IL-1 receptor signaling is required at multiple stages of sensitization and elicitation of the contact hypersensitivity response

Journal of Immunology

Volumn 188, Issue 4, 2012, Pages 1761-1771

  Kish, Danielle D ^a   Gorbachev, Anton V ^a   Fairchild, Robert L ^a,b  

^a LERNER RESEARCH INSTITUTE   (United States)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; HAPTEN; INTERLEUKIN 1 RECEPTOR; INTERLEUKIN 17; MESSENGER RNA; SECONDARY LYMPHOID TISSUE CHEMOKINE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CD8+ T LYMPHOCYTE; CELL INFILTRATION; CELL MIGRATION; CELLULAR IMMUNITY; CONTACT ALLERGY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION; INNATE IMMUNITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION;

ADOPTIVE TRANSFER; ANIMALS; ANTIGEN PRESENTATION; CD8-POSITIVE T-LYMPHOCYTES; CELL MOVEMENT; DENDRITIC CELLS; DERMATITIS, CONTACT; DINITROFLUOROBENZENE; HAPTENS; IMMUNIZATION; INTERFERON-GAMMA; INTERLEUKIN-17; LYMPH NODES; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RECEPTORS, INTERLEUKIN-1; SIGNAL TRANSDUCTION;

EID: 84856939971     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1100928     Document Type: Article

References (45)

