To respond or not to respond: T cells in allergic asthma

Nature Reviews Immunology

Volumn 3, Issue 5, 2003, Pages 405-412

  Herrick, Christina A ^a   Bottomly, Kim ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 13; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 9; TOLL LIKE RECEPTOR;

ALLERGIC ASTHMA; DENDRITIC CELL; DISEASE ASSOCIATION; HOMEOSTASIS; HUMAN; PRIORITY JOURNAL; REVIEW; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TH2 CELL; ASTHMA; BIOLOGICAL MODEL; IMMUNOLOGY; RESPIRATORY TRACT ALLERGY; TH1 CELL;

ASTHMA; HOMEOSTASIS; HUMANS; MODELS, IMMUNOLOGICAL; RESPIRATORY HYPERSENSITIVITY; T-LYMPHOCYTES; TH1 CELLS; TH2 CELLS;

EID: 0038387445     PISSN: 14741733     EISSN: None     Source Type: Journal    
DOI: 10.1038/nri1084     Document Type: Review

References (116)

1. Holgate, S. T. The epidemic of allergy and asthma. Nature 402, B2-B4 (1999).
2. Umetsu, D. T., McIntire, J. J., Akbari, O., Macaubas, C. & DeKruyff, R. H. Asthma: an epidemic of dysregulated immunity. Nature Immunol. 3, 715-720 (2002).
3. Cookson, W. The alliance of genes and environment in asthma and allergy. Nature 402, B5-B11 (1999).
4. Strachan, D. P. Hay fever, hygiene, and household size. BMJ 299, 1259-1260 (1989).
5. Strachan, D. P. Family size, infection and atopy: the first decade of the 'hygiene hypothesis'. Thorax 55 Suppl. 1, S2-S10 (2000).
6. von Mutius, E. et al. Skin test reactivity and number of siblings. BMJ 308, 692-695 (1994).
7. Kramer, U., Heinrich, J., Wjst, M. & Wichmann, H. E. Age of entry to day nursery and allergy in later childhood. Lancet 353, 450-454 (1999).
8. Ball, T. M. et al. Siblings, day-care attendance, and the risk of asthma and wheezing during childhood. N. Engl. J. Med. 343, 538-543 (2000).
9. Busse, W. W. & Lemanske, R. F. Jr. Asthma. N. Engl. J. Med. 344, 350-362 (2001).
10. Kim, J., Woods, A., Becker-Dunn, E. & Bottomly, K. Distinct functional phenotypes of cloned la-restricted helper T cells. J. Exp. Med. 162, 188-201 (1985).
11. Mosmann, T. R., Cherwinski, H., Bond, M. W., Giedlin, M. A. & Coffman, R. L. Two types of murine helper T cell clone. I. Definition according to profiles of lymphokine activities and secreted proteins. J. Immunol. 136, 2348-2357 (1986).
12. H2 phenotype in patients with atopic dermatitis. J. Allergy Clin. Immunol. 90, 184-192 (1992).
13. H2-like bronchoalveolar T-lymphocyte population in atopic asthma. N. Engl. J. Med. 326, 298-304 (1992).
14. Walker, C. et al. Allergic and nonallergic asthmatics have distinct patterns of T-cell activation and cytokine production in peripheral blood and bronchoalveolar lavage. Am. Rev. Respir. Dis. 146, 109-115 (1992).
15. H2-type cytokine mRNA expression, and eosinophil recruitment in bronchoalveolar lavage after allergen inhalation challenge in patients with atopic asthma. J. Allergy Clin. Immunol. 92, 313-324 (1993).
16. Hamid, Q., Boguniewicz, M. & Leung, D. Y. Differential in situ cytokine gene expression in acute versus chronic atopic dermatitis. J. Clin. Invest. 94, 870-876 (1994).
17. Huang, S. K. et al. IL-13 expression at the sites of allergen challenge in patients with asthma. J. Immunol. 155, 2688-2694 (1995).
18. Hamid, Q. et al. In vivo expression of IL-12 and IL-13 in atopic dermatitis. J. Allergy Clin. Immunol. 98, 225-231 (1996)
19. + T-lymphocytes and interleukin-5 mediate antigen-induced eosinophil infiltration into the mouse trachea. Am. Rev. Respir. Dis. 146, 374-377 (1992).
20. + T lymphocytes prevents antigen-induced airway hyperreactivity and pulmonary eosinophilia. Am. J. Respir. Cell. Mol. Biol. 10, 587-593 (1994).
