Natural Foxp3+ regulatory T cells inhibit Th2 polarization but are biased toward suppression of Th17-driven lung inflammation

Journal of Leukocyte Biology

Volumn 88, Issue 3, 2010, Pages 537-546

  Girtsman, Teri ^a   Jaffar, Zeina ^a   Ferrini, Maria ^a   Shaw, Pamela ^a   Roberts, Kevan ^a  

^a UNIVERSITY OF MONTANA   (United States)

Author keywords

Airway inflammation; CD4+; nTregs; Regulation

Indexed keywords

GAMMA INTERFERON; GLUCOCORTICOID INDUCED TUMOR NECROSIS FACTOR RECEPTOR; INTERLEUKIN 17; INTERLEUKIN 4; OX40 LIGAND; TRANSCRIPTION FACTOR FOXP3;

ANIMAL CELL; ANIMAL MODEL; ARTICLE; BAGG ALBINO MOUSE; CD4+ CD25+ T LYMPHOCYTE; CELL CULTURE; CELL DIFFERENTIATION; CELL TRANSFER; CONTROLLED STUDY; CYTOKINE RELEASE; FLUORESCENCE ACTIVATED CELL SORTING; IMMUNOSUPPRESSIVE TREATMENT; MOUSE; NONHUMAN; PNEUMONIA; POLARIZATION; PRIORITY JOURNAL; TH1 CELL; TH17 CELL; TH2 CELL;

ANIMALS; ANTIGENS, CD4; BRONCHIAL HYPERREACTIVITY; CD4-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; CELL POLARITY; CELL PROLIFERATION; EPITOPES; FORKHEAD TRANSCRIPTION FACTORS; INTERLEUKIN-17; INTERLEUKIN-2 RECEPTOR ALPHA SUBUNIT; INTERLEUKIN-4; MICE; MICE, INBRED BALB C; OVALBUMIN; PNEUMONIA; T-LYMPHOCYTES, REGULATORY; TH1 CELLS; TH2 CELLS;

MUS;

EID: 77957154678     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0110044     Document Type: Article

References (51)