1. Engeman, T. M., A. V. Gorbachev, R. P. Gladue, P. S. Heeger, and R. L. Fairchild. 2000. Inhibition of functional T cell priming and contact hypersensitivity responses by treatment with anti-secondary lymphoid chemokine antibody during hapten sensitization. J. Immunol. 164: 5207-5214. (Pubitemid 30305197)
2. Förster, R., A. Schubel, D. Breitfeld, E. Kremmer, I. Renner-Müller, E. Wolf, and M. Lipp. 1999. CCR7 coordinates the primary immune response by establishing functional microenvironments in secondary lymphoid organs. Cell 99: 23-33. (Pubitemid 29468627)
3. Macatonia, S. E., S. C. Knight, A. J. Edwards, S. Griffiths, and P. Fryer. 1987. Localization of antigen on lymph node dendritic cells after exposure to the contact sensitizer fluorescein isothiocyanate. Functional and morphological studies. J. Exp. Med. 166: 1654-1667. (Pubitemid 18000346)
4. Saeki, H., A. M. Moore, M. J. Brown, and S. T. Hwang. 1999. Cutting edge: secondary lymphoid-tissue chemokine (SLC) and CC chemokine receptor 7 (CCR7) participate in the emigration pathway of mature dendritic cells from the skin to regional lymph nodes. J. Immunol. 162: 2472-2475. (Pubitemid 29309263)
5. Robbiani, D. F., R. A. Finch, D. Jäger, W. A. Muller, A. C. Sartorelli, and G. J. Randolph. 2000. The leukotriene C(4) transporter MRP1 regulates CCL19 (MIP-3β, ELC)-dependent mobilization of dendritic cells to lymph nodes. Cell 103: 757-768.
6. Campbell, J. J., G. Haraldsen, J. Pan, J. Rottman, S. Qin, P. Ponath, D. P. Andrew, R. Warnke, N. Ruffing, N. Kassam, et al. 1999. The chemokine receptor CCR4 in vascular recognition by cutaneous but not intestinal memory T cells. Nature 400: 776-780. (Pubitemid 29399540)
7. Dudda, J. C., A. Lembo, E. Bachtanian, J. Huehn, C. Siewert, A. Hamann, E. Kremmer, R. Förster, and S. F. Martin. 2005. Dendritic cells govern induction and reprogramming of polarized tissue-selective homing receptor patterns of T cells: important roles for soluble factors and tissue microenvironments. Eur. J. Immunol. 35: 1056-1065. (Pubitemid 40542212)
8. + T cell trafficking to inflamed skin: role for tissue microenvironment and dendritic cells in establishment of T cell-homing subsets. J. Immunol. 172: 857-863.
9. Mora, J. R., G. Cheng, D. Picarella, M. Briskin, N. Buchanan, and U. H. von Andrian. 2005. Reciprocal and dynamic control of CD8 T cell homing by dendritic cells from skin- and gut-associated lymphoid tissues. J. Exp. Med. 201: 303-316. (Pubitemid 40189439)
10. + T cells, respectively, mediate and regulate contact sensitivity to dinitrofluorobenzene. Eur. J. Immunol. 25: 3006-3010.
11. + T cells in murine contact sensitivity revealed by in vivo monoclonal antibody depletion. J. Immunol. 144: 4121-4128.
12. Kalish, R. S., and K. L. Johnson. 1990. Enrichment and function of urushiol (poison ivy)-specific T lymphocytes in lesions of allergic contact dermatitis to urushiol. J. Immunol. 145: 3706-3713.
13. Xu, H., N. A. DiIulio, and R. L. Fairchild. 1996. T cell populations primed by hapten sensitization in contact sensitivity are distinguished by polarized patterns of cytokine production: interferon γ-producing (Tc1) effector CD8+ T cells and interleukin (Il) 4/Il-10-producing (Th2) negative regulatory CD4+ T cells. J. Exp. Med. 183: 1001-1012.
14. + IL-17- producing T cells are important in effector functions for the elicitation of contact hypersensitivity responses. J. Immunol. 177: 6852-6858.
15. He, D., L. Wu, H. K. Kim, H. Li, C. A. Elmets, and H. Xu. 2009. IL-17 and IFN-γ mediate the elicitation of contact hypersensitivity responses by different mechanisms and both are required for optimal responses. J. Immunol. 183: 1463-1470.
16. Kish, D. D., X. Li, and R. L. Fairchild. 2009. CD8 T cells producing IL-17 and IFN-γ initiate the innate immune response required for responses to antigen skin challenge. J. Immunol. 182: 5949-5959.
17. Kish, D. D., N. Volokh, W. M. Baldwin, III, and R. L. Fairchild. 2011. Hapten application to the skin induces an inflammatory program directing haptenprimed effector CD8 T cell interaction with hapten-presenting endothelial cells. J. Immunol. 186: 2117-2126.
18. Dilulio, N. A., T. M. Engeman, D. Armstrong, C. Tannenbaum, T. A. Hamilton, and R. L. Fairchild. 1999. Groalpha-mediated recruitment of neutrophils is required for elicitation of contact hypersensitivity. Eur. J. Immunol. 29: 3485-3495. (Pubitemid 29527796)
19. Engeman, T. M., A. V. Gorbachev, D. D. Kish, and R. L. Fairchild. 2004. The intensity of neutrophil infiltration controls the number of antigen-primed CD8 T cells recruited into cutaneous antigen challenge sites. J. Leukoc. Biol. 76: 941-949.
20. Enk, A. H., V. L. Angeloni, M. C. Udey, and S. I. Katz. 1993. An essential role for Langerhans cell-derived IL-1 β in the initiation of primary immune responses in skin. J. Immunol. 150: 3698-3704. (Pubitemid 23129751)
21. Enk, A. H., and S. I. Katz. 1992. Early molecular events in the induction phase of contact sensitivity. Proc. Natl. Acad. Sci. USA 89: 1398-1402.
22. Kermani, F., M. S. Flint, and S. A. M. Hotchkiss. 2000. Induction and localization of cutaneous interleukin-1 β mRNA during contact sensitization. Toxicol. Appl. Pharmacol. 169: 231-237. (Pubitemid 32048500)
