IL-21R is essential for epicutaneous sensitization and allergic skin inflammation in humans and mice

Journal of Clinical Investigation

Volumn 119, Issue 1, 2009, Pages 47-60

  Jin, Haoli ^a   Oyoshi, Michiko K ^a   Le, Yi ^a   Bianchi, Teresa ^b   Koduru, Suresh ^a   Mathias, Clinton B ^a   Kumar, Lalit ^a   Le Bras, Séverine ^a   Young, Deborah ^c   Collins, Mary ^c   Grusby, Michael J ^d   Wenzel, Joerg ^e   Bieber, Thomas ^e   Boes, Marianne ^b   Silberstein, Leslie E ^a   Oettgen, Hans C ^a   Geha, Raif S ^a  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c PFIZER INC   (United States)

^d HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^e UNIVERSITY OF BONN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; CHEMOKINE RECEPTOR CCR7; GELATINASE A; HYBRID PROTEIN; IMMUNOGLOBULIN G2A; INTERLEUKIN 21; INTERLEUKIN 21 RECEPTOR; INTERLEUKIN DERIVATIVE; OVALBUMIN;

ADOPTIVE TRANSFER; ALLERGIC REACTION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; EPIDERMIS CELL; HUMAN; HUMAN TISSUE; LYMPH NODE; MOUSE; MOUSE STRAIN; NONHUMAN; PRIORITY JOURNAL; SCRATCHING; SKIN ALLERGY; SKIN CELL; SKIN DEFECT; SKIN INFLAMMATION; SKIN SENSITIZATION; UPREGULATION; WILD TYPE; ANIMAL; ATOPIC DERMATITIS; BAGG ALBINO MOUSE; CELL CULTURE; CHEMICALLY INDUCED DISORDER; CYTOLOGY; DISEASE MODEL; ENZYME ACTIVATION; FEMALE; GENETICS; IMMUNIZATION; IMMUNOLOGY; INFLAMMATION; METABOLISM; MOUSE MUTANT; PATHOLOGY; SKIN; SPLEEN;

ADOPTIVE TRANSFER; ANIMALS; CELLS, CULTURED; DERMATITIS, ATOPIC; DISEASE MODELS, ANIMAL; ENZYME ACTIVATION; FEMALE; HUMANS; IMMUNIZATION; INFLAMMATION; INTERLEUKINS; MATRIX METALLOPROTEINASE 2; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; OVALBUMIN; RECEPTORS, CCR7; RECEPTORS, INTERLEUKIN-21; RECOMBINANT FUSION PROTEINS; SKIN; SPLEEN;

EID: 61749085092     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI32310     Document Type: Article

References (60)

