, H., Kumagai, Y., Tsuchida, T., Koenig, P. A., Satoh, T., Guo, Z., Jang, M. H., Saitoh, T., Akira, S., and Kawai, T. (2009). Involvement of the NLRP3 inflammasome in innate and humoral adaptive immune responses to fungal β-glucan. J. Immunol. 183, 8061-8067.
67. Latgé, J. (2001). The pathobiology of Aspergillus fumigatus. Trends Micro-biol. 9, 382-389.
68. Latgé, J. (2010). Tasting the fungal cell wall. Cell. Microbiol. 12, 863-872.
69. Lee, R. T., Hsu, T. L., Huang, S. K., Hsieh, S. L., Wong, C. H., and Lee, Y C. (2011). Survey of immune-related, mannose/fucose-binding C-type lectin receptors reveals widely divergent sugar-binding specificities. Glycobiology 21, 512-520.
70. Lee, S. J., Zheng, N. Y., Clavijo, M., and Nussenzweig, M. C. (2003). Normal host defense during systemic candidiasis in mannose receptor-deficient mice. Infect. Immun. 71, 437-445.
71. Leitão, E. A., Bittencourt, V .C., Haido, R. M., Valente, A. P., Peter-Katalinic, J., Letzel, M., de Souza, L. M., and Barreto-Bergter, E. (2003). Beta-galactofuranose-containing O-linked oligosaccha-rides present in the cell wall pep-tidogalactomannan of Aspergillus fumigatus contain immunodominant epitopes. Glycobiology 13, 681-692.
72. Lemaitre, B., Nicolas, E., Michaut, L., Reichhart, J. M., and Hoffmann, J. A. (1996). The dorsoventral regulatory gene cassette spät-zle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell 86, 973-983.
73. Lund, J. M., Alexopoulou, L., Sato, A., Karow, M., Adams, N. C., Gale, N. W., Iwasaki, A., and Flavell, R. A. (2004). Recognition of single-stranded RNA viruses by Toll-like receptor 7. Proc. Natl. Acad. Sci. U.S.A. 101, 5598-5603.
74. Luther, K., Torosantucci, A., Brakhage, A. A., Heesemann, J., and Ebel, F. (2007). Phagocytosis of Aspergillus fumigatus conidia by murine macrophages involves recognition by the dectin-1 beta-glucan receptor and Toll-like receptor 2. Cell. Microbiol. 9,368-381.
75. Mambula, S. S., Sau, K., Henneke, P., Golenbock, D. T., and Levitz, S. M. (2002). Toll-like receptor (TLR) signaling in response to Aspergillus fumigatus. J. Biol. Chem. 277, 39320-39326.
76. Marr, K. A., Carter, R. A., Crippa, F., Wald, A., and Corey, L. (2002). Epidemiology and outcome of mould infections in hematopoietic stem cell transplant recipients. Clin. Infect. Dis. 34,909-917.
77. Masuoka, J. (2004). Surface glycans of Candida albicans and other pathogenic fungi: physiological roles, clinical uses, and experimental changes. Clin. Microbiol. Rev. 17,281-310.
78. Matsumoto, M., Tanaka, T., Kaisho, T., Sanjo, H., Copeland, N. G., Gilbert, D. J., Jenkins, N. A., and Akira, S. (1999). A novel LPS-inducible C-type lectin is a transcriptional target of NF-IL6 in macrophages. J. Immunol. 163, 5039-5048.
79. McGreal, E. P., Rosas, M., Brown, G. D., Zamze, S., Wong, S. Y., Gordon, S., Martinez-Pomares, L., and Taylor, P. R. (2006). The carbohydrate-recognition domain of dectin-2 is a C-type lectin with specificity for high mannose. Glycobiology 16, 422-430.
80. Means, T. K., Lien, E., Yoshimura, A., Wang, S., Golenbock, D. T., and Fenton, M. J. (1999). The CD 14 ligands lipoarabinomannan and lipopolysaccharide differ in their requirement for Toll-like receptors. J. Immunol. 163, 6748-6755.
81. Medzhitov, R. (2007). Recognition of microorganisms and activation of the immune response. Nature 449, 819-826.
82. Meersseman, W., Lagrou, K., Maertens, J., Wilmer, A., Hermans, G., Van-derschueren, S., Spriet, I., Verbeken, E., and Van Wijngaerden, E. (2008) Galactomannan in bronchoalveolar lavage fluid: a tool for diagnosing aspergillosis in intensive care unit patients. Am. J. Respir. Crit. Care Med. 177,27-34.