21. Brusselle, G. G. et al. Attenuation of allergic airway inflammation in IL-4 deficient mice. Clin. Exp. Allergy 24, 73-80 (1994).
22. H1, cells. J. Immunol. 161, 3813-3816 (1998).
23. H2 mucosal immunity. Am. J. Respir. Cell. Mol. Biol. 13, 54-59 (1995).
24. Kips, J. C. et al. Importance of interleukin-4 and interleukin-12 in allergen-induced airway changes in mice. Int. Arch. Allergy Immunol. 107, 115-118 (1995).
25. Corry, D. B. et al. Interleukin 4, but not interleukin 5 or eosinophils, is required in a murine model of acute airway hyperreactivity. J. Exp. Med. 183, 109-117 (1996)
26. H2 responses induced by epicutaneous or inhalational protein exposure are differentially dependent on IL-4. J. Clin. Invest. 105, 765-775 (2000).
27. Schwarze, J. et al. CD8 T cells are essential in the development of respiratory syncytial virus-induced lung aosinophilia and airway hyperresponsiveness. J. Immunol. 162, 4207-4211 (1999).
28. Schwarze, J. et al. Transfer of the enhancing effect of respiratory syncytial virus infection on subsequent allergic airway sensitization by T lymphocytes. J. Immunol. 163, 5729-5734 (1999).
29. Abbas, A. K., Murphy, K. M. & Sher, A. Functional diversity of helper T lymphocytes. Nature 383, 787-793 (1996)
30. Shirakawa, T., Enomoto, T., Shimazu, S. & Hopkin, J. M. The inverse association between tuberculin responses and atopic disorder. Science 275, 77-79 (1997).
31. Shaheen, S. O. et al. Measles and atopy in Guinea-Bissau. Lancet 347, 1792-1796 (1996).
32. von Hertzen, L., Klaukka, T., Mattila, H. & Haahtela, T. Mycobacterium tuberculosis infection and the subsequent development of asthma and allergic conditions. J Allergy Clin. Immunol. 104, 1211-1214 (1999).
33. Fonager, K., Sorensen, H. T. & Olsen, J. Change in incidence of Crohn's disease and ulcerative colitis in Denmark. A study based on the National Registry of Patients, 1981-1992. Int. J. Epidemiol. 26, 1003-1008 (1997).
34. Armitage, E., Drummond, H. E., Wilson, D. C. & Ghosh, S. Increasing incidence of both juvenile-onset Crohn's disease and ulcerative colitis in Scotland. Eur. J. Gastroenterol. Hepatol. 13, 1439-1447 (2001).
35. Onkamo, P., Vaananen, S., Karvonen, M. & Tuomilehto, J. Woddwide increase in incidence of type I diabetes - the analysis of the data on published incidence trends. Diabetologia 42, 1395-1403 (1999).
36. van den Biggelaar, A. H. et al. The prevalence of parasite infestation and house dust mite sensitization in Gabonese schoolchildren. Int. Arch. Allergy Immunol. 126, 231-238 (2001).
37. H2 responses without atopy: immunoregulation in chronic helminth infections and reduced allergic disease. Trends Immunol. 22, 372-377 (2001).
38. H2-induced airway mucus production is dependent on IL-4Rα, but not on eosinophils. J. Immunol. 162, 6178-6183 (1999).
39. H2 cell-induced airway hyperreactivity but cause severe airway inflammation. J. Clin. Invest. 103, 175-183 (1999).
40. H2 cell-dependent bronchial hyperresponsiveness and eosinophilic inflammation partly via IFN-γ. J. Immunol. 166, 207-217 (2001).
41. Hogan, S. P., Mould, A. Kikutani, H., Ramsay, A. J. & Foster P. S. Aeroallergen-induced eosinophilic inflammation, lung damage, and airways hyperreactivity in mice can occur independently of IL-4 and allergen-specific immunoglobulins. J. Clin. Invest. 99, 1329-1339 (1997).
42. Cohn, L., Herrick, C., Niu, N., Homer, R. & Bottomly, K. IL-4 promotes airway eosinophilia by suppressing IFN-γ production: defining a novel role for IFN-γ in the regulation of allergic airway inflammation. J. Immunol. 166, 2760-2767 (2001).
43. H1 responses at the effector stage of lung inflammation. J. Immunol. 161, 3128-3135 (1998).
44. H2 cells in a murine model of eosinophilic airway inflammation. J. Clin. Invest. 104, 1021-1029 (1999).
45. Boguniewicz, M. et al. The effects of nebulized recombinant interferon-γ in asthmatic airways. J Allergy Clin. Immunol. 95, 133-135 (1995).
