Resolution of airway inflammation and hyperreactivity after in vivo transfer of CD4+CD25+ regulatory T cells is interleukin 10 dependent

Journal of Experimental Medicine

Volumn 202, Issue 11, 2005, Pages 1539-1547

  Kearley, Jennifer ^a   Barker, Jane E ^b   Robinson, Douglas S ^a   Lloyd, Clare M ^a  

^a NATIONAL HEART AND LUNG INSTITUTE   (United Kingdom)

^b ASTRAZENECA   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALLERGEN; CD4 ANTIGEN; INTERLEUKIN 10; INTERLEUKIN 2 RECEPTOR ALPHA; OVALBUMIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; BRONCHITIS; BRONCHUS HYPERREACTIVITY; CONTROLLED STUDY; DENDRITIC CELL; EOSINOPHIL; FEMALE; GENETIC TRANSFECTION; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECIPIENT; RESPIRATORY TRACT DISEASE; SENSITIZATION; T LYMPHOCYTE; TH2 CELL;

ADOPTIVE TRANSFER; ANIMALS; ANTIBODIES, MONOCLONAL; B-LYMPHOCYTES; DENDRITIC CELLS; EOSINOPHILS; HUMANS; INFLAMMATION; INTERLEUKIN-10; LUNG; MACROPHAGES, ALVEOLAR; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; RECEPTORS, INTERLEUKIN; RECEPTORS, INTERLEUKIN-10; RESPIRATORY HYPERSENSITIVITY; T-LYMPHOCYTES, REGULATORY; TH2 CELLS;

EID: 28544444024     PISSN: 00221007     EISSN: 00221007     Source Type: Journal    
DOI: 10.1084/jem.20051166     Document Type: Article

References (41)