83. Meier, A., Kirschning, C. J., Nikolaus, T., Wagner, H., Heesemann, J., and Ebel, F. (2003). Toll-like receptor (TLR) 2 and TLR4 are essential for Aspergillus-induced activation of murine macrophages. Cell. Microbiol. 5, 561-570.
84. Miyake, Y., Ishikawa, E., Ishikawa, T., and Yamasaki, S. (2010). Self and nonself recognition through C-type lectin receptor, mincle. Self Nonself 1,310-313.
85. Monari, C., Bistoni, F., Casadevall, A., Pericolini, E., Pietrella, D., Kozel, T. R., and Vecchiarelli, A. (2005). Glucuronoxylomannan, a micro-bial compound, regulates expression of costimulatory molecules and production of cytokines in macrophages. J. Infect. Dis. 191, 127-137.
86. Morgan, J., Wannemuehler, K. A., Marr, K. A., Hadley, S., Kontoyiannis, D. P., Walsh, T. J., Fridkin, S. K., Pappas, P. G., and Warnock, D. W (2005) Incidence of invasive aspergillosis following hematopoietic stem cell and solid organ transplantation: interim results of a prospective multicenter surveillance program. Med. Mycol. 43(Suppl. 1),S49-S58.
87. Murata, T., Sullivan, J. A., Sawyer, D. W., and Mandell, G. L. (1987). Influence of type and opsonization of ingested particle on intracellular free calcium distribution and superoxide production by human neutrophils. Infect. Immun. 55, 1784-1791.
88. Murray, C. K., Loo, F. L., Hospenthal, D. R., Cancio, L. C., Jones, J. A., Kim, S. H., Holcomb, J. B., Wade, C. E., and Wolf, S. E. (2008). Incidence of systemic fungal infection and related mortality following severe burns. Burns 34, 1108-1112.
89. Nathan, C. (2002). Points of control in inflammation. Nature 420, 846-852.
90. Netea, M. G., Gow, N. A., Munro, C. A., Bates, S., Collins, C., Ferwerda, G., Hobson, R. P., Bertram, G., Hughes, H. B., Jansen, T., Jacobs, L., Buur-man, E. T.,Gijzen, K., Williams, D. L., Torensma, R., McKinnon, A., Mac-Callum, D. M., Odds, F. C., Van der Meer, J. W., Brown, A. J., and Kull-berg, B. J. (2006). Immune sensing of Candida albicans requires cooperative recognition of mannans and glucans by lectin and Toll-like receptors.J. Clin. Invest. 116,1642-1650.
91. Netea, M. G., Van Der Graaf, C. A.,Vonk, A. G., Verschueren, I., Van Der Meer, J. W., and Kullberg, B. J. (2002). The role of Toll-like receptor (TLR) 2 and TLR4 in the host defense against disseminated candidiasis. J. Infect. Dis. 185,1483-1489.
92. Netea, M. G., Warris, A., Van der Meer, J. W., Fenton, M. J., Verver-Janssen, T. J., Jacobs, L. E., Andresen, T., Verweij, P. E., and Kullberg, B. J. (2003). Aspergillus fumigatus evades immune recognition during germination through loss of Toll-like receptor-4-mediated signal transduction. J. Infect. Dis. 188, 320-326.
93. Ozinsky, A., Underhill, D. M., Fontenot, J. D., Hajjar, A. M., Smith, K. D., Wilson, C. B., Schroeder, L., and Aderem, A. (2000). The repertoire for pattern recognition of pathogens by the innate immune system is defined by cooperation between Toll-like receptors. Proc. Natl. Acad. Sci. U.S.A. 97, 13766-13771.
94. Park, B. S., Song, D. H., Kim, H. M., Choi, B. S., Lee, H., and Lee, J. O. (2009). The structural basis of lipopolysaccharide recognition by the TLR4-MD-2 complex. Nature 458,1191-1195. Pasqualotto, A. C., and Denning, D. W (2006). Post-operative aspergillosis. Clin. Microbiol. Infect. 12, 1060-1076.