46. Martin, R. J. et al. The effects of inhaled interferon-γ in normal human airways. Am Rev. Respir. Dis. 148, 1677-1682 (1993).
47. H2 in asthma? Clin. Exp. Allergy 32, 17-29 (2002)
48. Wills-Karp, M., Santeliz, J. & Karp, C. L. The germless theory of allergic disease: revisiting the hygiene hypothesis. Nature Rev. Immunol. 1, 69-75. (2001).
49. Yssel, H., Lecart, S. & Pene, J. Regulatory T cells and allergic asthma. Microbes Infect. 3, 899-904 (2001).
50. + suppressor T cells: more questions than answers. Nature Rev. Immunol. 2, 389-400 (2002).
51. + regulatory T cells. Curr. Opin. Immunol. 13, 644-649 (2001).
52. R1) cells.
53. H2 paradigm in immunity to infectious diseases. Trends Immunol. 23, 450-455 (2002).
54. + or T cell receptor (TCR)-γδ-T cells or interferon (IFN)-γ in a murine model of allergen sensitization. J. Ex. Med. 187, 721-731 (1998).
55. + T cells. J. Immunol. 163, 2592-2600 (1999).
56. Akbari, O., DeKruyff, R. H. & Umetsu, D. T. Pulmonary denddtic cells producing IL-10 mediate tolerance induced by respiratory exposure to antigen. Nature Immunol. 2, 725-731 (2001).
57. Schwartz, R. H. Costimulation of T lymphocytes: the role of CD28, CTLA-4, and B7/BB1 in interleukin-2 production and immunotherapy. Cell 71, 1065-1068 (1992).
58. Medzhitov, R. Toll-like receptors and innate immunity. Nature Rev. Immunol. 1, 135-145 (2001).
59. Janeway, C. A. Jr & Medzhitov, R. Innate immune recognition. Annu. Rev. Immunol. 20, 197-216 (2002).
60. Zuany-Amorim, C. et al. Suppression of airway eosinophilia by killed Mycobacterium vaccae-induced allergen-specific regulatory T-cells Nature Med. 8, 625-629 (2002). This paper shows that prior exposure to microbial antigens can suppress the subsequent generation of an antigen-specific airway inflammatory response.
61. Wakkach, A. et al. Characterization of dendritic cells that induce tolerance and T regulatory 1 cells differentiation in vivo. Immunity (in the press).
62. Holt, P. G., Batty, J. E. & Turner, K. J. Inhibition of specific IgE responses in mice by pre-exposure to inhaled antigen. Immunology 42, 409-417 (1981).
63. Akban, O. et al. Antigen-specific regulatory T cells develop via the ICOS-ICOS-ligand pathway and inhibit allergen-induced airway hyperreactivity. Nature Med. 8, 1024-1032 (2002). This study shows both the ability of inhaled antigen to induce a population of dendritic cells (DCs), which can then induce regulatory T cells in vitro, as well as the capacity of regulatory T cells to suppress airway inflammatory responses.
64. H2-cell responses in the airways is dependent on the innate immune system signalling through Toll-like receptor 4 (TLR4) and provides a probable mechanism involving DC maturation.
65. H2 immune responses: role of dendritic cells. J. Immunol. 168, 4524-4530 (2002).
66. von Mutius, E. et al. Exposure to endotoxin or other bacterial components might protect against the development of atopy. Clin. Exp. Allergy 30, 1230-1234 (2000)
67. Park, J. H., Gold, D. R., Spiegelman, D. L., Burge, H. A. & Milton, D. K. House dust endotoxin and wheeze in the first year of life. Am. J. Respir. Crit. Care Med. 163, 322-328 (2001).
68. Reed, C. E. & Milton, D. K. Endotoxin-stimulated innate immunity: a contributing factor for asthma. J. Allergy Clin. Immunol. 108, 157-166 (2001).
69. + T cells with regulatory properties by repetitive stimulation with allogeneic immature human dendritic cells. J. Exp. Med. 192, 1213-1222 (2000).
70. Barnes, P. F. et al. Cytokine production induced by Mycobacterium tuberculosis lipoarabinomannan. Relationship to chemical structure. J. Immunol. 149, 541-547 (1992).
