IL-1β, but not IL-1α, is required for antigen-specific T cell activation and the induction of local inflammation in the delayed-type hypersensitivity responses

International Immunology

Volumn 18, Issue 5, 2006, Pages 701-712

  Nambu, Aya ^a   Nakae, Susumu ^a,b   Iwakura, Yoichiro ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Allergy; Cytokines; Inflammation; Knockout mice

Indexed keywords

INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; BOVINE SERUM ALBUMIN; EPITOPE; GAMMA INTERFERON; INTERLEUKIN 1; METHYLATED ALBUMIN; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN SPECIFICITY; ARTICLE; CD4+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; DELAYED HYPERSENSITIVITY; DENDRITIC CELL; IMMUNE DEFICIENCY; IMMUNE RESPONSE; INFLAMMATION; LYMPH NODE CELL; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; SENSITIZATION; T LYMPHOCYTE ACTIVATION; WILD TYPE; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; FEMALE; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; MALE; MOUSE MUTANT; T LYMPHOCYTE;

ANIMALS; EPITOPES, T-LYMPHOCYTE; FEMALE; HYPERSENSITIVITY, DELAYED; INTERFERON TYPE II; INTERLEUKIN-1; LYMPHOCYTE ACTIVATION; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; SERUM ALBUMIN, BOVINE; T-LYMPHOCYTES; TUMOR NECROSIS FACTOR-ALPHA;

EID: 33646862631     PISSN: 09538178     EISSN: 14602377     Source Type: Journal    
DOI: 10.1093/intimm/dxl007     Document Type: Article

References (61)