23. Kupper, T. S., and R. W. Groves. 1995. The interleukin-1 axis and cutaneous inflammation. J. Invest. Dermatol. 105(1, Suppl)62S-66S.
24. Nakae, S., C. Naruse-Nakajima, K. Sudo, R. Horai, M. Asano, and Y. Iwakura. 2001. IL-1 α, but not IL-1 β, is required for contact-allergen-specific T cell activation during the sensitization phase in contact hypersensitivity. Int. Immunol. 13: 1471-1478. (Pubitemid 33133876)
25. Shornick, L. P., P. De Togni, S. Mariathasan, J. Goellner, J. Strauss-Schoenberger, R. W. Karr, T. A. Ferguson, and D. D. Chaplin. 1996. Mice deficient in IL-1β manifest impaired contact hypersensitivity to trinitrochlorobenzone. J. Exp. Med. 183: 1427-1436. (Pubitemid 26134286)
26. Kondo, S., S. Pastore, H. Fujisawa, G. M. Shivji, R. C. McKenzie, C. A. Dinarello, and D. N. Sauder. 1995. Interleukin-1 receptor antagonist suppresses contact hypersensitivity. J. Invest. Dermatol. 105: 334-338.
27. Cumberbatch, M., R. J. Dearman, R. W. Groves, C. Antonopoulos, and I. Kimber. 2002. Differential regulation of epidermal langerhans cell migration by interleukins (IL)-1α and IL-1β during irritant- and allergen-induced cutaneous immune responses. Toxicol. Appl. Pharmacol. 182: 126-135. (Pubitemid 34971717)
28. Antonopoulos, C., M. Cumberbatch, R. J. Dearman, R. J. Daniel, I. Kimber, and R. W. Groves. 2001. Functional caspase-1 is required for Langerhans cell migration and optimal contact sensitization in mice. J. Immunol. 166: 3672-3677. (Pubitemid 32224888)
29. Antonopoulos, C., M. Cumberbatch, J. B. Mee, R. J. Dearman, X.-Q. Wei, F. Y. Liew, I. Kimber, and R. W. Groves. 2008. IL-18 is a key proximal mediator of contact hypersensitivity and allergen-induced Langerhans cell migration in murine epidermis. J. Leukoc. Biol. 83: 361-367. (Pubitemid 351225617)
30. Klekotka, P. A., L. Yang, and W. M. Yokoyama. 2010. Contrasting roles of the IL-1 and IL-18 receptors in MyD88-dependent contact hypersensitivity. J. Invest. Dermatol. 130: 184-191.
31. Sutterwala, F. S., Y. Ogura, M. Szczepanik, M. Lara-Tejero, G. S. Lichtenberger, E. P. Grant, J. Bertin, A. J. Coyle, J. E. Galán, P. W. Askenase, and R. A. Flavell. 2006. Critical role for NALP3/CIAS1/Cryopyrin in innate and adaptive immunity through its regulation of caspase-1. Immunity 24: 317-327.
32. Watanabe, H., O. Gaide, V. Pétrilli, F. Martinon, E. Contassot, S. Roques, J. A. Kummer, J. Tschopp, and L. E. French. 2007. Activation of the IL-1β-processing inflammasome is involved in contact hypersensitivity. J. Invest. Dermatol. 127: 1956-1963. (Pubitemid 47075373)
33. Watanabe, H., S. Gehrke, E. Contassot, S. Roques, J. Tschopp, P. S. Friedmann, L. E. French, and O. Gaide. 2008. Danger signaling through the inflammasome acts as a master switch between tolerance and sensitization. J. Immunol. 180: 5826-5832.
34. Labow, M., D. Shuster, M. Zetterstrom, P. Nunes, R. Terry, E. B. Cullinan, T. Bartfai, C. Solorzano, L. L. Moldawer, R. Chizzonite, and K. W. McIntyre. 1997. Absence of IL-1 signaling and reduced inflammatory response in IL-1 type I receptor-deficient mice. J. Immunol. 159: 2452-2461. (Pubitemid 127681040)
35. 7) results in resistance to contact hypersensitivity. J. Exp. Med. 207: 2609-2619.
36. + T cell-mediated cutaneous immune responses by restricting effector T cell development through a Fas ligand-dependent mechanism. J. Immunol. 172: 2286-2295.
37. + regulatory T cells utilize FasL as a mechanism to restrict DC priming functions in cutaneous immune responses. Eur. J. Immunol. 40: 2006-2015.
38. Chung, Y., S. H. Chang, G. J. Martinez, X. O. Yang, R. Nurieva, H. S. Kang, L. Ma, S. S. Watowich, A. M. Jetten, Q. Tian, and C. Dong. 2009. Critical regulation of early Th17 cell differentiation by interleukin-1 signaling. Immunity 30: 576-587.
39. Akira, S., S. Uematsu, and O. Takeuchi. 2006. Pathogen recognition and innate immunity. Cell 124: 783-801. (Pubitemid 43261452)
40. Randolph, G. J., J. Ochando, and S. Partida-Sánchez. 2008. Migration of dendritic cell subsets and their precursors. Annu. Rev. Immunol. 26: 293-316. (Pubitemid 351600378)
41. Pior, J., T. Vogl, C. Sorg, and E. MacHer. 1999. Free hapten molecules are dispersed by way of the bloodstream during contact sensitization to fluorescein isothiocyanate. J. Invest. Dermatol. 113: 888-893. (Pubitemid 30013327)
42. Rao, D. A., R. E. Eid, L. Qin, T. Yi, N. C. Kirkiles-Smith, G. Tellides, and J. S. Pober. 2008. Interleukin (IL)-1 promotes allogeneic T cell intimal infiltration and IL-17 production in a model of human artery rejection. J. Exp. Med. 205: 3145-3158.
43. Viguier, M., P. Guigue, C. Pagès, A. Smahi, and H. Bachelez. 2010. Successful treatment of generalized pustular psoriasis with the interleukin-1-receptor antagonist Anakinra: lack of correlation with IL1RN mutations. Ann. Intern. Med. 153: 66-67.
44. Jung, N., M. Hellmann, R. Hoheisel, C. Lehmann, I. Haase, A. Perniok, M. Hallek, and A. Rubbert. 2010. An open-label pilot study of the efficacy and safety of anakinra in patients with psoriatic arthritis refractory to or intolerant of methotrexate (MTX). Clin. Rheumatol. 29: 1169-1173.
45. Larsen, C. M., M. Faulenbach, A. Vaag, A. Vølund, J. A. Ehses, B. Seifert, T. Mandrip-Poulsn, and M. Y. Donath. 2007. Interleukin-1-receptor antagonist in type 2 diabetes mellitus. N. Engl. J. Med. 356: 1517-1526. (Pubitemid 46588416)