71. Van der Kleij, D. et al. Triggering of innate immune responses by schistosome egg glycolipids and their carbohydrate epitope GalNAc β1-4(Fuc α1-2Fuc α1-3)GlcNAc. J. Infect. Dis. 185, 531-539 (2002).
72. Mahanty, S. et al. High levels of spontaneous and parasite antigen-driven interleukin-10 production are associated with antigen-specific hyporesponsiveness in human lymphatic filariasis. J. Infect. Dis. 173, 769-773 (1996)
73. Gale, E. A. A missing link in the hygiene hypothesis? Diabetologia 45, 588-594 (2002)
74. Chen, Y., Kuchroo, V. K., Inobe, J., Hafler, D. A. & Weiner, H. L. Regulatory T cell clones induced by oral tolerance: suppression of autoimmune encephalomyelitis. Science 265, 1237-1240 (1994).
75. + T-cell subset inhibits antigen-specific T-cell responses and prevents colitis. Nature 389, 737-742 (1997).
76. Roncarolo, M. G. & Levings, M. K. The role of different subsets of T regulatory cells in controlling autoimmunity. Curr. Opin. Immunol. 12, 676-683 (2000).
77. H2-specific response in vivo. J. Immunol. 165, 4848-4853 (2000).
78. Akdis, C. A., Blesken, T., Akdis, M., Wuthrich, B & Blaser, K. Role of interleukin 10 in specific immunotherapy. J. Clin. Invest. 102, 98-106 (1998).
79. Pierkes, M. et al. Decreased release of histamine and sulfidoleukotrienes by human peripheral blood leukocytes after wasp venom immunotherapy is partially due to induction of IL-10 and IFN-γ production of T cells. J. Allergy Clin. Immunol. 103, 326-332 (1999).
80. Jilek, S., Barbey, C., Spertini, F. & Corthesy, B. Antigen-independent suppression of the allergic immune response to bee venom phospholipase A(2) by DNA vaccination in CBA/J mice. J. Immunol. 166, 3612-3621 (2001).
81. Zuany-Amorim, C. et al. Interleukin-10 inhibits antigen-induced cellular recruitment into the airways of sensitized mice. J. Clin. Invest. 95, 2644-2651 (1995).
82. Stampfli, M. R. et al. Interleukin-10 gene transfer to the airway regulates allergic mucosal sensitization in mice. Am. J. Respir. Cell. Mol. Biol. 21, 586-596 (1999).
83. van den Biggelaar, A. H. et al. Decreased atopy in children infected with Schistosoma haematobium: a role for parasite-induced interleukin-10. Lancet 356, 1723-1727 (2000).
84. Oh, J. W. et al. CD4T-helper cells engineered to produce IL-10 prevent allergen-induced airway hyperreactivity and inflammation. J. Allergy Clin. Immunol. 110, 460-468 (2002).
85. H2-dependent pulmonary pathology. J. Immunol. 169, 84-89 (2002)
86. Koslewicz, M. M., Alard, P. & Strellein, J. W. Alterations in cytokine production following intraocular injection of soluble protein antigen: impairment in IFN-γ and induction of TGF-β and IL-4 production. J. Immunol. 161, 5382-5390 (1998).
87. D'Orazio, T. J. & Niederkorn, J. Y. A novel role for TGF-β and IL-10 in the induction of immune privilege. J. Immunol. 160, 2089-2098 (1998).
88. Kung, T. T. et al. Involvement of IL-5 in a murine model of allergic pulmonary inflammation: prophylactic and therapeutic effect of an anti-IL-5 antibody. Am. J. Respir. Cell. Mol. Biol. 13, 360-365 (1995)
89. Van Oosterhout, A. J. et al. Eosinophil infiltration precedes development of airway hyperreactivity and mucosal exudation after intranasal administration of interleukin-5 to mice. J. Allergy Clin. Immunol. 96, 104-112 (1995).
90. Foster, P. S., Hogan, S. P., Ramsay, A. J., Matthaei, K. I. & Young, I. G. Interleukin 5 deficiency abolishes eosinophilia, airways hyperreactivity, and lung damage in a mouse asthma model. J. Exp. Med. 183, 195-201 (1996).
91. Lee, J. J. et al. Interleukin-5 expression in the lung epithelium of transgenic mice leads to pulmonary changes pathognomonic of asthma. J. Exp. Med. 185, 2143-2156 (1997).