1. Kobayashi, K., Kaneda, K. and Kasama, T. 2001. Immunopathogenesis of delayed-type hypersensitivity. Microsc. Res. Tech. 53:241.
2. Black, C. A. 1999. Delayed type hypersensitivity: Current theories with an historic perspective. Dermatol. Online J. 5:7.
3. Grabbe, S. and Schwarz, T. 1998. Immunoregulatory mechanisms involved in elicitation of allergic contact hypersensitivity. Immunol. Today 19:37.
4. Kariyone, A., Tamura, T, Kano, H. et al. 2003. Immunogenicity of peptide-25 of Ag85B in Th1 development: Role of IFN-gamma. Int. Immunol. 15:1183.
5. Molesworth-Kenyon, S. J., Oakes, J. E. and Lausch, R. N. 2005. A novel role for neutrophils as a source of T cell-recruiting chemokines IP-10 and Mig during the DTH response to HSV-1 antigen. J. Leukoc. Biol. 3:3.
6. Bochner, B. S., Luscinskas, F. W., Gimbrone, M. A., Jr et al. 1991. Adhesion of human basophils, eosinophils, and neutrophils to interleukin 1-activated human vascular endothelial cells: Contributions of endothelial cell adhesion molecules. J. Exp. Med. 173:1553.
7. Walsh, G. M., Mermod, J. J., Hartnell, A., Kay, A. B. and Wardlaw, A. J. 1991. Human eosinophil, but not neutrophil, adherence to IL-1-stimulated human umbilical vascular endothelial cells is alpha 4 beta 1 (very late antigen-4) dependent. J. Immunol. 146:3419.
8. Iademarco, M. F, Barks, J. L. and Dean, D. C. 1995. Regulation of vascular cell adhesion molecule-1 expression by IL-4 and TNF-alpha in cultured endothelial cells. J. Clin. Invest. 95:264.
9. Thorlacius, H., Lindbom, L. and Raud, J. 1997. Cytokine-induced leukocyte rolling in mouse cremaster muscle arterioles in P-selectin dependent. Am. J. Physiol. 272:H1725.
10. Ferreri, N. R., Millet, I., Paliwal, V. et al. 1991. Induction of macrophage TNF alpha, IL-1, IL-6, and PGE2 production by DTH-initiating factors. Cell. Immunol. 137:389.
11. Dinarello, C. A. 1996. Biologic basis for interleukin-1 in disease. Blood 87:2095.
12. Dinarello, C.A. 1997. Interleukin-1. Cytokine Growth Factor Rev. 8:253.
13. Song, X., Voronov, E., Dvorkin, T. et al. 2003. Differential effects of IL-1alpha and IL-1beta on tumorigenicity patterns and invasiveness. J. Immunol. 171:6448.
14. Igarashi, K., Mitsuyama, M., Muramori, K., Tsukada, H. and Nomoto, K. 1990. Interleukin-1-induced promotion of T-cell differentiation in mice immunized with killed Listeria monocyto-genes. Infect. lmmun. 58:3973.
15. Shibuya, K., Robinson, D., Zonin, F. et al. 1998. IL-1 alpha and TNF-alpha are required for IL-12-induced development of Th1 cells producing high levels of IFN-gamma in BALB/c but not C57BL/6 mice. J. Immunol. 160:1708.
16. Labow, M., Shuster, D., Zetterstrom, M. et al. 1997. Absence of IL-1 signaling and reduced inflammatory response in IL-1 type I receptor-deficient mice. J. Immunol. 159:2452.
17. Kluczyk, A., Siemion, I. Z., Slon-Usakiewicz, J. J. and Wieczorek, Z. 1997. Immunomodulatory activity of oligopeptides related to interleukin 1 receptor antagonist sequence. Arch. Immunol. Ther. Exp. (Warsz) 45:427.
18. Zheng, H., Fletcher, D., Kozak, W. et al. 1995. Resistance to fever induction and impaired acute-phase response in interleukin-1 beta-deficient mice. Immunity 3:9.
19. Nakae, S., Naruse-Nakajima, C., Sudo, K., Horai, R., Asano, M. and Iwakura, Y. 2001. IL-1alpha, but not IL-1beta, is required for contact-allergen-specific T cell activation during the sensitization phase in contact hypersensitivity. Int. Immunity. 13:1471.
20. Horai, R., Asano,. M., Sudo, K. et al. 1998. Production of mice deficient in genes for interleukin (IL)-1alpha, IL-1beta, IL-1 alpha/ beta, and IL-1 receptor antagonist shows that IL-1 beta is crucial in turpentine-induced fever development and glucocorticoid secretion. J. Exp. Med. 187:1463.
21. Glaccum, M. B., Stocking, K. L., Charrier, K. et al. 1997. Phenotypic and functional characterization of mice that lack the type I receptor for IL-1. J. Immunol. 159:3364.