1. Holgate, S. T. (2008) The airway epithelium is central to the pathogenesis of asthma. Allergol. Int. 57, 1-10.
2. Zhu, J., Paul, W. E. (2008) CD4 T cells: fates, functions, and faults. Blood 112, 1557-1569.
3. Song, C., Luo, L., Lei, Z., Li, B., Liang, Z., Liu, G., Li, D., Zhang, G., Huang, B., Feng, Z. H. (2008) IL-17-producing alveolar macrophages mediate allergic lung inflammation related to asthma. J. Immunol. 181, 6117-6124.
4. Chakir, J., Shannon, J., Molet, S., Fukakusa, M., Elias, J., Laviolette, M., Boulet, L. P., Hamid, Q. (2003) Airway remodeling-associated mediators in moderate to severe asthma: effect of steroids on TGF-β, IL-11, IL-17, and type I and type III collagen expression. J. Allergy Clin. Immunol. 111, 1293-1298.
5. McKinley, L., Alcorn, J. F., Peterson, A., Dupont, R. B., Kapadia, S., Logar, A., Henry, A., Irvin, C. G., Piganelli, J. D., Ray, A., Kolls, J. K. (2008) TH17 cells mediate steroid-resistant airway inflammation and airway hyperresponsiveness in mice. J. Immunol. 181, 4089-4097.
6. Groux, H., Powrie, F. (1999) Regulatory T cells and inflammatory bowel disease. Immunol. Today 20, 442-445.
7. Akbari, O., Freeman, G. J., Meyer, E. H., Greenfield, E. A., Chang, T. T., Sharpe, A. H., Berry, G., DeKruyff, R. H., Umetsu, D. T. (2002) Antigen-specific regulatory T cells develop via the ICOS-ICOS-ligand pathway and inhibit allergen-induced airway hyperreactivity. Nat. Med. 8, 1024-1032.
8. Shevach, E. M., DiPaolo, R. A., Andersson, J., Zhao, D. M., Stephens, G. L., Thornton, A. M. (2006) The lifestyle of naturally occurring CD4+ CD25+ Foxp3+ regulatory T cells. Immunol. Rev. 212, 60-73.
9. Sakaguchi, S. (2005) Naturally arising Foxp3-expressing CD25+CD4+ regulatory T cells in immunological tolerance to self and non-self. Nat. Immunol. 6, 345-352.
10. Sakaguchi, S., Sakaguchi, N., Asano, M., Itoh, M., Toda, M. (1995) Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor α-chains (CD25). Breakdown of a single mechanism of self-tolerance causes various autoimmune diseases. J. Immunol. 155, 1151-1164.
11. Horwitz, D. A., Zheng, S. G., Gray, J. D. (2008) Natural and TGF-β-induced Foxp3(+)CD4(+) CD25(+) regulatory T cells are not mirror images of each other. Trends Immunol. 29, 429-435.
12. Brunkow, M. E., Jeffery, E. W., Hjerrild, K. A., Paeper, B., Clark, L. B., Yasayko, S. A., Wilkinson, J. E., Galas, D., Ziegler, S. F., Ramsdell, F. (2001) Disruption of a new forkhead/winged-helix protein, scurfin, results in the fatal lymphoproliferative disorder of the scurfy mouse. Nat. Genet. 27, 68-73.
13. Hori, S., Nomura, T., Sakaguchi, S. (2003) Control of regulatory T cell development by the transcription factor Foxp3. Science 299, 1057-1061.
14. Itoh, M., Takahashi, T., Sakaguchi, N., Kuniyasu, Y., Shimizu, J., Otsuka, F., Sakaguchi, S. (1999) Thymus and autoimmunity: production of CD25+CD4+ naturally anergic and suppressive T cells as a key function of the thymus in maintaining immunologic self-tolerance. J. Immunol. 162, 5317-5326.
15. Asano, M., Toda, M., Sakaguchi, N., Sakaguchi, S. (1996) Autoimmune disease as a consequence of developmental abnormality of a T cell subpopulation. J. Exp. Med. 184, 387-396.
16. Hadeiba, H., Locksley, R. M. (2003) Lung CD25 CD4 regulatory T cells suppress type 2 immune responses but not bronchial hyperreactivity. J. Immunol. 170, 5502-5510.
17. Jaffar, Z., Sivakuru, T., Roberts, K. (2004) CD4+CD25+ T cells regulate airway eosinophilic inflammation by modulating the Th2 cell phenotype. J. Immunol. 172, 3842-3849.
18. Bluestone, J. A., Abbas, A. K. (2003) Natural versus adaptive regulatory T cells. Nat. Rev. Immunol. 3, 253-257.
