Differential IL-17 production and mannan recognition contribute to fungal pathogenicity and commensalism

Journal of Immunology

Volumn 184, Issue 8, 2010, Pages 4258-4268

  Rizzetto, Lisa ^a   Kuka, Mirela ^b   De Filippo, Carlotta ^a   Cambi, Alessandra ^c   Netea, Mihai G ^d   Beltrame, Luca ^a   Napolitani, Giorgio ^e   Torcia, Maria Gabriella ^a   D'Oro, Ugo ^b   Cavalieri, Duccio ^a  

^a UNIVERSITY OF FLORENCE   (Italy)

^b NOVARTIS VACCINES AND DIAGNOSTICS   (Italy)

^c RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^d RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^e V V Vela   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 12P70; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 6; MANNAN; INTERLEUKIN 12;

ANIMAL EXPERIMENT; ANTIGEN RECOGNITION; ARTICLE; CANDIDA ALBICANS; CD4+ T LYMPHOCYTE; CELLULAR IMMUNITY; COMMENSALISM; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; EFFECTOR CELL; FUNGAL CELL; FUNGAL VIRULENCE; FUNGUS HYPHAE; FUNGUS SPORE; HOST CELL; HUMAN; HUMAN CELL; IMMUNOSTIMULATION; LYMPHOCYTE DIFFERENTIATION; NONHUMAN; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE; TH1 CELL; TH17 CELL; BIOSYNTHESIS; CELL DIFFERENTIATION; CELL WALL; CHEMISTRY; COMPARATIVE STUDY; CONFORMATION; CYTOLOGY; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; MONOCYTE; PATHOGENICITY; PHYSIOLOGY;

CANDIDA ALBICANS; CARBOHYDRATE CONFORMATION; CD4-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; CELL WALL; DENDRITIC CELLS; HUMANS; HYPHAE; INTERLEUKIN-12; INTERLEUKIN-17; MANNANS; MONOCYTES; SACCHAROMYCES CEREVISIAE; SPORES, FUNGAL; TH1 CELLS;

EID: 77952766743     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0902972     Document Type: Article

References (51)