1. Robinson, D.S., Q. Hamid, S. Ying, A. Tsicopoulos, J. Barkans, A.M. Bentley, C. Corrigan, S.R. Durham, and A.B. Kay. 1992. Predominant TH2-like bronchoalveolar T-lymphocyte population in atopic asthma. N. Engl. J. Med. 326:298-304.
2. Gavett, S.H., X. Chen, F. Finkelman, and M. Wills-Karp. 1994. Depletion of murine CD4+ T lymphocytes prevents antigen-induced airway hyperreactivity and pulmonary eosinophilia. Am. J. Respir. Cell Mol. Biol. 10:587-593.
3. Gonzalo, J.A., C.M. Lloyd, L. Kremer, E. Finger, A. Martinez, M.H. Siegelman, M. Cybulsky, and J.C. Gutierrez-Ramos. 1996. Eosinophil recruitment to the lung in a murine model of allergic inflammation. The role of T cells, chemokines, and adhesion receptors. J. Clin. Invest. 98:2332-2345.
4. Mosmann, T.R., and R.L. Coffman. 1989. TH1 and TH2 cells: different patterns of lymphokine secretion lead to different functional properties. Annu. Rev. Immunol. 7:145-173.
5. O'Garra, A., and P. Vieira. 2004. Regulatory T cells and mechanisms of immune system control. Nat. Med. 10:801-805.
6. Asseman, C., S. Mauze, M.W. Leach, R.L. Coffman, and F. Powrie. 1999. An essential role for interleukin 10 in the function of regulatory T cells that inhibit intestinal inflammation. J. Exp. Med. 190:995-1004.
7. + T cells. J. Exp. Med. 183:2669-2674.
8. Akdis, M., J. Verhagen, A. Taylor, F. Karamloo, C. Karagiannidis, R. Crameri, S. Thunberg, G. Deniz, R. Valenta, H. Fiebig, et al. 2004. Immune responses in healthy and allergic individuals are characterized by a fine balance between allergen-specific T regulatory 1 and T helper 2 cells. J. Exp. Med. 199:1567-1575.
9. Ling, E.M., T. Smith, X.D. Nguyen, C. Pridgeon, P.M. Dallman, J. Arbery, V.A. Carr, and D.S. Robinson. 2004. Relation of CD4CD25 regulatory T-cell suppression of allergen-driven T-cell activation to atopic status and expression of allergic disease. Lancet. 363:608-615.
10. Jaffar, Z., T. Sivakuru, and K. Roberts. 2004. CD4+CD25+ T cells regulate airway eosinophilic inflammation by modulating the Th2 cell phenotype. J. Immunol. 172:3842-3849.
11. Hadeiba, H., and R.M. Locksley. 2003. Lung CD25 CD4 regulatory T cells suppress type 2 immune responses but not bronchial hyperreactivity. J. Immunol. 170:5502-5510.
12. Doganci, A., T. Eigenbrod, N. Krug, G.T. De Sanctis, M. Hausding, V.J. Erpenbeck, E.B. Haddad, E. Schmitt, T. Bopp, K.J. Kallen, et al. 2005. The IL-6R alpha chain controls lung CD4+CD25+ Treg development and function during allergic airway inflammation in vivo. J. Clin. Invest. 115:313-325.
13. Bishop, B., and C.M. Lloyd. 2003. CC Chemokine ligand 1 promotes recruitment of eosinophils but not Th2 cells during the development of allergic airways disease. J. Immunol. 170:4810-4817.
14. Lloyd, C.M., and S.M. Rankin. 2003. Chemokines in allergic airway disease. Curr. Opin. Pharmacol. 3:443-448.
15. + T regulatory cells suppress innate immune pathology through cytokine-dependent mechanisms. J. Exp. Med. 197:111-119.
16. + T cells is induced by immunosuppressive drugs and inhibited by T helper type 1 (Th1)- and Th2-inducing cytokines. J. Exp. Med. 195:603-616.
17. Xu, D., H. Liu, M. Komai-Koma, C. Campbell, C. McSharry, J. Alexander, and F.Y. Liew. 2003. CD4+CD25+ regulatory T cells suppress differentiation and functions of Th1 and Th2 cells, Leishmania major infection, and colitis in mice. J. Immunol. 170:394-399.
18. Curotto de Lafaille, M.A., S. Muriglan, M.J. Sunshine, Y. Lei, N. Kutchukhidze, G. Furtado, A.K. Wensky, D. Olivares-Villagomez, and J.J. Lafaille. 2001. Hyper immunoglobulin E response in mice with monoclonal populations of B and T lymphocytes. J. Exp. Med. 194:1349-1360.
19. Wildin, R.S., S. Smyk-Pearson, and A.H. Filipovich. 2002. Clinical and molecular features of the immunodysregulation, polyendocrinopathy, enteropathy, X linked (IPEX) syndrome. J. Med. Genet. 39:537-545.
20. Jeannin, P., S. Lecoanet, Y. Delneste, J.F. Gauchat, and J.Y. Bonnefoy. 1998. IgE versus IgG4 production can be differentially regulated by IL-10. J. Immunol. 160:3555-3561.