22. Taniguchi, T., Takata, M., Ikeda, A., Momotani, E. and Sekikawa, K. 1997. Failure of germinal center formation and impairment of response to endotoxin in tumor necrosis factor alpha-deficient mice. Lab. Investig. 77:647.
23. Sarnstrand, B., Jansson, A. H., Matuseviciene, G., Scheynius, A., Pierrou, S. and Bergstrand, H. 1999. N,N'-Diacetyl-L-cystine-the disulfide dimer of N-acetylcysteine-is a potent modulator of contact sensitivity/delayed type hypersensitivity reactions in rodents. J. Pharmacol. Exp. Ther. 288:1174.
24. Yoshimoto, T., Wang, C. R., Yoneto, T, Matsuzawa, A., Cruikshank, W. W. and Nariuchi, H. 2000. Role of IL-16 in delayed-type hypersensitivity reaction. Blood 95:2869.
25. Ohshima, S., Saeki, Y., Mima, T. et al. 1998. Interleukin 6 plays a key role in the development of antigen-induced arthritis. Proc. Natl Acad. Sci. USA 95:8222.
26. Nakae, S., Komiyama, Y, Narumi, S. et al. 2003. IL-1-induced tumor necrosis factor-alpha elicits inflammatory cell infiltration in the skin by inducing IFN-gamma-inducible protein 10 in the elicitation phase of the contact hypersensitivity response. Int. Immunol. 15:251.
27. Banerjee, D., Liou, H. C. and Sen, R. 2005. c-Rel-dependent priming of naive T cells by inflammatory cytokines. Immunity 23:445.
28. Nakae, S., Komiyama, Y., Yokoyama, H. et al. 2003. IL-1 is required for allergen-specific Th2 cell activation and the development of airway hypersensitivity response. Int. Immunol. 15:483.
29. Nakae, S., Horai, R., Asano, M. and Iwakura, I. 2001. Interleukin-1beta, but not Interleukin-1alpha, is required for T-cell-dependent antibody production. Immunology 104:402.
30. Nakae, S., Asano, M., Horai, R., Sakaguchi, N. and Iwakura, Y. 2001. IL-1 enhances T cell-dependent antibody production through induction of CD40 ligand and OX40 on T cells. J. Immunol. 167:90.
31. Rissoan, M. C., Soumelis, V., Kadowaki, N. et al. 1999. Reciprocal control of T helper cell and dendritic cell differentiation. Science 283:1183.
32. Hope, J. C., Sopp, P., Collins, R. A. and Howard, C. J. 2001. Differences in the induction of CD8+ T cell responses by subpopulations of dendritic cells from afferent lymph are related to IL-1 alpha secretion. J. Leukoc. Biol. 69:271.
33. Shornick, L., De Togni, P., Mariathasan, S. et al. 1996. Mice deficient in IL-1beta manifest impaired contact hypersensitivity to trinitrochlorobenzone. J. Exp. Med. 183:1427.
34. Fong, T. A. and Mosmann, T. R. 1989. The role of IFN-gamma in delayed-type hypersensitivity mediated by Th1 clones. J. Immunol. 143:2887.
35. Magram, J., Connaughton, S. E., Warrier, R. R. et al. 1996. IL-12-deficient mice are defective in IFN gamma production and type 1 cytokine responses. Immunity 4:471.
36. Werman, A., Werman-Venkert, R., White, R. et al. 2004. The precursor form of IL-1alpha is an intracrine proinflammatory activator of transcription. Proc. Natl Acad. Sci. USA 101:2434.
37. Flynn, J. L., Chan, J., Triebold, K. J., Dalton, D. K., Stewart, T. A. and Bloom, B. R. 1993. An essential role for interferon gamma in resistance to Mycobacterium tuberculosis infection. J. Exp. Med. 178:2249.
38. Cooper, A. M., Dalton, D. K., Stewart, T. A., Griffin, J. P., Russell, D. G. and Orme, I. M. 1993. Disseminated tuberculosis in interferon gamma gene-disrupted mice. J. Exp. Med. 178:2243.
39. Guo, Z., Zhang, M., An, H. et al. 2003. Fas ligation induces IL-1beta-dependent maturation and IL-1beta-independent survival of dendritic cells: Different roles of ERK and NF-kappaB signaling pathways. Blood 102:4441. (Epub August 14, 2003.)
40. Khoruts, A., Osness, R. E. and Jenkins, M. K. 2004. IL-1 acts on antigen-presenting cells to enhance the in vivo proliferation of antigen-stimulated naive CD4 T cells via a CD28-dependent mechanism that does not involve increased expression of CD28 ligands. Eur. J. Immunol. 34:1085.