19. Dardalhon, V., Awasthi, A., Kwon, H., Galileos, G., Gao, W., Sobel, R. A., Mitsdoerffer, M., Strom, T. B., Elyaman, W., Ho, I. C., Khoury, S., Oukka, M., Kuchroo, V. K. (2008) IL-4 inhibits TGF-β-induced Foxp3+ T cells and, together with TGF-β, generates IL-9+ IL-10+ Foxp3(-) effector T cells. Nat. Immunol. 9, 1347-1355.
20. Shevach, E. M. (2009) Mechanisms of Foxp3+ T regulatory cell-mediated suppression. Immunity 30, 636-645.
21. Asseman, C., Mauze, S., Leach, M. W., Coffman, R. L., Powrie, F. (1999) An essential role for interleukin 10 in the function of regulatory T cells that inhibit intestinal inflammation. J. Exp. Med. 190, 995-1004.
22. Powrie, F., Carlino, J., Leach, M. W., Mauze, S., Coffman, R. L. (1996) A critical role for transforming growth factor-β but not interleukin 4 in the suppression of T helper type 1-mediated colitis by CD45RB(low) CD4+ T cells. J. Exp. Med. 183, 2669-2674.
23. Allan, S. E., Broady, R., Gregori, S., Himmel, M. E., Locke, N., Roncarolo, M. G., Bacchetta, R., Levings, M. K. (2008) CD4+ T-regulatory cells: toward therapy for human diseases. Immunol. Rev. 223, 391-421. (Pubitemid 351986179)
24. Jiang, S., Tsang, J., Game, D. S., Stevenson, S., Lombardi, G., Lechler, R. I. (2006) Generation and expansion of human CD4+ CD25+ regulatory T cells with indirect allospecificity: potential reagents to promote donor-specific transplantation tolerance. Transplantation 82, 1738-1743. (Pubitemid 46035661)
25. Tang, Q., Henriksen, K. J., Bi, M., Finger, E. B., Szot, G., Ye, J., Masteller, E. L., McDevitt, H., Bonyhadi, M., Bluestone, J. A. (2004) In vitro-expanded antigen-specific regulatory T cells suppress autoimmune diabetes. J. Exp. Med. 199, 1455-1465. (Pubitemid 38780401)
26. Lee, S. C., Jaffar, Z. H., Wan, K. S., Holgate, S. T., Roberts, K. (1999) Regulation of pulmonary T cell responses to inhaled antigen: role in Th1- and Th2-mediated inflammation. J. Immunol. 162, 6867-6879.
27. Lee, W. T., Cole-Calkins, J., Street, N. E. (1996) Memory T cell development in the absence of specific antigen priming. J. Immunol. 157, 5300-5307. (Pubitemid 126448947)
28. Piccirillo, C. A., Letterio, J. J., Thornton, A. M., McHugh, R. S., Mamura, M., Mizuhara, H., Shevach, E. M. (2002) CD4(+)CD25(+) regulatory T cells can mediate suppressor function in the absence of transforming growth factor β1 production and responsiveness. J. Exp. Med. 196, 237-246. (Pubitemid 34787513)
29. Jaffar, Z., Ferrini, M. E., Buford, M. C., Fitzgerald, G. A., Roberts, K. (2007) Prostaglandin I2-IP signaling blocks allergic pulmonary inflammation by preventing recruitment of CD4+ Th2 cells into the airways in a mouse model of asthma. J. Immunol. 179, 6193-6203.
30. Mohrs, M., Shinkai, K., Mohrs, K., Locksley, R. M. (2001) Analysis of type 2 immunity in vivo with a bicistronic IL-4 reporter. Immunity 15, 303-311.
31. Shimizu, J., Yamazaki, S., Takahashi, T., Ishida, Y., Sakaguchi, S. (2002) Stimulation of CD25(+)CD4(+) regulatory T cells through GITR breaks immunological self-tolerance. Nat. Immunol. 3, 135-142. (Pubitemid 34141443)
32. Wills-Karp, M. (1999) Immunologic basis of antigen-induced airway hyperresponsiveness. Annu. Rev. Immunol. 17, 255-281.
33. Zhao, Y., Yang, J., Gao, Y. D., Guo, W. (2009) Th17 immunity in patients with allergic asthma. Int. Arch. Allergy Immunol. 151, 297-307.
34. Wong, C. K., Lun, S. W., Ko, F. W., Wong, P. T., Hu, S. Q., Chan, I. H., Hui, D. S., Lam, C. W. (2009) Activation of peripheral Th17 lymphocytes in patients with asthma. Immunol. Invest. 38, 652-664.