1. Medzhitov, R. 2007. Recognition of microorganisms and activation of the immune response. Nature 449: 819-826. (Pubitemid 47598622)
2. Richardson, M. D. 2005. Changing patterns and trends in systemic fungal infections. J. Antimicrob. Chemother. 56(Suppl 1): i5-i11.
3. Cavalieri, D., P. E. McGovern, D. L. Hartl, R. Mortimer, and M. Polsinelli. 2003. Evidence for S. cerevisiae fermentation in ancient wine. J. Mol. Evol. 57(Suppl 1): S226-S232.
4. Salonen, J. H., M. D. Richardson, K. Gallacher, J. Issakainen, H. Helenius, O. P. Lehtonen, and J. Nikoskelainen. 2000. Fungal colonization of haematological patients receiving cytotoxic chemotherapy: emergence of azole-resistant Saccharomyces cerevisiae. J. Hosp. Infect. 45: 293-301.
5. Muñoz, P., E. Bouza, M. Cuenca-Estrella, J. M. Eiros, M. J. Pérez, M. Sánchez-Somolinos, C. Rincón, J. Hortal, and T. Peláez. 2005. Saccharomyces cerevisiae fungemia: an emerging infectious disease. Clin. Infect. Dis. 40: 1625-1634.
6. Sethi, N., and W. Mandell. 1988. Saccharomyces fungemia in a patient with AIDS. N. Y. State J. Med. 88: 278-279.
7. Hernanz-Falcón, P., O. Joffre, D. L. Williams, and C. Reis e Sousa. 2009. Internalization of Dectin-1 terminates induction of inflammatory responses. Eur. J. Immunol. 39: 507-513.
8. Newman, S. L., and A. Holly. 2001. Candida albicans is phagocytosed, killed, and processed for antigen presentation by human dendritic cells. Infect. Immun. 69: 6813-6822.
9. Cambi, A., M. G. Netea, H. M. Mora-Montes, N. A. Gow, S. V. Hato, D. W. Lowman, B. J. Kullberg, R. Torensma, D. L. Williams, and C. G. Figdor. 2008. Dendritic cell interaction with Candida albicans critically depends on N-linked mannan. J. Biol. Chem. 283: 20590-20599.
10. van der Veerdonk, F. L., R. J. Marijnissen, B. J. Kullberg, H. J. Koenen, S. C. Cheng, I. Joosten, W. B. van den Berg, D. L. Williams, J. W. van der Meer, L. A. Joosten, and M. G. Netea. 2009. The macrophage mannose receptor induces IL-17 response to Candida albicans. Cell Host Microbe 5: 1-12.
11. d'Ostiani, C. F., G. Del Sero, A. Bacci, C. Montagnoli, A. Spreca, A. Mencacci, P. Ricciardi-Castagnoli, and L. Romani. 2000. Dendritic cells discriminate between yeasts and hyphae of the fungus Candida albicans. Implications for initiation of T helper cell immunity in vitro and in vivo. J. Exp. Med. 191: 1661-1674.
12. Gantner, B. N., R. M. Simmons, and D. M. Underhill. 2005. Dectin-1 mediates macrophage recognition of Candida albicans yeast but not filaments. EMBO J. 24: 1277-1286.
13. Kreger-Van Rij, N. J. 1978. Electron microscopy of germinating ascospores of Saccharomyces cerevisiae. Arch. Microbiol. 117: 73-77.
14. Coluccio, A., E. Bogengruber, M. N. Conrad, M. E. Dresser, P. Briza, and A. M. Neiman. 2004. Morphogenetic pathway of spore wall assembly in Saccharomyces cerevisiae. Eukaryot. Cell 3: 1464-1475. (Pubitemid 40025105)
15. Chorvatovicová, D., E. Machová, J. Sandula, and G. Kogan. 1999. Protective effect of the yeast glucomannan against cyclophosphamide- induced mutagenicity. G. Mutat. Res 21: 117-122.
16. Lowman, D. W., D. A. Ferguson, and D. L. Williams. 2003. Structural characterization of (1→3)-beta-D-glucans isolated from blastospore and hyphal forms of Candida albicans. Carbohydr. Res. 338: 1491-1496.
17. Geijtenbeek, T. B., R. Torensma, S. J. van Vliet, G. C. van Duijnhoven, G. J. Adema, Y. van Kooyk, and C. G. Figdor. 2000. Identification of DC-SIGN, a novel dendritic cell-specific ICAM-3 receptor that supports primary immune responses. Cell 100: 575-585.
