IL-13 is necessary, not simply sufficient, for epicutaneously induced Th2 responses to soluble protein antigen

Journal of Immunology

Volumn 170, Issue 5, 2003, Pages 2488-2495

  Herrick, Christina A ^a   Xu, Lan ^a   McKenzie, Andrew N J ^b   Tigelaar, Robert E ^a   Bottomly, Kim ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

1 FLUORO 2,4 DINITROBENZENE; ALLERGEN; ANTIGEN; IMMUNOGLOBULIN G1; INTERLEUKIN 13; INTERLEUKIN 4; INTERLEUKIN 5;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ATOPY; CONTACT ALLERGY; CONTROLLED STUDY; EFFECTOR CELL; FEMALE; IMMUNE RESPONSE; INFLAMMATION; MOUSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; SENSITIZATION; TH1 CELL; TH2 CELL;

EID: 0344211820     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.170.5.2488     Document Type: Article

References (53)

1. van Reijsen, F. C., C. A. F. M. Bruijnzeel-Koomen, F. S. Kalthoff, E. Maggi, S. Romagnani, J. K. T. Westland, and G. C. Mudde. 1992. Skin-derived aeroallergen-specific T-cell clones of Th2 phenotype in patients with atopic dermatitis. J. Allergy Clin. Immunol. 90:184.
2. Hamid, Q., M. Boguniewicz, and D. Y. Leung. 1994. Differential in situ cytokine gene expression in acute versus chronic atopic dermatitis. J. Clin. Invest. 94:870.
3. Hamid, Q., T. Naseer, E. M. Minshall, Y. L. Song, M. Boguniewicz, and D. Y. Leung. 1996. In vivo expression of IL-12 and IL-13 in atopic dermatitis. J. Allergy Clin. Immunol. 98:225.
4. 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.
5. + T cells, increased TH2-type cytokine mRNA expression, and eosinophil recruitment in bronchoalveolar lavage after allergen inhalation challenge in patients with atopic asthma. J. Allergy Clin. Immunol. 92:313.
6. Huang, S. K., H. Q. Xiao, J. Kleine-Tebbe, G. Paciotti, D. G. Marsh, L. M. Lichtenstein, and M. C. Liu. 1995. IL-13 expression at the sites of allergen challenge in patients with asthma. J. Immunol. 155:2688.
7. Bonnefoy, J. Y., J. F. Gauchat, S. Lecoanet-Henchoz, P. Graber, and J. P. Aubry. 1996. Regulation of human IgE synthesis. Ann. NY Acad. Sci. 796:59.
8. Finkelman, F. D., I. M. Katona, J. F. Urban, Jr., J. Holmes, J. Ohara, A. S. Tung, J. V. Sample, and W. E. Paul. 1988. IL-4 is required to generate and sustain in vivo IgE responses. J. Immunol. 141:2335.
9. Resnick, M. B., and P. F. Weller. 1993. Mechanisms of eosinophil recruitment. Am. J. Respir. Cell Mol. Biol. 8:349.
10. Wills-Karp, M., J. Luyimbazi, X. Xu, B. Schofield, T. Y. Neben, C. L. Karp, and D. D. Donaldson. 1998. Interleukin-13: central mediator of allergic asthma [see comments]. Science 282:2258.
11. Grunig, G., M. Warnock, A. E. Wakil, R. Venkayya, F. Brombacher, D. M. Rennick, D. Sheppard, M. Mohrs, D. D. Donaldson, R. M. Locksley, and D. B. Corry. 1998. Requirement for IL-13 independently of IL-4 in experimental asthma. Science 282:2261.
12. Lee, J. J., M. P. McGarry, S. C. Farmer, K. L. Denzler, K. A. Larson, P. E. Carrigan, I. E. Brenneise, M. A. Horton, A. Haczku, E. W. Gelfand, G. D. Leikauf, and N. A. Lee. 1997. Interleukin-5 expression in the lung epithelium of transgenic mice leads to pulmonary changes pathognomonic of asthma. J. Exp. Med. 185:2143.
13. Brombacher, F. 2000. The role of interleukin-13 in infectious diseases and allergy. Bioessays 22:646.
14. de Waal Malefyt, R., C. G. Figdor, R. Huijbens, S. Mohan-Peterson, B. Bennett, J. Culpepper, W. Dang, G. Zurawski, and J. E. de Vries. 1993. Effects of IL-13 on phenotype, cytokine production, and cytotoxic function of human monocytes: comparison with IL-4 and modulation by IFN-γ or IL-10. J. Immunol. 151:6370.
15. Doherty, T. M., R. Kastelein, S. Menon, S. Andrade, and R. L. Coffman. 1993. Modulation of murine macrophage function by IL-13. J. Immunol. 151:7151.
16. McKenzie, A. N., J. A. Culpepper, R. de Waal Malefyt, F. Briere, J. Punnonen, G. Aversa, A. Sato, W. Dang, B. G. Cocks, S. Menon, et al. 1993. Interleukin 13. a T-cell-derived cytokine that regulates human monocyte and B-cell function. Proc. Natl. Acad. Sci. USA 90:3735.