35. Pichavant, M., Goya, S., Meyer, E. H., Johnston, R. A., Kim, H. Y., Matangkasombut, P., Zhu, M., Iwakura, Y., Savage, P. B., DeKruyff, R. H., Shore, S. A., Umetsu, D. T. (2008) Ozone exposure in a mouse model induces airway hyperreactivity that requires the presence of natural killer T cells and IL-17. J. Exp. Med. 205, 385-393.
36. Ferretti, S., Bonneau, O., Dubois, G. R., Jones, C. E., Trifilieff, A. (2003) IL-17, produced by lymphocytes and neutrophils, is necessary for lipopolysaccharide- induced airway neutrophilia: IL-15 as a possible trigger. J. Immunol. 170, 2106-2112. (Pubitemid 36197433)
37. Mottet, C., Uhlig, H. H., Powrie, F. (2003) Cutting edge: cure of colitis by CD4+CD25+ regulatory T cells. J. Immunol. 170, 3939-3943.
38. Maloy, K. J., Powrie, F. (2001) Regulatory T cells in the control of immune pathology. Nat. Immunol. 2, 816-822.
39. Uhlig, H. H., Coombes, J., Mottet, C., Izcue, A., Thompson, C., Fanger, A., Tannapfel, A., Fontenot, J. D., Ramsdell, F., Powrie, F. (2006) Characterization of Foxp3+CD4+CD25+ and IL-10-secreting CD4+CD25+ T cells during cure of colitis. J. Immunol. 177, 5852-5860.
40. Bopp, T., Dehzad, N., Reuter, S., Klein, M., Ullrich, N., Stassen, M., Schild, H., Buhl, R., Schmitt, E., Taube, C. (2009) Inhibition of cAMP degradation improves regulatory T cell-mediated suppression. J. Immunol. 182, 4017-4024.
41. Bettelli, E., Carrier, Y., Gao, W., Korn, T., Strom, T. B., Oukka, M., Weiner, H. L., Kuchroo, V. K. (2006) Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 441, 235-238.
42. Ahern, P. P., Izcue, A., Maloy, K. J., Powrie, F. (2008) The interleukin-23 axis in intestinal inflammation. Immunol. Rev. 226, 147-159.
43. Brand, S. (2009) Crohn's disease: Th1, Th17 or both? The change of a paradigm: new immunological and genetic insights implicate Th17 cells in the pathogenesis of Crohn's disease. Gut 58, 1152-1167.
44. Fujino, S., Andoh, A., Bamba, S., Ogawa, A., Hata, K., Araki, Y., Bamba, T., Fujiyama, Y. (2003) Increased expression of interleukin 17 in inflammatory bowel disease. Gut 52, 65-70. (Pubitemid 36020767)
45. Zhu, J., Paul, W. E. (2010) Heterogeneity and plasticity of T helper cells. Cell Res. 20, 4-12.
46. Mangan, P. R., Harrington, L. E., O'Quinn, D. B., Helms, W. S., Bullard, D. C., Elson, C. O., Hatton, R. D., Wahl, S. M., Schoeb, T. R., Weaver, C. T. (2006) Transforming growth factor-β induces development of the T(H)17 lineage. Nature 441, 231-234.
47. Korn, T., Bettelli, E., Gao, W., Awasthi, A., Jager, A., Strom, T. B., Oukka, M., Kuchroo, V. K. (2007) IL-21 initiates an alternative pathway to induce proinflammatory T(H)17 cells. Nature 448, 484-487. (Pubitemid 47123515)
48. Zhou, L., Ivanov, I. I., Spolski, R., Min, R., Shenderov, K., Egawa, T., Levy, D. E., Leonard, W. J., Littman, D. R. (2007) IL-6 programs T(H)-17 cell differentiation by promoting sequential engagement of the IL-21 and IL-23 pathways. Nat. Immunol. 8, 967-974. (Pubitemid 47300011)
49. Sakaguchi, S., Yamaguchi, T., Nomura, T., Ono, M. (2008) Regulatory T cells and immune tolerance. Cell 133, 775-787.
50. Elias, K. M., Laurence, A., Davidson, T. S., Stephens, G., Kanno, Y., Shevach, E. M., O'Shea, J. J. (2008) Retinoic acid inhibits Th17 polarization and enhances FoxP3 expression through a Stat-3/Stat-5 independent signaling pathway. Blood 111, 1013-1020. (Pubitemid 351213378)
51. Mucida, D., Park, Y., Kim, G., Turovskaya, O., Scott, I., Kronenberg, M., Cheroutre, H. (2007) Reciprocal TH17 and regulatory T cell differentiation mediated by retinoic acid. Science 317, 256-260. (Pubitemid 47076203)