Immunity and tolerance to Aspergillus involve functionally distinct regulatory T cells and tryptophan catabolism

Journal of Immunology

Volumn 176, Issue 3, 2006, Pages 1712-1723

  Montagnoli, Claudia ^a   Fallarino, Francesca ^a   Gaziano, Roberta ^a   Bozza, Silvia ^a   Bellocchio, Silvia ^a   Zelante, Teresa ^a   Kurup, Wiswanath P ^b   Pitzurra, Lucia ^a   Puccetti, Paolo ^a   Romani, Luigina ^a  

^a UNIVERSITY OF PERUGIA   (Italy)

^b CLEMENT J ZABLOCKI VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD28 ANTIGEN; CD4 ANTIGEN; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; GAMMA INTERFERON; HLA B7 ANTIGEN; INDOLEAMINE 2,3 DIOXYGENASE; INTERLEUKIN 10; INTERLEUKIN 2 RECEPTOR ALPHA; TRANSFORMING GROWTH FACTOR BETA; TRYPTOPHAN;

ALLERGY; AMINO ACID METABOLISM; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASPERGILLUS FUMIGATUS; CATABOLISM; CD25+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CONIDIUM; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; EXPOSURE; FEMALE; FUNGAL SPORE GERMINATION; HOST RESISTANCE; IMMUNOLOGICAL TOLERANCE; IMMUNOREGULATION; INFLAMMATION; INTERFERON PRODUCTION; MOUSE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; T LYMPHOCYTE ACTIVATION; TH2 CELL;

EID: 31144456173     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.176.3.1712     Document Type: Article

References (53)