41. Luft, T., Jefford, M., Luetjens, P. et al. 2002. IL-1beta enhances CD40 ligand-mediated cytokine secretion by human dendritic cells (DC): A mechanism for T cell-independent DC activation. J. Immunol. 168:713.
42. Wesa, A. K. and Galy, A. 2001. IL-1beta induces dendritic cells to produce IL-12. Int. Immunol. 13:1053.
43. Freedman, A. S., Freeman, G., Whitman, J., Segil, J., Daley, J. and Nadler, L. M. 1988. Pre-exposure of human B cells to recombinant IL-1 enhances subsequent proliferation. J. Immunol. 141:3398.
44. Rousset, F, Garcia, E. and Banchereau, J. 1991. Cytokine-induced proliferation and immunoglobulin production of human B lymphocytes triggered through their CD40 antigen. J. Exp. Med. 173:705.
45. Liu, Y. J., Cairns, J. A., Holder, M. J. et al. 1991. Recombinant 25-kDa CD23 and interleukin 1 alpha promote the survival of germinal center B cells: Evidence for bifurcation in the development of centrocytes rescued from apoptosis. Eur. J. Immunol. 21:1107.
46. Toellner, K. M., Scheel-Toellner, D., Sprenger, R. et al. 1995. The human germinal centre cells, follicular dendritic cells and germinal centre T cells produce B cell-stimulating cytokines. Cytokine 7:344.
47. Snapper, C. M. and Paul, W. E. 1987. Interferon-gamma and B cell stimulatory factor-1 reciprocally regulate Ig isotype production. Science 236:944.
48. Peng, S. L., Szabo, S. J. and Glimcher, L. H. 2002. T-bet regulates IgG class switching and pathogenic autoantibody production. Proc. Natl Acad. Sci. USA 99:5545.
49. Lagrange, P. H. and Mackaness, G. B. 1975. A stable form of delayed-type hypersensitivity. J. Exp. Med. 141:82.
50. Koide, S. L., Inaba, K. and Steinman, R. M. 1987. Interleukin 1 enhances T-dependent immune responses by amplifying the function of dendritic cells. J. Exp. Med. 165:515.
51. Richards, H. B., Satoh, M., Shaw, M., Libert, C., Poli, V. and Reeves, W. H. 1998. Interleukin 6 dependence of anti-DNA antibody production: evidence for two pathways of auto-antibody formation in pristane-induced lupus. J. Exp. Med. 188:985.
52. Eugster, H. P., Frei, K., Bachmann, R., Bluethmann, H., Lassmann, H. and Fontana, A. 1999. Severity of symptoms and demyelination in MOG-induced EAE depends on TNFR1. Eur. J. Immunol. 29:626.
53. Kassiotis, G. and Kollias, G. 2001. Uncoupling the proinflammatory from the immunosuppressive properties of tumor necrosis factor (TNF) at the p55 TNF receptor level: Implications for pathogenesis and therapy of autoimmune demyelination. J. Exp. Med. 193:427.
54. Campbell, I. K., O'Donnell, K., Lawlor, K. E. and Wicks, I. P. 2001. Severe inflammatory arthritis and lymphadenopathy in the absence of TNF. J. Clin. Invest. 107:1519.
55. Tada, Y., Ho, A., Koarada, S. et al. 2001. Collagen-induced arthritis in TNF receptor-1-deficient mice: TNF receptor-2 can modulate arthritis in the absence of TNF receptor-1. Clin. Immunol. 99:325.
56. Mori, L., Iselin, S., De Libero, G. and Lesslauer, W. 1996. Attenuation of collagen-induced arthritis in 55-kDa TNF receptor type 1 (TNFR1)-IgG1-treated and TNFR1-deficient mice. J. Immunol. 157:3178.
57. Huang, D., Tani, M., Wang, J. et al. 2002. Pertussis toxin-induced reversible encephalopathy dependent on monocyte chemoattractant protein-1 overexpression in mice. J. Neurosci. 22:10633.
58. Rand, M. L., Warren, J. S., Mansour, M. K., Newman, W. and Ringler, D. J. 1996. Inhibition of T cell recruitment and cutaneous delayed-type hypersensitivity-induced inflammation with antibodies to monocyte chemoattractant protein-1. Am. J. Pathol. 148:855.
59. Kawakami, K., Koguchi, Y., Qureshi, M. H. et al. 2000. Reduced host resistance and Th1 response to Cryptococcus neoformans in interleukin-18 deficient mice. FEMS Microbiol. Lett. 186:121.
60. Cruikshank, W. W., Kornfeld, H. and Center, D. M. 2000. Interleukin-16. J. Leukoc. Biol. 67:757.
61. Wilkinson, R. J., Patel, P., Llewelyn, M. et al. 1999. Influence of polymorphism in the genes for the interleukin (IL)-1 receptor antagonist and IL-1beta on tuberculosis. J. Exp. Med. 189:1863.