17. Lin, J. X., T. S. Migone, M. Tsang, M. Friedmann, J. A. Weatherbee, L. Zhou, A. Yamauchi, E. T. Bloom, J. Mietz, S. John, et al. 1995. The role of shared receptor motifs and common Stat proteins in the generation of cytokine pleiotropy and redundancy by IL-2, IL-4, IL-7, IL-13, and IL-15. Immunity 2:331.
18. Smerz-Bertling, C., and A. Duschl. 1995. Both interleukin 4 and interleukin 13 induce tyrosine phosphorylation of the 140-kDa subunit of the interleukin 4 receptor. J. Biol. Chem. 270:966.
19. Zurawski, S. M., P. Chomarat, O. Djossou, C. Bidaud, A. N. McKenzie, P. Miossec, J. Banchereau, and G. Zurawski. 1995. The primary binding subunit of the human interleukin-4 receptor is also a component of the interleukin-13 receptor. J. Biol. Chem. 270:13869.
20. Takeda, K., T. Tanaka, W. Shi, M. Matsumoto, M. Minami, S. Kashiwamura, K. Nakanishi, N. Yoshida, T. Kishimoto, and S. Akira. 1996. Essential role of Stat6 in IL-4 signalling. Nature 380:627.
21. Shimoda, K., J. van Deursen, M. Y. Sangster, S. R. Sarawar, R. T. Carson, R. A. Tripp, C. Chu, F. W. Quelle, T. Nosaka, D. A. Vignali, et al. 1996. Lack of IL-4-induced Th2 response and IgE class switching in mice with disrupted Stat6 gene. Nature 380:630.
22. Akimoto, T., F. Numata, M. Tamura, Y. Takata, N. Higashida, T. Takashi, K. Takeda, and S. Akira. 1998. Abrogation of bronchial eosinophilic inflammation and airway hyperreactivity in signal transducers and activators of transcription (STAT)6-deficient mice. J. Exp. Med. 187:1537.
23. Kaplan, M. H., and M. J. Grusby. 1998. Regulation of T helper cell differentiation by STAT molecules. J. Leukocyte Biol. 64:2.
24. Swain, S. L., A. D. Weinberg, M. English, and G. Huston. 1990. IL-4 directs the development of Th2-like helper effectors. J. Immunol. 145:3796.
25. + T cells from T cell receptor transgenic mice. J. Exp. Med. 176:1091.
26. Zurawski, G., and J. E. de Vries. 1994. Interleukin 13, an interleukin 4-like cytokine that acts on monocytes and B cells, but not on T cells. Immunol. Today 15:19.
27. Noben-Trauth, N., P. Kropf, and I. Muller. 1996. Susceptibility to Leishmania major infection in interleukin-4-deficient mice. Science 271:987.
28. Chensue, S. W., K. Warmington, J. H. Ruth, N. Lukacs, and S. L. Kunkel. 1997. Mycobacterial and schistosomal antigen-elicited granuloma formation in IFN-γ and IL-4 knockout mice: analysis of local and regional cytokine and chemokine networks. [Published erratum appears in 1999 J. Immunol. 162:3106.] J. Immunol. 159:3565.
29. von der Weid, T., M. Kopf, G. Kohler, and J. Langhorne. 1994 The immune response to Plasmodium chabaudi malaria in interleukin-4-deficient mice. Eur. J. Immunol. 24:2285.
30. Lawrence, R. A., C. A. Gray, J. Osborne, and R. M. Maizels. 1996. Nippostrongylus brasiliensis: cytokine responses and nematode expulsion in normal and IL-4-deficient mice. Exp. Parasitol. 84:65.
31. Barner, M., M. Mohrs, F. Brombacher, and M. Kopf. 1998. Differences between IL-4Rα-deficient and IL-4-deficient mice reveal a role for IL-13 in the regulation of Th2 responses. Curr. Biol. 8:669.
32. McKenzie, G. J., C. L. Emson, S. E. Bell, S. Anderson, P. Fallon, G. Zurawski, R. Murray, R. Grencis, and A. N. McKenzie. 1998. Impaired development of Th2 cells in IL-13-deficient mice. Immunity 9:423.
33. Urban, J. F., Jr., N. Noben-Trauth, D. D. Donaldson, K. B. Madden, S. C. Morris, M. Collins, and F. D. Finkelman. 1998. IL-13, IL-4Rα, and Stat6 are required for the expulsion of the gastrointestinal nematode parasite Nippostrongylus brasiliensis. Immunity 8:255.
34. Herrick, C. A., H. MacLeod, E. Glusac, R. E. Tigelaar, and K. Bottomly. 2000. Th2 responses induced by epicutaneous or inhalational protein exposure are differentially dependent on IL-4. J. Clin. Invest. 105:765.
35. Zhu, Z., R. J. Homer, Z. Wang, Q. Chen, G. P. Geba, J. Wang, Y. Zhang, and J. A. Elias. 1999. Pulmonary expression of interleukin-13 causes inflammation, mucus hypersecretion, subepithelial fibrosis, physiologic abnormalities, and eotaxin production. J. Clin. Invest. 103:779.