1. Marr, K. A., T. Patterson, and D. Denning. 2002. Aspergillosis: pathogenesis, clinical manifestations, and therapy. Infect. Dis. Clin. North Am. 16: 875-894.
2. Kurup, V. P. 2000. Immunology of allergic bronchopulmonary aspergillosis. Ind. J. Chest. Dis. Allied Sci. 42: 225-237.
3. Garlanda, C., E. Hirsch, S. Bozza, A. Salustri, M. De Acetis, R. Nota, A. Maccagno, F. Riva, B. Bottazzi, G. Peri, et al. 2002. Non-redundant role of the long pentraxin PTX3 in anti-fungal innate immune response. Nature 420: 182-186.
4. Akbari, O., R. H. DeKruyff, and D. T. Umetsu. 2001. Pulmonary dendritic cells producing IL-10 mediate tolerance induced by respiratory exposure to antigen. Nat. Immunol 2: 725-731.
5. Akbari, O., G. J. Freeman, E. H. Meyer, E. A. Greenfield, T. T. Chang, A. H. Sharpe, G. Berry, R. H. DeKruyff, and D. T. Umetsu. 2002. Antigen-specific regulatory T cells develop via the ICOS-ICOS-ligand pathway and inhibit allergen-induced airway hyperreactivity. Nat. Med. 8: 1024-1032.
6. + T cells expressing membrane-bound TGF-β and FOXP3. J. Clin. Invest. 114: 28-38.
7. Bluestone, J. A., and A. K. Abbas. 2003. Natural versus adaptive regulatory T cells. Nat. Rev. Immunol. 3: 253-257.
8. O'Garra, A., and P. Vieira. 2004. Regulatory T cells and mechanisms of immune system control. Nat. Med. 10: 801-805.
9. von Boehmer, H. 2005. Mechanisms of suppression by suppressor T cells. Nat. Immunol. 6: 338-344.
10. Belkaid, Y., and B. T. Rouse. 2005. Natural regulatory T cells in infectious disease. Nat. Immunol. 6: 353-360.
11. Mills, K. H. 2004. Regulatory T cells: friend or foe in immunity to infection? Nat. Rev. Immunol. 4: 841-855.
12. + T cell-mediated pulmonary hyperinflammation driven by Pneumocystis carinii in immunodeficient mice. Eur. J. Immunol. 32: 1282-1291.
13. + regulatory T cells are essential components of the memory-protective immunity to Candida albicans. J. Immunol. 169: 6298-6308.
14. Tai, X., M. Cowan, L. Feigenbaum, and A. Singer. 2005. CD28 costimulation of developing thymocytes induces Foxp3 expression and regulatory T cell differentiation independently of interleukin 2. Nat. Immunol. 6: 152-162.
15. + regulatory T cells in vivo requires B7 costimulation, but not the thymus. J. Exp. Med. 201: 127-137.
16. Lohr, J., B. Knoechel, S. Jiang, A. H. Sharpe, and A. K. Abbas. 2003. The inhibitory function of B7 costimulators in T cell responses to foreign and self-antigens. Nat. Immunol. 4: 664-669.
17. Bozza, S., F. Fallarino, L. Pitzurra, T. Zelante, C. Montagnoli, S. Bellocchio, P. Mosci, C. Vacca, P. Puccetti, and L. Romani. 2005. A crucial role for tryptophan catabolism at the host/Candida albicans interface. J. Immunol 174: 2910-2918.
18. Romani, L., F. Bistoni, R. Gaziano, S. Bozza, C. Montagnoli, K. Perruccio, L. Pitzurra, S. Bellocchio, A. Velardi, G. Rasi, P. Di Francesco, and E. Garaci. 2004. Thymosin α-activates dendritic cells for antifungal Th1 resistance through Toll-like receptor signaling. Blood 103: 4232-4239.
19. Bozza, S., R. Gaziano, A. Spreca, A. Bacci, C. Montagnoli, P. di Francesco, and L. Romani. 2002. Dendritic cells transport conidia and hyphae of Aspergillus fumigatus from the airways to the draining lymph nodes and initiate disparate Th responses to the fungus. J. Immunol. 168: 1362-1371.
20. Hogaboam, C. M., K. Blease, B. Mehrad, M. L. Steinhauser, T. J. Standiford, S. L. Kunkel, and N. W. Lukacs. 2000. Chronic airway hyperreactivity, goblet cell hyperplasia, and peribronchial fibrosis during allergic airway disease induced by Aspergillus fumigatus. Am. J. Pathol. 156: 723-732.
21. Fallarino, F., U. Grohmann, K. W. Hwang, C. Orabona, C. Vacca, R. Bianchi, M. L. Belladonna, M. C. Fioretti, M. L. Alegre, and P. Puccetti. 2003. Modulation of tryptophan catabolism by regulatory T cells. Nat. Immunol. 4: 1206-1212.
22. + myeloid cells inhibit development of antifungal Th1 immunity in mice with candidiasis. J. Immunol. 169: 3180-3190.
23. Grohmann, U., C. Orabona, F. Fallarino, C. Vacca, F. Calcinaro, A. Falorni, P. Candeloro, M. L. Belladonna, R. Bianchi, M. C. Fioretti, and P. Puccetti. 2002. CTLA-4-Ig regulates tryptophan catabolism in vivo. Nat. Immunol. 3: 1097-1101.
24. Banerjee, B., K. J. Kelly, J. N. Fink, J. D. Henderson, Jr., N. K. Bansal, and V. P. Kurup. 2004. Modulation of airway inflammation by immunostimulatory CpG oligodeoxynucleotides in a murine model of allergic aspergillosis. Infect. Immun. 72: 6087-6094.
25. Sallusto, F., C. R. Mackay, and A. Lanzavecchia. 2000. The role of chemokine receptors in primary, effector, and memory immune responses. Annu. Rev. Immunol. 18: 593-620.
26. Bromley, S. K., S. Y. Thomas, and A. D. Luster. 2005. Chemokine receptor CCR7 guides T cell exit from peripheral tissues and entry into afferent lymphatics. Nat. Immunol. 6: 895-901.
27. + regulatory T cells in immunological tolerance to self and non-self. Nat. Immunol. 6: 345-352.
28. + T(R) cells suppress innate immune pathology through cytokine-dependent mechanisms. J. Exp. Med. 197: 111-119.
29. Romani, L. 2004. Immunity to fungal infections. Nat. Rev. Immunol 4: 11-23.
30. Orabona, C., U. Grohmann, M. L. Belladonna, F. Fallarino, C. Vacca, R. Bianchi, S. Bozza, C. Volpi, B. L. Salomon, M. C. Fioretti, L. Romani, and P. Puccetti. 2004. CD28 induces immunostimulatory signals in dendritic cells via CD80 and CD86. Nat. Immunol. 5: 1134-1142.