18. Casalone, E., C. Barberio, D. Cavalieri, I. Ceccarelli, M. Riparbelli, S. Ugolini, and M. Polsinelli. 1999. Disruption and phenotypic analysis of six novel genes from chromosome IV of Saccharomyces cerevisiae reveal YDL060w as an essential gene for vegetative growth. Yeast 15: 1691-1701.
19. Sallusto, F., and A. Lanzavecchia. 1994. Efficient presentation of soluble antigen by cultured human dendritic cells is maintained by granulocyte/macrophage colony-stimulating factor plus interleukin 4 and downregulated by tumor necrosis factor alpha. J. Exp. Med. 179: 1109-1118.
20. Choi, H. S., J. W. Kim, Y. N. Cha, and C. Kim. 2006. A quantitative nitroblue tetrazolium assay for determining intracellular superoxide anion production in phagocytic cells. J. Immunoassay Immunochem. 27: 31-44.
21. Cambi, A., K. Gijzen, J. M. de Vries, R. Torensma, B. Joosten, G. J. Adema, M. G. Netea, B. J. Kullberg, L. Romani, and C. G. Figdor. 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.
22. Du, P., W. A. Kibbe, and S. M. Lin. 2007. nuID: a universal naming scheme of oligonucleotides for illumina, affymetrix, and other microarrays. Biol.Direct 2:16.
23. Du, P., W. A. Kibbe, and S. M. Lin. 2008. lumi: a pipeline for processing Illumina microarray. Bioinformatics 24: 1547-1548.
24. Hong, F., R. Breitling, C. W. McEntee, B. S. Wittner, J. L. Nemhauser, and J. Chory. 2006. RankProd: a bioconductor package for detecting differentially expressed genes in meta-analysis. Bioinformatics 22: 2825-2827.
25. Cavalieri, D., C. Castagnini, S. Toti, K. Maciag, T. Kelder, L. Gambineri, S. Angioli, and P. Dolara. 2007. Eu.Gene Analyzer a tool for integrating gene expression data with pathway databases. Bioinformatics 23: 2631-2632.
26. Beltrame, L., L. Rizzetto, R. Paola, P. Rocca-Serra, L. Gambineri, C. Battaglia, and D. Cavalieri. 2009. Using pathway signatures as means of identifying similarities among microarray experiments. PLoS One 4: e4128.
27. Robinson, M. J., F. Osorio, M. Rosas, R. P. Freitas, E. Schweighoffer, O. Gross, J. S. Verbeek, J. Ruland, V. Tybulewiez, G. G. Beown, et al. 2009. Dectin-2 is a Syk-coupled pattern recognition receptor crucial for Th17 responses to fungal infection. J. Exp. Med. 206: 2037-2051.
28. Romani, L. 2008. Cell mediated immunity to fungi: a reassessment. Med. Mycol. 46: 515-529.
29. Steinman, R. M., D. Hawiger, and M. C. Nussenzweig. 2003. Tolerogenic dendritic cells. Annu. Rev. Immunol. 21: 685-711.
30. Romani, L., and P. Puccetti. 2007. Controlling pathogenic inflammation to fungi. Expert Rev. Anti Infect. Ther. 5: 1007-1017.
31. Reske, A., G. Pollara, C. Krummenacher, D. R. Katz, and B. M. Chain. 2008 Glycoprotein-dependent and TLR2-independent innate immune recognition of herpes simplex virus-1 by dendritic cells. J. Immunol. 180: 7525-7536.
32. Bonecchi, R., G. Bianchi, P. P. Bordignon, D. D'Ambrosio, R. Lang, A. Borsatti, S. Sozzani, P. Allavena, P. A. Gray, A. Mantovani, and F. Sinigaglia. 1998. Differential expression of chemokine receptors and chemotactic responsiveness of type 1 T helper cells (Th1s) and Th2s. J. Exp. Med. 187: 129-134.
33. Acosta-Rodriguez, E. V., L. Rivino, J. Geginat, D. Jarrossay, M. Gattorno, A. Lanzavecchia, F. Sallusto, and G. Napolitani. 2007. Surface phenotype and antigenic specificity of human interleukin 17-producing T helper memory cells. Nat. Immunol. 8: 639-646.
34. Hirota, K, H. Yoshitomi, M. Hashimoto, S. Maeda, S. Teradaira, N. Sugimoto, T. Yamaguchi, T. Nomura, H. Ito, T. Nakamura, et al. 2007. Preferential recruitment of CCR6-expressing Th17 cells to inflamed joints via CCL20 in rheumatoid arthritis and its animal model. J. Exp. Med. 204: 2803-2812.
