Dual TCR expression biases lung inflammation in DO11.10 transgenic mice and promotes neutrophilia via microbiota-induced Th17 differentiation

Journal of Immunology

Volumn 187, Issue 7, 2011, Pages 3530-3537

  Lemaire, Muriel M ^a,b   Dumoutier, Laure ^a,b   Warnier, Guy ^a   Uyttenhove, Catherine ^a   Van Snick, Jacques ^a,b   De Heusch, Magali ^a,b   Stevens, Monique ^a   Renauld, Jean Christophe ^a,b  

^a LUDWIG INSTITUTE FOR CANCER RESEARCH   (Belgium)

^b DE DUVE INSTITUTE   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 17; INTERLEUKIN 17F; OVALBUMIN; PAROMOMYCIN; PENICILLIN G; STREPTOMYCIN; T LYMPHOCYTE RECEPTOR; T LYMPHOCYTE RECEPTOR ALPHA CHAIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGEN SPECIFICITY; ARTICLE; ASTHMA; CD4+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL POPULATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; EOSINOPHILIA; FEMALE; IN VITRO STUDY; IN VIVO STUDY; INTESTINE FLORA; LYMPHOCYTE COUNT; LYMPHOCYTE DIFFERENTIATION; MEMORY CELL; MICROFLORA; MOUSE; NEUTROPHIL CHEMOTAXIS; NEUTROPHILIA; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RESPIRATORY TRACT INFLAMMATION; TH17 CELL; TRANSGENIC MOUSE;

ADOPTIVE TRANSFER; ANIMALS; CELL DIFFERENTIATION; CELL SEPARATION; CHEMOTAXIS, LEUKOCYTE; FLOW CYTOMETRY; INTERFERON-GAMMA; INTERLEUKIN-17; LYMPHOCYTE ACTIVATION; MICE; MICE, TRANSGENIC; NEUTROPHILS; OVALBUMIN; PNEUMONIA; RECEPTORS, ANTIGEN, T-CELL; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TH17 CELLS;

EID: 80053485014     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1101720     Document Type: Article

References (43)