31. Hayashi, T., L. Beck, C. Rossetto, X. Gong, O. Takikawa, K. Takabayashi, D. H. Broide, D. A. Carson, and E. Raz. 2004. Inhibition of experimental asthma by indoleamine 2,3-dioxygenase. J. Clin. Invest. 114: 270-279.
32. Levitz, S. M., and R. D. Diamond. 1985. Mechanisms of resistance of Aspergillus fumigatus Conidia to killing by neutrophils in vitro. J. Infect. Dis. 152: 33-42.
33. + T cells controlling distinct organ-specific autoimmune diseases. Proc. Natl. Acad. Sci. USA 100: 15806-15811.
34. + regulatory T cells protects from lethal acute GVHD. Blood 105: 2220-2226.
35. Roilides, E., A. Dimitriadou, I. Kadiltsoglou, T. Sein, J. Karpouzas, P. A. Pizzo, and T. J. Walsh. 1997. IL-10 exerts suppressive and enhancing effects on antifungal activity of mononuclear phagocytes against Aspergillus fumigatus. J. Immunol. 158: 322-329.
36. Cenci, E., A. Mencacci, C. Fe d'Ostiani, C. Montagnoli, A. Bacci, G. Del Sero, S. Perito, F. Bistoni, and L. Romani. 1998. Cytokine- and T-helper-dependent immunity in murine aspergillosis. Res. Immunol. 149: 445-454.
37. Zuany-Amorim, C., E. Sawicka, C. Manlius, A. Le Moine, L. R. Brunet, D. M. Kemeny, G. Bowen, G. Rook, and C. Walker. 2002. Suppression of airway eosinophilia by killed Mycobacterium vaccae-induced allergen-specific regulatory T-cells. Nat. Med. 8: 625-629.
38. Stock, P., O. Akbari, G. Berry, G. J. Freeman, R. H. Dekruyff, and D. T. Umetsu. 2004. Induction of T helper type 1-like regulatory cells that express Foxp3 and protect against airway hyper-reactivity. Nat. Immunol. 5: 1149-1156.
39. Grunig, G., D. B. Corry, M. W. Leach, B. W. Seymour, V. P. Kurup, and D. M. Rennick. 1997. Interleukin-10 is a natural suppressor of cytokine production and inflammation in a murine model of allergic bronchopulmonary aspergillosis. J. Exp. Med. 185: 1089-1099.
40. Casaulta, C., M. H. Schoni, M. Weichel, R. Crameri, M. Jutel, I. Daigle, M. Akdis, K. Blaser, and C. A. Akdis. 2003. IL-10 controls Aspergillus fumigatus- and Pseudomonas aeruginosa-specific T-cell response in cystic fibrosis. Pediatr. Res. 53: 313-319.
41. Munn, D. H., M. D. Sharma, J. R. Lee, K. G. Jhaver, T. S. Johnson, D. B. Keskin, B. Marshall, P. Chandler, S. J. Antonia, R. Burgess, C. L. Slingluff, Jr., and A. L. Mellor. 2002. Potential regulatory function of human dendritic cells expressing indoleamine 2,3-dioxygenase. Science 297: 1867-1870.
42. McMillan, S. J., G. Xanthou, and C. M. Lloyd. 2005. Manipulation of allergen-induced airway remodeling by treatment with anti-TGF-β antibody: effect on the Smad signaling pathway. J. Immunol. 174: 5774-5780.
43. Paust, S., L. Lu, N. McCarty, and H. Cantor. 2004. Engagement of B7 on effector T cells by regulatory T cells prevents autoimmune disease. Proc. Natl. Acad. Sci. USA 101: 10398-10403.
44. Odemuyiwa, S. O., A. Ghahary, Y. Li, L. Puttagunta, J. E. Lee, S. Musat-Marcu, and R. Moqbel. 2004. Cutting edge: human eosinophils regulate T cell subset selection through indoleamine 2,3-dioxygenase. J. Immunol. 173: 5909-5913.
45. Huh, J. C., D. H. Strickland, F. L. Jahnsen, D. J. Turner, J. A. Thomas, S. Napoli, I. Tobagus, P. A. Stumbles, P. D. Sly, and P. G. Holt. 2003. Bidirectional interactions between antigen-bearing respiratory tract dendritic cells (DCs) and T cells precede the late phase reaction in experimental asthma: DC activation occurs in the airway mucosa but not in the lung parenchyma. J. Exp. Med. 198: 19-30.
46. de Heer, H. J., H. Hammad, T. Soullie, D. Hijdra, N. Vos, M. A. Willart, H. C. Hoogsteden, and B. N. Lambrecht. 2004. Essential role of lung plasmacytoid dendritic cells in preventing asthmatic reactions to harmless inhaled antigen. J. Exp. Med. 200: 89-98.
47. Dahl, M. E., K. Dabbagh, D. Liggitt, S. Kim, and D. B. Lewis. 2004. Viral-induced T helper type 1 responses enhance allergic disease by effects on lung dendritic cells. Nat. Immunol. 5: 337-343.
48. Umetsu, D. T., J. J. McIntire, O. Akbari, C. Macaubas, and R. H. DeKruyff. 2002. Asthma: an epidemic of dysregulated immunity. Nat. Immunol. 3: 715-720.
49. Arora, S., Y. Hernandez, J. R. Erb-Downward, R. A. McDonald, G. B. Toews, and G. B. Huffnagle. 2005. Role of IFN-γ in regulating T2 immunity and the development of alternatively activated macrophages during allergic bronchopulmonary mycosis. J. Immunol. 174: 6346-6356.
50. Heaton, T., J. Rowe, S. Turner, R. C. Aalberse, N. de Klerk, D. Suriyaarachchi, M. Serralha, B. J. Holt, E. Hollams, S. Yerkovich, et al. 2005. An immunoepidemiological approach to asthma: identification of in-vitro T-cell response patterns associated with different wheezing phenotypes in children. Lancet 365: 142-149.
51. Hansen, G., G. Berry, R. H. DeKruyff, and D. T. Umetsu. 1999. Allergen-specific Th1 cells fail to counterbalance Th2 cell-induced airway hyperreactivity but cause severe airway inflammation. J. Clin. Invest. 103: 175-183.
52. Hagendorens, M. M., D. G. Ebo, A. J. Schuerwegh, A. Huybrechs, H. P. Van Bever, C. H. Bridts, L. S. De Clerck, and W. J. Stevens. 2003. Differences in circulating dendritic cell subtypes in cord blood and peripheral blood of healthy and allergic children. Clin. Exp. Allergy 33: 633-639.
53. von Bubnoff, D., R. Fimmers, M. Bogdanow, H. Matz, S. Koch, and T. Bieber. 2004. Asymptomatic atopy is associated with increased indoleamine 2,3-dioxygenase activity and interleukin-10 production during seasonal allergen exposure. Clin. Exp. Allergy 34: 1056-1063.