95. Pasqualotto A.C., Denning D.W. Post-operative aspergillosis. Clin. Microbiol. Infect. 2006. 12: 1060-1076.
96. Poltorak, A., He, X., Smirnova, I., Liu, M. Y., Van Huffel, C., Du, X., Birdwell, D., Alejos, E., Silva, M., Galanos, C., Freudenberg, M., Ricciardi-Castagnoli, P., Layton, B., and Beutler, B. (1998). Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 282, 2085-2088.
97. Qureshi, S. T., Larivière, L., Leveque, G., Clermont, S., Moore, K. J., Gros, P., and Malo, D. (1999) Endotoxin-tolerant mice have mutations in Toll-like receptor 4 (Tlr4). J. Exp. Med. 189,615-625.
98. Retini, C., Vecchiarelli, A., Monari, C., Tascini, C., Bistoni, F., and Kozel, T. R. (1996). Capsular polysaccharide of Cryptococcus neoformans induces proinflammatory cytokine release by human neutrophils. Infect. Immun. 64, 2897-2903.
99. Rodrigues, M. L., Nimrichter, L., Cordero, R. J., and Casadevall, A. (2011). Fungal polysaccha-rides: biological activity beyond the usual structural properties. Front. Microbiol. 2:171. doi:10.3389/fmicb.2011.00171
100. Rogers, N. C., Slack, E. C., Edwards, A. D., Nolte, M. A., Schulz, O., Schweighoffer, E., Williams, D. L., Gordon, S.,Tybulewicz,V.L., Brown, G. D., and Reis e Sousa, C. (2005). Syk-dependent cytokine induction by dectin-1 reveals a novel pattern recognition pathway for C type lectins. Immunity 22, 507-517.
101. Saïd-Sadler, N., Padilla, E., Langs-ley, G., and Ojcius, D. M. (2010). Aspergillus fumigatus stimulates the NLRP3 inflammasome through a pathway requiring ROS production and the Syk tyrosine kinase. PLoS ONE 5, e10008. doi:10.1371/jour-nal.pone.0010008
102. Saijo, S., Fujikado,N.,Furuta, T., Chung, S. H., Kotaki, H., Seki, K., Sudo, K., Akira, S., Adachi, Y., Ohno, N., Kinjo, T., Nakamura, K., Kawakami, K., and Iwakura, Y. (2007). Dectin-1 is required for host defense against Pneumocystis carinii but not against Candida albicans. Nat. Immunol. 8, 39-46.
103. Saijo, S., Ikeda, S., Yamabe, K., Kakuta, S., Ishigame, H.,Akitsu,A.,Fujikado, N., Kusaka, T., Kubo, S., Chung, S. H., Komatsu, R., Miura, N., Adachi, Y., Ohno, N., Shibuya, K., Yamamoto, N., Kawakami, K., Yamasaki, S., Saito, T., Akira, S., and Iwakura, Y (2010). Dectin-2 recognition of alpha-mannans and induction of Th17 cell differentiation is essential for host defense against Candida albicans. Immunity 32, 681-691.
104. Sandor, F., Latz, E., Re, F., Mandell, L., Repik, G., Golenbock, D. T., Espevik, T., Kurt-Jones, E. A., and Finberg, R. W. (2003). Importance of extra- and intracellular domains of TLR1 and TLR2 in NFkappa B signaling. J. Cell Biol. 162, 1099-1110.
105. Sato, K., Yang, X. L., Yudate, T., Chung, J. S., Wu, J., Luby-Phelps, K., Kim-berly, R. P., Underhill, D., Cruz, P. D. Jr., and Ariizumi, K. (2006). Dectin-2 is a pattern recognition receptor for fungi that couples with the Fc receptor gamma chain to induce innate immune responses. J. Biol. Chem. 281,38854-38866.
106. Schröder, N. W., Heine, H., Alexander, C., Manukyan, M., Eckert, J., Hamann, L., Göbel, U. B., and Schumann, R. R. (2004). Lipopolysaccharide binding protein binds to triacylated and diacylated lipopeptides and mediates innate immune responses. J. Immunol. 173, 2683-2691.