36. Walter, D. M., J. J. McIntire, G. Berry, A. N. McKenzie, D. D. Donaldson, R. H. DeKruyff, and D. T. Umetsu. 2001. Critical role for IL-13 in the development of allergen-induced airway hyperreactivity. J. Immunol. 167:4668.
37. van der Ploeg, I., G. Matuseviciene, J. Fransson, C. F. Wahlgren, T. Olsson, and A. Scheynius. 1999. Localization of interleukin-13 gene-expressing cells in tuberculin reactions and lesional skin from patients with atopic dermatitis. Scand. J. Immunol. 49:447.
38. Chiaramonte, M. G., A. W. Cheever, J. D. Malley, D. D. Donaldson, and T. A. Wynn. 2001. Studies of murine schistosomiasis reveal interleukin-13 blockade as a treatment for established and progressive liver fibrosis. Hepatology 34: 273.
39. Guo, L., J. Hu-Li, J. Zhu, C. Pannetier, C. Watson, G. J. McKenzie, A. N. McKenzie, and W. E. Paul. 2001. Disrupting I113 impairs production of IL-4 specified by the linked allele. Nat. Immunol. 2:461.
40. + T cells in murine contact sensitivity revealed by in vivo monoclonal antibody depletion. J. Immunol. 144:4121.
41. Seidenari, S., and G. Giusti. 1995. Objective assessment of the skin of children affected by atopic dermatitis: a study of pH, capacitance and TEWL in eczematous and clinically uninvolved skin. Acta Derm. Venereol. 75:429.
42. Berardesca, E., D. Fideli, G. Borroni, G. Rabbiosi, and H. Maibach. 1990. In vivo hydration and water-retention capacity of stratum corneum in clinically uninvolved skin in atopic and psoriatic patients. Acta Derm. Venereol. 70:400.
43. Wang, L. F., J. Y. Lin, K. H. Hsieh, and R. H. Lin. 1996. Epicutaneous exposure of protein antigen induces a predominant Th2-like response with high IgE production in mice. J. Immunol. 156:4077.
44. Spergel, J. M., E. Mizoguchi, J. P. Brewer, T. R. Martin, A. K. Bran, and R. S. Geha. 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.
45. Oranje, A. P., D. Van Gysel, P. G. Mulder, and P. H. Dieges. 1994. Food-induced contact urticaria syndrome (CUS) in atopic dermatitis: reproducibility of repeated and duplicate testing with a skin provocation test, the skin application food test (SAFT). Contact Dermatitis 31:314.
46. Hunt, L. W., A. F. Fransway, C. E. Reed, L. K. Miller, R. T. Jones, M. C. Swanson, and J. W. Yunginger. 1995. An epidemic of occupational allergy to latex involving health care workers. J. Occup. Environ. Med. 37:1204.
47. Morales, C., A. Basomba, J. Carreira, and A. Sastre. 1989. Anaphylaxis produced by rubber glove contact: case reports and immunological identification of the antigens involved. Clin. Exp. Allergy 19:425.
48. Bohle, B., B. Wagner, U. Vollmann, D. Buck, B. Niggemann, Z. Szepfalusi, G. Fischer, O. Scheiner, H. Breiteneder, and C. Ebner. 2000. Characterization of T cell responses to Hev b 3, an allergen associated with latex allergy in spina bifida patients. J. Immunol. 164:4393.
49. Kopf, M., G. L. Gros, M. Bachmann, M. C. Lamers, H. Bluethmann, and G. Kohler. 1993. Disruption of the murine IL-4 gene blocks Th2 cytokine responses. Nature 362:245.
50. Vajdy, M., M. H. Kosco-Vilbois, M. Kopf, G. Kohler, and N. Lycke. 1995. Impaired mucosal immune responses in interleukin 4-targeted mice. J. Exp. Med. 181:41.
51. Coyle, A. J., G. Le Gros, C. Bertrand, S. Tsuyuki, C. H. Heusser, M. Kopf, and G. P. Anderson. 1995. Interleukin-4 is required for the induction of lung Th2 mucosal immunity. Am. J. Respir. Cell Mol. Biol. 13:54.
52. Brusselle, G. G., J. C. Kips, J. H. Tavernier, J. G. van der Heyden, C. A. Cuvelier, R. A. Pauwels, and H. Bluethmann. 1994. Attenuation of allergic airway inflammation in IL-4 deficient mice. Clin. Exp. Allergy 24:73.
53. Soumelis, V., P. A. Reche, H. Kanzler, W. Yuan, G. Edward, B. Homey, M. Gilliet, S. Ho, S. Antonenko, A. Lauerma, et al. 2002. Human epithelial cells trigger dendritic cell mediated allergic inflammation by producing TSLP. Nat. Immunol. 3:673.