35. Reboldi, A., C. Coisne, D. Baumjohann, F. Benvenuto, D. Bottinelli, S. Lira, A. Uccelli, A. Lanzavecchia, B. Engelhardt, and F. Sallusto. 2009. C-C chemokine receptor 6-regulated entry of TH-17 cells into the CNS through the choroid plexus is required for the initiation of EAE. Nat. Immunol. 10: 514-523.
36. Chiani, P., C. Bromuro, and A. Torosantucci. 2000. Defective induction of interleukin-12 in human monocytes by germ-tube forms of Candida albicans. Infect. Immun. 68: 5628-5634.
37. Vulcano, M., S. Dusi, D. Lissandrini, R. Badolato, P.Mazzi, E. Borroni, E. Calleri, M. Donini, A. Plebani, L. Notarangelo, et al. 2004. Toll receptor-mediated regulation of NADPH oxidase in human dendritic cells. J. Immunol. 173: 5749-5756.
38. Donini, M., E. Zenaro, N. Tamassia, and S. Dusi. 2007. NADPH oxidase of human dendritic cells: role in Candida albicans killing and regulation by interferons, dectin-1 and CD206. Eur. J. Immunol. 37: 1194-1203.
39. Bettelli, E., T. Korn, M. Oukka, and V. K. Kuchroo. 2008. Induction and effector functions of T(H)17 cells. Nature 453: 1051-1057.
40. Netea, M. G., G. D. Brown, B. J. Kullberg, and N. A. Gow. 2008. An integrated model of the recognition of Candida albicans by the innate immune system. Natl. Rev. 6: 67-78.
41. Cambi, A., M. Koopman, and C. G. Figdor. 2005. How C-type lectins detect pathogens. Cell. Microbiol. 7: 481-488.
42. Wheeler, R. T., and G. R. Fink. 2006. A drug-sensitive genetic network masks fungi from the immune system. PLoS Pathog. 2: e35.
43. Huang, Q., D. Liu, P. Majewski, L. C. Schulte, J. M. Korn, R. A. Young, E. S. Lander, and N. Hacohen. 2001. The plasticity of dendritic cell responses to pathogens and their components. Science 294: 870-875.
44. Liti, G., D. M. Carter, A. M. Moses, J. Warringer, L. Parts, S. A. James, R. P. Davey, I. N. Roberts, A. Burt, V. Koufopanou, et al. 2009. Population genomics of domestic and wild yeasts. Nature 458: 337-341.
45. Huang, W., L. Na, P. L. Fidel, and P. Schwarzenberger. 2004. Requirement of interleukin-17A for systemic anti-Candida albicans host defense in mice. J. Infect. Dis. 190: 624-631.
46. Milner, J. D., J. M. Brenchley, A. Laurence, A. F. Freeman, B. J. Hill, K. M. Elias, Y. Kanno, C. Spalding, H. Z. Elloumi, M. L. Paulson, et al. 2008. Impaired T(H)17 cell differentiation in subjects with autosomal dominant hyper-IgE syndrome. Nature 452: 773-776.
47. Conti, H. R., F. Shen, N. Nayyar, E. Stocum, J. N. Sun, M. J. Lindemann, A. W. Ho, J. H. Hai, J. J. Yu, J. W. Jung, et al. 2009. Th17 cells and IL-17 receptor signaling are essential for mucosal host defense against oral candidiasis. J. Exp. Med. 16: 299-311.
48. Urban, C. F., U. Reichard, V. Brinkmann, and A. Zychlinsky. 2008. Neutrophil extracellular traps capture and kill Candida albicans yeast and hyphal forms. Cell. Microbiol. 8: 668-676.
49. Standaert-Vitse, A., T. Jouault, P. Vandewalle, C. Mille, M. Seddik, B. Sendid, J. M. Mallet, J. F. Colombel, and D. Poulain. 2006. Candida albicans is an immunogen for anti-Saccharomyces cerevisiae antibody markers of Crohn's disease. Gastroenterology 130: 1764-1775.
50. Coluccio, A. E., R. K. Rodriguez, M. J. Kernan, and A. M. Neiman. 2008. The yeast spore wall enables spores to survive passage through the digestive tract of Drosophila. PLoS One 3: e2873.
51. Mortimer, R. K. 2000. Evolution and variation of the yeast (Saccharomyces) genome. Genome Res. 10: 403-409.