1. Mehta, D.S., Wurster, A.L., and Grusby, M.J. 2004. Biology of IL-21 and the IL-21 receptor. Immunol. Rev. 202:84-95.
2. Coquet, J.M., et al. 2007. IL-21 Is produced by NKT cells and modulates NKT cell activation and cytokine production. J. Immunol. 178:2827-2834.
3. Spolski, R., and Leonard, W.J. 2008. Interleukin-21: basic biology and implications for cancer and autoimmunity. Annu. Rev. Immunol. 26:57-79.
4. Suto, A., Wurster, A.L., Reiner, S.L., and Grusby, M.J. 2006. IL-21 inhibits IFN-gamma production in developing Th1 cells through the repression of Eomesodermin expression. J. Immunol. 177:3721-3727.
5. Strengell, M., et al. 2003. IL-21 in synergy with IL-15 or IL-18 enhances IFN-gamma production in human NK and T cells. J. Immunol. 170:5464-5469.
6. Zeng, R., et al. 2005. Synergy of IL-21 and IL-15 in regulating CD8+ T cell expansion and function. J. Exp. Med. 201:139-148.
7. Ozaki, K., et al. 2002. A critical role for IL-21 in regulating immunoglobulin production. Science. 298:1630-1634.
8. Pesce, J., et al. 2006. The IL-21 receptor augments Th2 effector function and alternative macrophage activation. J. Clin. Invest. 116:2044-2055.
9. Frohlich, A., et al. 2007. IL-21 receptor signaling is integral to the development of Th2 effector responses in vivo. Blood. 109:2023-2031.
10. Nurieva, R., et al. 2007. Essential autocrine regulation by IL-21 in the generation of inflammatory T cells. Nature. 448:480-483.
11. Korn, T., et al. 2007. IL-21 initiates an alternative pathway to induce proinflammatory T(H)17 cells. Nature. 448:484-487.
12. Zhou, L., et al. 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.
13. Brady, J., Hayakawa, Y., Smyth, M.J., and Nutt, S.L. 2004. IL-21 induces the functional maturation of murine NK cells. J. Immunol. 172:2048-2058.
14. Roda, J.M., et al. 2006. Interleukin-21 enhances NK cell activation in response to antibody-coated targets. J. Immunol. 177:120-129.
15. Takaki, R., et al. 2005. IL-21 enhances tumor rejection through a NKG2D-dependent mechanism. J. Immunol. 175:2167-2173.
16. Ettinger, R., et al. 2007. IL-21 and BAFF/BLyS synergize in stimulating plasma cell differentiation from a unique population of human splenic memory B cells. J. Immunol. 178:2872-2882.
17. Erazo, A., et al. 2007. Unique maturation program of the IgE response in vivo. Immunity. 26:191-203.
18. Laughter, D., Istvan, J.A., Tofte, S.J., and Hanifin, J.M. 2000. The prevalence of atopic dermatitis in Oregon schoolchildren. J. Am. Acad. Dermatol. 43:649-655.
19. Leung, D.Y. 2000. Atopic dermatitis: new insights and opportunities for therapeutic intervention. J. Allergy Clin. Immunol. 105:860-876.
20. Mitchell, E.B., et al. 1982. Basophils in allergeninduced patch test sites in atopic dermatitis. Lancet. 1:127-130.
21. Vickery, B.P. 2007. Skin barrier function in atopic dermatitis. Curr. Opin. Pediatr. 19:89-93.
22. Palmer, C.N., et al. 2006. Common loss-of-function variants of the epidermal barrier protein filaggrin are a major predisposing factor for atopic dermatitis. Nat. Genet. 38:441-446.
23. Homey, B., Steinhoff, M., Ruzicka, T., and Leung, D.Y. 2006. Cytokines and chemokines orchestrate atopic skin inflammation. J. Allergy Clin. Immunol. 118:178-189.
24. Spergel, J.M., et al. 1998. Epicutaneous sensitization with protein antigen induces localized allergic dermatitis and hyperresponsiveness to methacholine after single exposure to aerosolized antigen in mice. J. Clin. Invest. 101:1614-1622.
25. Spergel, J.M., Mizoguchi, E., Oettgen, H., Bhan, A.K., and Geha, R. 1999. Roles of T(H)1 and T(H)2 cytokines in a murine model of allergic dermatitis. J. Clin. Invest. 103:1103-1111.
26. Ma, W., et al. 2002. CCR3 is essential for skin eosinophilia and airway hyperresponsiveness in a murine model of allergic skin inflammation. J. Clin. Invest. 109:621-628.
27. Ohl, L., et al. 2004. CCR7 governs skin dendritic cell migration under inflammatory and steadystate conditions. Immunity. 21:279-288.
28. Robert, C., and Kupper, T.S. 1999. Inflammatory skin diseases, T cells, and immune surveillance. N. Engl. J. Med. 341:1817-1828.
29. Waithman, J., et al. 2007. Skin-derived dendritic cells can mediate deletional tolerance of class I-restricted self-reactive T cells. J. Immunol. 179:4535-4541.
30. Merad, M., et al. 2002. Langerhans cells renew in the skin throughout life under steady-state conditions. Nat. Immunol. 3:1135-1141.
31. Marsland, B.J., et al. 2005. CCL19 and CCL21 induce a potent proinflammatory differentiation program in licensed dendritic cells. Immunity. 22:493-505.
32. Kobayashi, Y., Matsumoto, M., Kotani, M., and Makino, T. 1999. Possible involvement of matrix metalloproteinase-9 in Langerhans cell migration and maturation. J. Immunol. 163:5989-5993.