21. + immunoregulatory T cells suppress polyclonal T cell activation in vitro by inhibiting interleukin 2 production. J. Exp. Med. 188:287-296.
22. + regulatory T cells can mediate suppressor function in the absence of transforming growth factor-β 1 production and responsiveness. J. Exp. Med. 196:237-246.
23. Suri-Payer, E., and H. Cantor. 2001. Differential cytokine requirements for regulation of autoimmune gastritis and colitis by CD4+ CD25+ T cells. J. Autoimmun. 16:115-123.
24. Oh, J.W., C. Seroogy, E. Meyer, O. Akbari, G. Berry, C. Fathman, R. DeKruyff, and D. Umetsu. 2002. CD4 T-helper cells engineered to produce IL-10 prevent allergen-induced airway hyperreactivity and inflammation. J. Allergy Clin. Immunol. 110:460-468.
25. Asseman, C., S. Read, and F. Powrie. 2003. Colitogenic Th1 cells are present in the antigen-experienced T cell pool in normal mice: control by CD4+ regulatory T cells and IL-10. J. Immunol. 171:971-978.
26. + T helper cells. J. Exp. Med. 196:255-260.
27. Mekala, D.J., R.S. Alli, and T.L. Geiger. 2005. IL-10-dependent infectious tolerance after the treatment of experimental allergic encephalomyelitis with redirected CD4+CD25+ T lymphocytes. Proc. Natl. Acad. Sci. USA. 102:11817-11822.
28. Nguyen, X.D., and D.S. Robinson. 2004. Fluticasone propionate increases CD4+CD25+ T regulatory cell suppression of allergen-stimulated CD4+CD25- T cells by an IL-10-dependent mechanism. J. Allergy Clin. Immunol. 114:296-301.
29. 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.
30. Zuany-Amorim, C., C. Manlius, A. Trifilieff, L.R. Brunet, G. Rook, G. Bowen, G. Pay, and C. Walker. 2002. Long-term protective and antigen-specific effect of heat-killed Mycobacterium vaccae in a murine model of allergic pulmonary inflammation. J. Immunol. 169:1492-1499.
31. Ostroukhova, M., C. Seguin-Devaux, T.B. Oriss, B. Dixon-McCarthy, L. Yang, B.T. Ameredes, T.E. Corcoran, and A. Ray. 2004. Tolerance induced by inhaled antigen involves CD4+ T cells expressing membrane-bound TGF-beta and FOXP3. J. Clin. Invest. 114:28-38.
32. Robinson, D.S., M. Larche, and S.R. Durham. 2004. Tregs and allergic disease. J. Clin. Invest. 114:1389-1397.
33. Blaser, K., and C.A. Akdis. 2004. Interleukin-10, T regulatory cells and specific allergy treatment. Clin. Exp. Allergy. 34:328-331.
34. Briner, T.J., M. Kuo, K.M. Keating, B.L. Rogers, and J.L. Greenstein. 1993. Peripheral T-cell tTolerance induced in naive and primed mice by subcutaneous injection of peptides from the major cat allergen Fel d I. Proc. Natl. Acad. Sci. USA. 90:7608-7612.
35. Oldfield, W.L.G., M. Larche, and A.B. Kay. 2002. Effect of T-cell peptides derived from Fel d 1 on allergic reactions and cytokine production in patients sensitive to cats: a randomised controlled trial. Lancet. 360:47-53.
36. 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.
37. Kuhn, R., J. Lohler, D. Rennick, K. Rajewsky, and W. Muller. 1993. Interleukin-10-deficient mice develop chronic enterocolitis. Cell. 75:263-274.
38. Hamelmann, E., J. Schwarze, K. Takeda, A. Oshiba, G. Larsen, C. Irvin, and E. Gelfand. 1997. Noninvasive measurement of airway responsiveness in allergic mice using barometric plethysmography. Am. J. Respir. Crit. Care Med. 156:766-775.
39. Martin, T.R., N.P. Gerard, S.J. Galli, and J.M. Drazen. 1988. Pulmonary responses to bronchoconstrictor agonists in the mouse. J. Appl. Physiol. 64:2318-2323.
40. McMillan, S.J., J. Kearley, J.D. Campbell, X.W. Zhu, K.Y. Larbi, J.M. Shipley, R.M. Senior, S. Nourshargh, and C.M. Lloyd. 2004. Matrix metalloproteinase-9 deficiency results in enhanced allergen-induced airway inflammation. J. Immunol. 172:2586-2594.
41. Lloyd, C.M., J.A. Gonzalo, T. Nguyen, T. Delaney, J. Tian, H. Oettgen, A.J. Coyle, and J.C. Gutierrez-Ramos. 2001. Resolution of bronchial hyperresponsiveness and pulmonary inflammation is associated with IL-3 and tissue leukocyte apoptosis. J. Immunol. 166:2033-2040.