107. Schröder, N. W., Morath, S., Alexan der, C., Hamann, L., Hartung, T., Zähringer, U., Göbel, U. B., Weber, J. R., and Schumann, R. R. (2003) Lipoteichoic acid (LTA) of Streptococcus pneumoniae and Staphylococcus aureus activates immune cells via Toll-like receptor (TLR)-2, lipopolysaccharide-binding protein (LBP), and CD 14, whereas TLR-4 and MD-2 are not involved. J. Biol. Chem. 278, 15587-15594.
108. Schwandner, R., Dziarski, R., Wesche, H., Rothe, M., and Kirschning, C. J. (1999). Peptidoglycan, and lipoteichoic acid-induced cell activation is mediated by Toll-like receptor 2. J. Biol. Chem. 274, 17406-17409.
109. Segal, B. H., and Walsh, T. J. (2006). Current approaches to diagnosis and treatment of invasive aspergillosis. Am. J. Respir. Crit. Care Med. 173, 707-717.
110. Serrano-Gómez, D., Domínguez-Soto, A., Ancochea, J., Jimenez-Heffernan, J. A., Leal, J. A., and Corbí, A. L. (2004). Dendritic cell-specific intercellular adhesion molecule 3-grabbing nonintegrin mediates binding and internalization of Aspergillus fumigatus conidia by dendritic cells and macrophages. J. Immunol. 173, 5635-5643.
111. Shoham, S., Huang, C., Chen, J. M., Golenbock, D. T., and Levitz, S. M. (2001). Toll-like receptor 4 mediates intracellular signaling without TNF-alpha release in response to Cryptococcus neoformans polysaccharide capsule. J. Immunol. 166, 4620-4626.
112. Singh, N. (2001). Trends in the epidemiology of opportunistic fungal infections: predisposing factors and the impact of antimicrobial use practices. Clin. Infect. Dis. 33, 1692-1696.
113. Steele, C., Marrero, L., Swain, S., Harm-sen, A. G., Zheng, M., Brown, G. D., Gordon, S., Shellito, J. E., and Kolls, J. K. (2003). Alveolar macrophage-mediated killing of Pneumocystis carinii f. spp. muris involves molecular recognition by the dectin-1 beta-glucan receptor. J. Exp. Med. 198, 1677-1688.
114. Steele, C., Rapaka, R. R., Metz, A., Pop, S. M., Williams, D. L., Gordon, S., Kolls, J. K., and Brown, G. D. (2005). The beta-glucan receptor dectin-1 recognizes specific morphologies of Aspergillus fumigatus. PLoS Pathog. 1, e42. doi:10.1371/jour-nal.ppat.0010042
115. Swain, S. D., Lee, S. J., Nussen-zweig, M. C., and Harmsen, A. G. (2003). Absence of the macrophage mannose receptor in mice does not increase susceptibility to Pneumocystis carinii infection in vivo. Infect. Immun. 71, 6213-6221.
116. Syme, R. M., Spurrell, J. C., Amankwah, E. K., Green, F. H., and Mody, C. H. (2002). Primary dendritic cells phagocytose Cryptococcus neoformans via mannose receptors and Fcgamma receptor II for presentation to T lymphocytes. Infect. Immun. 70, 5972-5981.
117. Tachado, S. D., Zhang, J., Zhu, J., Patel, N., Cushion, M., and Koziel, H. (2007). Pneumocystis-mediated IL-8 release by macrophages requires coexpression of mannose receptors and TLR2. J. Leukoc. Biol. 81, 205-211.
118. Tada, H., Nemoto, E., Shimauchi, H., Watanabe, T., Mikami, T., Mat-sumoto, T., Ohno, N., Tamura, H., Shibata, K., Akashi, S., Miyake, K., Sugawara, S., Takada, H. (2002). Saccharomyces cerevisiae, and Candida albicans-derived mannan induced production of tumor necrosis factor alpha by human monocytes in a CD 14, and Toll-like receptor 4-dependent manner. Microbiol. Immunol. 46, 503-512.
119. Takeuchi, O., Kaufmann, A., Grote, K., Kawai, T., Hoshino, K., Morr, M., Mühlradt, P. F., and Akira, S. (2000). Cutting edge: preferentially the R-stereoisomer of the mycoplasmal lipopeptide macrophage-activating lipopeptide-2 activates immune cells through a Toll-like receptor 2- and MyD88-dependent signaling pathway. J. Immunol. 164, 554-557.