1. Wills-Karp, M. 1999. Immunologic basis of antigen-induced airway hyperresponsiveness. Annu. Rev. Immunol. 17: 255-281. (Pubitemid 29241125)
2. Renauld, J. C. 2001. New insights into the role of cytokines in asthma. J. Clin. Pathol. 54: 577-589.
3. Kips, J. C., G. P. Anderson, J. J. Fredberg, U. Herz, M. D. Inman, M. Jordana, D. M. Kemeny, J. Lötvall, R. A. Pauwels, C. G. Plopper, et al. 2003. Murine models of asthma. Eur. Respir. J. 22: 374-382. (Pubitemid 36987013)
4. Wang, Y. H., and Y. J. Liu. 2008. The IL-17 cytokine family and their role in allergic inflammation. Curr. Opin. Immunol. 20: 697-702.
5. Nembrini, C., B. J. Marsland, and M. Kopf. 2009. IL-17-producing T cells in lung immunity and inflammation. J. Allergy Clin. Immunol. 123: 986-994; quiz 995-996.
6. Molet, S., Q. Hamid, F. Davoine, E. Nutku, R. Taha, N. Pagé, R. Olivenstein, J. Elias, and J. Chakir. 2001. IL-17 is increased in asthmatic airways and induces human bronchial fibroblasts to produce cytokines. J. Allergy Clin. Immunol. 108: 430-438. (Pubitemid 32881066)
7. Zhao, Y., J. Yang, Y. D. Gao, and W. Guo. 2010. Th17 immunity in patients with allergic asthma. Int. Arch. Allergy Immunol. 151: 297-307.
8. Barczyk, A., W. Pierzchala, and E. Sozañska. 2003. Interleukin-17 in sputum correlates with airway hyperresponsiveness to methacholine. Respir. Med. 97: 726-733. (Pubitemid 36675678)
9. He, R., M. K. Oyoshi, H. Jin, and R. S. Geha. 2007. Epicutaneous antigen exposure induces a Th17 response that drives airway inflammation after inhalation challenge. Proc. Natl. Acad. Sci. USA 104: 15817-15822. (Pubitemid 350035382)
10. Kim, S. R., K. S. Lee, S. J. Park, K. H. Min, K. Y. Lee, Y. H. Choe, Y. R. Lee, J. S. Kim, S. J. Hong, and Y. C. Lee. 2007. PTEN down-regulates IL-17 expression in a murine model of toluene diisocyanate-induced airway disease. J. Immunol. 179: 6820-6829.
11. Wilson, R. H., G. S. Whitehead, H. Nakano, M. E. Free, J. K. Kolls, and D. N. Cook. 2009. Allergic sensitization through the airway primes Th17- dependent neutrophilia and airway hyperresponsiveness. Am. J. Respir. Crit. Care Med. 180: 720-730.
12. Hellings, P. W., A. Kasran, Z. Liu, P. Vandekerckhove, A. Wuyts, L. Overbergh, C. Mathieu, and J. L. Ceuppens. 2003. Interleukin-17 orchestrates the granulocyte influx into airways after allergen inhalation in a mouse model of allergic asthma. Am. J. Respir. Cell Mol. Biol. 28: 42-50. (Pubitemid 36017049)
13. Liang, S. C., A. J. Long, F. Bennett, M. J. Whitters, R. Karim, M. Collins, S. J. Goldman, K. Dunussi-Joannopoulos, C. M. Williams, J. F. Wright, and L. A. Fouser. 2007. An IL-17F/A heterodimer protein is produced by mouse Th17 cells and induces airway neutrophil recruitment. J. Immunol. 179: 7791-7799.
14. McKinley, L., J. F. Alcorn, A. Peterson, R. B. Dupont, S. Kapadia, A. Logar, A. Henry, C. G. Irvin, J. D. Piganelli, A. Ray, and J. K. Kolls. 2008. TH17 cells mediate steroid-resistant airway inflammation and airway hyperresponsiveness in mice. J. Immunol. 181: 4089-4097.
15. He, R., H. Y. Kim, J. Yoon, M. K. Oyoshi, A. MacGinnitie, S. Goya, E. J. Freyschmidt, P. Bryce, A. N. McKenzie, D. T. Umetsu, et al. 2009. Exaggerated IL-17 response to epicutaneous sensitization mediates airway inflammation in the absence of IL-4 and IL-13. J. Allergy Clin. Immunol. 124: 761-770.e1.
16. Park, S. J., K. S. Lee, S. R. Kim, K. H. Min, Y. H. Choe, H. Moon, H. J. Chae, W. H. Yoo, and Y. C. Lee. 2009. Peroxisome proliferator-activated receptor gamma agonist down-regulates IL-17 expression in a murine model of allergic airway inflammation. J. Immunol. 183: 3259-3267.
17. Wakashin, H., K. Hirose, Y. Maezawa, S. Kagami, A. Suto, N. Watanabe, Y. Saito, M. Hatano, T. Tokuhisa, Y. Iwakura, et al. 2008. IL-23 and Th17 cells enhance Th2-cell-mediated eosinophilic airway inflammation in mice. Am. J. Respir. Crit. Care Med. 178: 1023-1032.
18. Knott, P. G., P. R. Gater, and C. P. Bertrand. 2000. Airway inflammation driven by antigen-specific resident lung CD4(+) T cells in alphabeta-T cell receptor transgenic mice. Am. J. Respir. Crit. Care Med. 161: 1340-1348. (Pubitemid 30243850)
19. Wilder, J. A., D. D. Collie, D. E. Bice, Y. Tesfaigzi, C. R. Lyons, and M. F. Lipscomb. 2001. Ovalbumin aerosols induce airway hyperreactivity in naïve DO11.10 T cell receptor transgenic mice without pulmonary eosinophilia or OVA-specific antibody. J. Leukoc. Biol. 69: 538-547. (Pubitemid 32294838)
20. Tanaka, S., T. Yoshimoto, T. Naka, S. Nakae, Y. Iwakura, D. Cua, and M. Kubo. 2009. Natural occurring IL-17 producing T cells regulate the initial phase of neutrophil mediated airway responses. J. Immunol. 183: 7523-7530.
21. Murphy, K. M., A. B. Heimberger, and D. Y. Loh. 1990. Induction by antigen of intrathymic apoptosis of CD4+CD8+TCRlo thymocytes in vivo. Science 250: 1720-1723. (Pubitemid 120031881)