92. Grunig, G. et al. Requirement for IL-13 independently of IL-4 in experimental asthma. Science 282, 2261-2263 (1998).
93. Wills-Karp, M. et al. Interleukin-13: central mediator of allergic asthma. Science 282, 2258-2261 (1998).
94. Zhu, Z. et al. Pulmonary expression of interleukin-13 causes inflammation, mucus hypersecretion, subepithelial fibrosis, physiologic abnormalities, and eotaxin production. J. Clin. Invest. 103, 779-788 (1999).
95. Walter, D. M. et al. Critical role for IL-13 in the development of allergen-induced airway hyperreactivity. J. Immunol. 167, 4668-4675 (2001).
96. Temann, U. A., Geba, G. P., Rankin, J. A. & Flavell, R. A. Expression of interleukin 9 in the lungs of transgenic mice causes airway inflammation, mast cell hyperplasia, and bronchial hyperresponsiveness. J. Exp. Med. 188, 1307-1320 (1998).
97. Townsend, J. M. et al. IL-9-deficient mice establish fundamental roles for IL-9 in pulmonary mastocytosis and goblet cell hyperplasia but not T cell development. Immunity 18, 573-583 (2000).
98. Temann, U.A., Ray, P. & Flavell, R. A. Pulmonary overexpression of IL-9 induces TH2 cytokine expression, leading to immune pathology. J. Clin. Invest. 109, 29-39 (2002).
99. McMillan, S. J., Bishop, B., Townsend, M. J., McKenzie, A. N. & Uoyd, C. M. The absence of interleukin 9 does not affect the development of allergen-induced pulmonary inflammation nor airway hyperreactivity. J. Exp. Med. 195, 51-57 (2002).
100. Whittaker, L. et al. Interleukin-13 mediates a fundamental pathway for airway epithelial mucus induced by CD4 T cells and interleukin-9. Am. J. Respir. Cell. Mol. Biol. 27, 593-602 (2002).
101. Kuperman, D. A. et al. Direct effects of interleukin-13 on epithelial cells cause airway hyperreactivity and mucus overproduction in asthma. Nature Med 8, 885-889 (2002).
102. Postlethwaite, A. E. & Seyer, J. M. Fibroblast chemotaxis induction by human recombinant interleukin-4. Identification by synthetic peptide analysis of two chemotactic domains residing in amino acid sequences 70-88 and 89-122. J. Clin. Invest. 87, 2147-2152 (1991).
103. Postlethwaite, A. E., Holness, M. A., Katai, H. & Raghow, R. Human fibroblasts synthesize elevated levels of extracellular matrix proteins in response to interleukin 4. J. Clin. Invest. 90, 1479-1485 (1992).
104. H2 cytokine regulation of type I collagen gel contraction mediated by human lung mesenchymal cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 282, L1049-L1056 (2002).
105. Blease, K. et al. Therapeutic effect of IL-13 immunoneutralization during chronic experimental fungal asthma. J. Immunol. 166, 5219-5224 (2001).
106. H2-like helper effectors. J. Immunol. 145, 3796-3806 (1990).
107. + T cells from T cell receptor transgenic mice. J. Exp. Med. 176, 1091-1098 (1992).
108. H2 cytokine responses. Nature 362, 246-248 (1993).
109. H2 responses even in the combined absence of IL-5, IL-9, and IL-13. Immunity 17, 7-17 (2002).
110. H2 responses. Curr. Biol. 8, 669-672 (1998).
111. H2 cells in IL-13-deficient mice. Immunity 9, 423-432 (1998).
112. Urban, J. F. Jr et al. IL-13, IL-4Rα, and Stat6 are required for the expulsion of the gastrointestinal nematode parasite Nippostrongylus brasiliensis. Immunity 8, 255-264 (1998).
113. Finkelman, F. D. et al. IL-4 is required to generate and sustain in vivo IgE responses. J. Immunol. 141, 2335-2341 (1988).
114. Kuhn, R., Rajewsky, K. & Muller, W. Generation and analysis of interleukin-4 deficient mice. Science 254, 707-710 (1991).
115. Bonnefoy, J. Y., Gauchat, J. F., Lecoanet-Henchoz, S., Graber, P. & Aubry, J. P. Regulation of human IgE synthesis. Ann. NY Acad. Sci. 796, 59-71 (1996).
116. Emson, C. L., Bell, S. E., Jones, A., Wisden, W. & McKenzie, A. N. Interleukin (IL)-4-independent induction of immunoglobulin (Ig)E, and perturbation of T cell development in transgenic mice expressing IL-13. J. Exp. Med. 188, 399-404 (1998).