120. Takeuchi, O., Kawai, T., Mühlradt, P. E, Morr, M., Radolf, J. D., Zychlinsky A., Takeda, K., and Akira, S. (2001). Discrimination of bacterial lipoproteins by Toll-like receptor 6. Int. Immunol. 13,933-940.
121. Takeuchi, O., Sato, S., Horiuchi, T., Hoshino, K., Takeda, K., Dong, Z., Modlin, R. L., and Akira, S. (2002). Cutting edge: role of Toll-like receptor 1 in mediating immune response to microbial lipoproteins. J. Immunol. 169,10-14.
122. Tapping, R. I., and Tobias, P. S. (2003). Mycobacterial lipoarabinomannan mediates physical interactions between TLR1, and TLR2 to induce signaling. J. Endotoxin Res. 9, 264-268.
123. Taylor, P. R., Tsoni, S. V., Willment, J. A., Dennehy, K. M., Rosas, M., Findon, H., Haynes, K., Steele, C., Botto, M., Gordon, S., and Brown, G. D. (2007a). Dectin-1 is required for beta-glucan recognition and control of fungal infection. Nat. Immunol. 8, 31-38.
124. Taylor, K. R., Yamasaki, K., Radek, K. A., Di Nardo, A., Goodarzi, H., Golenbock, D., Beutler, B., and Gallo, R. L. (2007b). Recognition of hyaluronan released in sterile injury involves a unique receptor complex dependent on Toll-like receptor 4, CD44, and MD-2. J. Biol. Chem. 282, 18265-18275.
125. Travassos,L. H., Girardin,S.E.,Philpott, D. J., Blanot, D., Nahori, M. A., Werts, C., and Boneca, I. G. (2004). Toll-like receptor 2-dependent bacterial sensing does not occur via peptidoglycan recognition. EMBO Rep. 5, 1000-1006.
126. Trinel, P. A., Maes, E., Zanetta, J. P., Delplace, F., Coddeville, B., Jouault, T., Strecker, G., and Poulain, D. (2002). Candida albicans phospholipomannan, a new member of the fungal mannose inositol phospho-ceramide family. J. Biol. Chem. 277, 37260-37271.
127. Underhill, D. M., Ozinsky, A., Haj-jar, A. M., Stevens, A., Wilson, C. B., Bassetti, M., and Aderem, A (1999). The Toll-like recep tor 2 is recruited to macrophage phagosomes and discriminates between pathogens. Nature 401, 811-815.
128. Van de Veerdonk, E L., Joosten, L. A., Shaw, P. J., Smeekens, S. P., Malireddi, R. K., van der Meer, B. J., Netea, M. G., and Kanneganti, T. D. (2011). The inflammasome drives protective Th1 and Th17 cellular responses in disseminated candidiasis. Eur. J. Immunol. 41, 2260-2268.
129. Van de Veerdonk, E L., Kullberg, B. J., van der Meer, J. W., Gow, N. A., and Netea, M. G. (2008). Host-microbe interactions: innate pattern recognitionof fungal pathogens. Curr. Opin. Microbiol. 11,305-312.
130. Van der Graaf, C. A., Netea, M. G., Franke, B., Girardin, S. E., van der Meer, J. W., and Kullberg, B. J. (2006). Nucleotide oligomerization domain 2 (Nod2) is not involved in the pattern recognition of Candida albicans. Clin. Vaccine Immunol. 13, 423-425.
131. van Kooyk, Y., and Geijtenbeek, T. B (2003). DC-SIGN: escape mech anism for pathogens. Nat. Rev. Immunol. 3, 697-709.
132. Vecchiarelli, A., Retini, C., Monari, C., Tascini, C., Bistoni, F., and Kozel, T. R. (1996). Purified capsular polysaccharide of Cryptococcus neoformans induces interleukin-10 secretion by human monocytes. Infect. Immun. 64, 2846-2849.
133. Villamón, E., Gozalbo, D., Roig, P., O'Connor, J. E., Fradelizi, D., and Gil, M. L. (2004). Toll-like receptor-2 is essential in murine defenses against Candida albicans infections. Microbes Infect. 6, 1-7.
134. Wang, J. E., Warris, A., Ellingsen, E. A., Jørgensen, P. F., Flo, T. H., Espevik, T., Solberg, R., Verweij, P. E., and Aasen, A. O. (2001). Involvement of CD14, and Toll-like receptors in activation of human monocytes by Aspergillus fumigatushyphae. Infect. Immun. 69, 2402-2406.