22. Billiau, A., H. Heremans, F. Vandekerckhove, and C. Dillen. 1987. Anti-interferon- gamma antibody protects mice against the generalized Shwartzman reaction. Eur. J. Immunol. 17: 1851-1854. (Pubitemid 18052056)
23. Uyttenhove, C., and J. Van Snick. 2006. Development of an anti-IL-17A autovaccine that prevents experimental auto-immune encephalomyelitis. Eur. J. Immunol. 36: 2868-2874. (Pubitemid 44782560)
24. Uyttenhove, C., R. G. Marillier, F. Tacchini-Cottier, M. Charmoy, R. R. Caspi, J. M. Damsker, S. Goriely, D. Su, J. Van Damme, S. Struyf, et al. 2011. Aminereactive OVA multimers for auto-vaccination against cytokines and other mediators: perspectives illustrated for GCP-2 in L. major infection. J. Leukoc. Biol. 89: 1001-1007.
25. Azzam, H. S., A. Grinberg, K. Lui, H. Shen, E. W. Shores, and P. E. Love. 1998. CD5 expression is developmentally regulated by T cell receptor (TCR) signals and TCR avidity. J. Exp. Med. 188: 2301-2311. (Pubitemid 29028502)
26. Hurst, S. D., S. M. Sitterding, S. Ji, and T. A. Barrett. 1997. Functional differentiation of T cells in the intestine of T cell receptor transgenic mice. Proc. Natl. Acad. Sci. USA 94: 3920-3925. (Pubitemid 27180474)
27. Saparov, A., L. A. Kraus, Y. Cong, J. Marwill, X. Y. Xu, C. O. Elson, and C. T. Weaver. 1999. Memory/effector T cells in TCR transgenic mice develop via recognition of enteric antigens by a second, endogenous TCR. Int. Immunol. 11: 1253-1264.
28. Zhou, P., R. Borojevic, C. Streutker, D. Snider, H. Liang, and K. Croitoru. 2004. Expression of dual TCR on DO11.10 T cells allows for ovalbumin-induced oral tolerance to prevent T cell-mediated colitis directed against unrelated enteric bacterial antigens. J. Immunol. 172: 1515-1523. (Pubitemid 38116795)
29. Alam, S. M., and N. R. Gascoigne. 1998. Posttranslational regulation of TCR Valpha allelic exclusion during T cell differentiation. J. Immunol. 160: 3883-3890. (Pubitemid 28176094)
30. Elliott, J. I., and D. M. Altmann. 1995. Dual T cell receptor alpha chain T cells in autoimmunity. J. Exp. Med. 182: 953-959.
31. Heath, W. R., F. R. Carbone, P. Bertolino, J. Kelly, S. Cose, and J. F. Miller. 1995. Expression of two T cell receptor alpha chains on the surface of normal murine T cells. Eur. J. Immunol. 25: 1617-1623.
32. Padovan, E., G. Casorati, P. Dellabona, S. Meyer, M. Brockhaus, and A. Lanzavecchia. 1993. Expression of two T cell receptor alpha chains: dual receptor T cells. Science 262: 422-424. (Pubitemid 23353384)
33. Schrum, A. G., and L. A. Turka. 2002. The proliferative capacity of individual naive CD4(+) T cells is amplified by prolonged T cell antigen receptor triggering. J. Exp. Med. 196: 793-803.
34. Lee, W. T., J. Cole-Calkins, and N. E. Street. 1996. Memory T cell development in the absence of specific antigen priming. J. Immunol. 157: 5300-5307. (Pubitemid 126448947)
35. Schnyder-Candrian, S., D. Togbe, I. Couillin, I. Mercier, F. Brombacher, V. Quesniaux, F. Fossiez, B. Ryffel, and B. Schnyder. 2006. Interleukin-17 is a negative regulator of established allergic asthma. J. Exp. Med. 203: 2715-2725. (Pubitemid 44833347)
36. Durrant, D. M., S. L. Gaffen, E. P. Riesenfeld, C. G. Irvin, and D. W. Metzger. 2009. Development of allergen-induced airway inflammation in the absence of T-bet regulation is dependent on IL-17. J. Immunol. 183: 5293-5300.
37. Li, X. M., R. K. Chopra, T. Y. Chou, B. H. Schofield, M. Wills-Karp, and S. K. Huang. 1996. Mucosal IFN-gamma gene transfer inhibits pulmonary allergic responses in mice. J. Immunol. 157: 3216-3219. (Pubitemid 126449128)
38. Iwamoto, I., H. Nakajima, H. Endo, and S. Yoshida. 1993. Interferon gamma regulates antigen-induced eosinophil recruitment into the mouse airways by inhibiting the infiltration of CD4+ T cells. J. Exp. Med. 177: 573-576. (Pubitemid 23117112)
39. Fazekas de St. Groth, S., and R. GWebster, . 1966. Disquisitions of original antigenic sin. I. Evidence in man. J. Exp. Med. 124: 331-345.
40. Ji, Q., A. Perchellet, and J. M. Goverman. 2010. Viral infection triggers central nervous system autoimmunity via activation of CD8+ T cells expressing dual TCRs. Nat. Immunol. 11: 628-634.
41. Olivares-Villagómez, D., Y. Wang, and J. J. Lafaille. 1998. Regulatory CD4(+) T cells expressing endogenous T cell receptor chains protect myelin basic protein-specific transgenic mice from spontaneous autoimmune encephalomyelitis. J. Exp. Med. 188: 1883-1894. (Pubitemid 28536776)
42. Sarukhan, A., C. Garcia, A. Lanoue, and H. Von Boehmer. 1998. Allelic inclusion of T cell receptor alpha genes poses an autoimmune hazard due to lowlevel expression of autospecific receptors. Immunity 8: 563-570. (Pubitemid 28264747)
43. Tuovinen, H., J. T. Salminen, and T. P. Arstila. 2006. Most human thymic and peripheral-blood CD4+ CD25+ regulatory T cells express 2 T-cell receptors. Blood 108: 4063-4070. (Pubitemid 44913276)