33. Ratzinger, G., et al. 2002. Matrix metalloproteinases 9 and 2 are necessary for the migration of Langerhans cells and dermal dendritic cells from human and murine skin. J. Immunol. 168:4361-4371.
34. Sawicki, G., Marcoux, Y., Sarkhosh, K., Tredget, E.E., and Ghahary, A. 2005. Interaction of keratinocytes and fibroblasts modulates the expression of matrix metalloproteinases-2 and -9 and their inhibitors. Mol. Cell. Biochem. 269:209-216.
35. Monteleone, G., et al. 2006. Control of matrix metalloproteinase production in human intestinal fibroblasts by interleukin 21. Gut. 55:1774-1780.
36. Herber, D., et al. 2007. IL-21 has a pathogenic role in a lupus-prone mouse model and its blockade with IL-21R.Fc reduces disease progression. J. Immunol. 178:3822-3830.
37. Distler, J.H., et al. 2005. Expression of interleukin-21 receptor in epidermis from patients with systemic sclerosis. Arthritis Rheum. 52:856-864.
38. Parrish-Novak, J., et al. 2000. Interleukin 21 and its receptor are involved in NK cell expansion and regulation of lymphocyte function. Nature. 408:57-63.
39. Brandt, K., Bulfone-Paus, S., Foster, D.C., and Ruckert, R. 2003. Interleukin-21 inhibits dendritic cell activation and maturation. Blood. 102:4090-4098.
40. He, R., Oyoshi, M.K., Jin, H., and Geha, R.S. 2007. Epicutaneous antigen exposure induces a Th17 response that drives airway inflammation after inhalation challenge. Proc. Natl. Acad. Sci. U. S. A. 104:15817-15822.
41. Imai, T., et al. 1999. Selective recruitment of CCR4-bearing Th2 cells toward antigen-presenting cells by the CC chemokines thymus and activation-regulated chemokine and macrophage-derived chemokine. Int. Immunol. 11:81-88.
42. Liddiard, K., et al. 2006. Interleukin-4 induction of the CC chemokine TARC (CCL17) in murine macrophages is mediated by multiple STAT6 sites in the TARC gene promoter. BMC Mol. Biol. 7:45.
43. Nomura, T., et al. 2002. Interleukin-13 induces thymus and activation-regulated chemokine (CCL17) in human peripheral blood mononuclear cells. Cytokine. 20:49-55.
44. Fantini, M.C., et al. 2007. IL-21 regulates experimental colitis by modulating the balance between Treg and Th17 cells. Eur. J. Immunol. 37:3155-3163.
45. Anderson, A.O., and Shaw, S. 2005. Conduit for privileged communications in the lymph node. Immunity. 22:3-5.
46. Brandt, K., et al. 2003. Interleukin-21 inhibits dendritic cell-mediated T cell activation and induction of contact hypersensitivity in vivo. J. Invest. Dermatol. 121:1379-1382.
47. Wurster, A.L., et al. 2002. Interleukin 21 is a T helper (Th) cell 2 cytokine that specifically inhibits the differentiation of naive Th cells into interferon gamma-producing Th1 cells. J. Exp. Med. 196:969-977.
48. Zeng, R., Spolski, R., Casas, E., Zhu, W., Levy, D.E., and Leonard, W.J. 2007. The molecular basis of IL-21-mediated proliferation. Blood. 109:4135-4142.
49. van Leeuwen, E.M., et al. 2005. Functional reexpression of CCR7 on CMV-specific CD8+ T cells upon antigenic stimulation. Int. Immunol. 17:713-719.
50. Leung, D.Y., Boguniewicz, M., Howell, M.D., Nomura, I., and Hamid, Q.A. 2004. New insights into atopic dermatitis. J. Clin. Invest. 113:651-657.
51. Wenzel, J., et al. 2005. Enhanced type I interferon signalling promotes Th1-biased inflammation in cutaneous lupus erythematosus. J. Pathol. 205:435-442.
52. Kasaian, M.T., et al. 2002. IL-21 limits NK cell responses and promotes antigen-specific T cell activation: a mediator of the transition from innate to adaptive immunity. Immunity. 16:559-569.
53. Ozaki, K., et al. 2004. Regulation of B cell differentiation and plasma cell generation by IL-21, a novel inducer of Blimp-1 and Bcl-6. J. Immunol. 173:5361-5371.
54. Kettner, A., et al. 2004. WIP regulates signaling via the high affinity receptor for immunoglobulin E in mast cells. J. Exp. Med. 199:357-368.
55. Pfaffl, M.W. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29:e45.
56. Lutz, M.B., et al. 1999. An advanced culture method for generating large quantities of highly pure dendritic cells from mouse bone marrow. J. Immunol. Methods. 223:77-92.
57. Pivniouk, V.I., et al. 1999. SLP-76 deficiency impairs signaling via the high-affinity IgE receptor in mast cells. J. Clin. Invest. 103:1737-1743.
58. Baekkevold, E.S., et al. 2005. A role for CCR4 in development of mature circulating cutaneous T helper memory cell populations. J. Exp. Med. 201:1045-1051.
59. Boes, M., et al. 2002. T-cell engagement of dendritic cells rapidly rearranges MHC class II transport. Nature. 418:983-988.
60. Le, Y., et al. 2007. SOCS3 protein developmentally regulates the chemokine receptor CXCR4-FAK signaling pathway during B lymphopoiesis. Immunity. 27:811-823.