135. Wells, C. A., Salvage-Jones, J. A., Li, X., Hitchens, K., Butcher, S., Murray, R. Z., Beckhouse, A. G., Lo, Y. L., Manzanero, S., Cobbold, C., Schroder, K., Ma, B., Orr, S., Stewart, L., Lebus, D., Sobieszczuk, P., Hume, D. A., Stow, J., Blanchard, H., and Ashman, R. B. (2008). The macrophage-inducible C-type lectin, mincle, is an essential component of the innate immune response to Candida albicans. J. Immunol. 180, 7404-7413.
136. Werner, J. L., Metz, A. E., Horn, D., Schoeb, T. R., Hewitt, M. M., Schwiebert, L. M., Faro-Trindade, I., Brown, G. D., and Steele, C. (2009). Requisite role for the dectin-1 beta-glucan receptor in pulmonary defense against Aspergillus fumigatus. J. Immunol. 182, 4938-4946.
137. West, X. Z., Malinin, N. L., Merkulova, A. A., Tischenko, M., Kerr, B. A., Bor-den, E. C., Podrez, E. A., Salomon, R. G., and Byzova, T. V (2010). Oxidative stress induces angiogen-esis by activating TLR2 with novel endogenous ligands. Nature 467, 972-976.
138. Willment, J.A.,and Brown,G.D. (2008). C-type lectin receptors in
139. Wright, S. D., Ramos, R. A., Tobias, P. S., Ulevitch, R. J., and Mathison, J. C. (1990). CD14, a receptor for complexes of lipopolysaccharide (LPS) and LPS binding protein. Science 249, 1431-1433.
140. Xin, H., Dziadek, S., Bundle, D. R., and Cutler, J. E. (2008). Synthetic glycopeptide vaccines combining beta-mannan and peptide epitopes induce protection against candidiasis. Proc. Natl. Acad. Sci. U.S.A. 105, 13526-13531.
141. Yamasaki, S., Ishikawa, E., Sakuma, M., Hara, H., Ogata, K., and Saito, T. (2008). Mincle is an ITAM-coupled activating receptor that senses damaged cells. Nat. Immunol. 9, 1179-1188.
142. Yamasaki, S., Matsumoto, M., Takeuchi, O., Matsuzawa, T., Ishikawa, E., Sakuma, M., Tateno, H., Uno, J., Hirabayashi, J., Mikami, Y., Takeda, K., Akira, S., and Saito, T. (2009). C-type lectin mincle is an activating receptor for pathogenic fungus, Malassezia. Proc. Natl. Acad. Sci. U.S.A. 106,1897-1902.
143. Yang, H., Hreggvidsdottir, H. S., Palm-blad, K., Wang, H., Ochani, M., Li, J., Lu, B., Chavan, S., Rosas-Ballina, M., Al-Abed, Y., Akira, S., Bierhaus, A., Erlandsson-Harris, H., Andersson, U., and Tracey, K. J. (2010). A critical cysteine is required for HMGB1 binding to Toll-like receptor 4 and activation of macrophage cytokine release. Proc. Natl. Acad. Sci. U.S.A. 107, 11942-11947.
144. Yoshitomi, H., Sakaguchi, N., Kobayashi, K., Brown, G. D., Tagami, T., Sakihama, T., Hirota, K., Tanaka, S., Nomura, T., Miki, I., Gordon, S., Akira, S., Nakamura, T., and Sakaguchi, S. (2005) A role for fungal {beta}-glucans and their receptor dectin-1 in the induction of autoimmune arthritis in genetically susceptible mice. J. Exp. Med. 201, 949-960.
145. Zhang, H. J., Qu, J. M., Shao, C. Z., Zhang, J., He, L. X., and Yuan, Z. H. (2008). Aspergillus fumiga-tus conidia upregulates NOD2 protein expression both in vitro and in vivo. Acta Pharmacol. Sin. 29, 1202-1208.
146. Zhang, J., Zhu, J., Bu, X., Cushion, M., Kinane, T. B., Avraham, H., and Koziel, H. (2005). Cdc42 and RhoB activation are required for mannose receptor-mediated phagocytosis by human alveolar macrophages. Mol. Biol. Cell 16,824-834.