CD8+ T cells regulate immune responses in a murine model of allergen-induced sensitization and airway inflammation

European Journal of Immunology

Volumn 34, Issue 7, 2004, Pages 1817-1827

  Stock, Philippe ^a,b   Kallinich, Tilmann ^b,c   Akbari, Omid ^a   Quarcoo, David ^b   Gerhold, Kerstin ^b   Wahn, Ulrich ^b   Umetsu, Dale T ^a   Hamelmann, Eckard ^b  

^a STANFORD UNIVERSITY   (United States)

^b HUMBOLDT UNIVERSITY   (Germany)

^c ROBERT KOCH INSTITUTE   (Germany)

Author keywords

Allergy; CD8; Inflammation; T lymphocytes; Th1 Th2 cells

Indexed keywords

ALLERGEN; CD8 ANTIGEN; CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 4; INTERLEUKIN 5; ANTIBODY;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTHMA; BRONCHUS; CELL COMPARTMENTALIZATION; CELL FUNCTION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DISEASE MODEL; EOSINOPHIL; FEMALE; IMMUNE RESPONSE; IMMUNITY; IMMUNOREGULATION; INHIBITION KINETICS; LYMPH NODE; LYMPHOCYTE FUNCTION; LYMPHOCYTE PROLIFERATION; LYMPHOCYTIC INFILTRATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; RESPIRATORY TRACT INFLAMMATION; SENSITIZATION; SPLEEN; T LYMPHOCYTE; TH2 CELL; ANIMAL; BAGG ALBINO MOUSE; BLOOD; CD8+ T LYMPHOCYTE; CELL CULTURE; HYPERSENSITIVITY; IMMUNOLOGY; INFLAMMATION; LUNG; PATHOPHYSIOLOGY;

ALLERGENS; ANIMALS; ANTIBODIES; CD8-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; DISEASE MODELS, ANIMAL; FEMALE; HYPERSENSITIVITY; INFLAMMATION; LUNG; MICE; MICE, INBRED BALB C;

EID: 3442889104     PISSN: 00142980     EISSN: None     Source Type: Journal    
DOI: 10.1002/eji.200324623     Document Type: Article

References (43)

1. Lemanske, R. F. Jr. and Busse, W. W., Asthma. Jama 1997. 278: 1855-1873.
2. Azzawi, M., Bradley, B., Jeffery, P. K., Frew, A. J., Wardlaw, A. J., Knowles, G., Assoufi, B., Collins, J. V., Durham, S. and Kay, A. B., Identification of activated T lymphocytes and eosinophils in bronchial biopsies in stable atopic asthma. Am. Pev. Respir. Dis. 1990. 142: 1407-1413.
3. Corrigan, C. J. and Kay, A. B., CD4 T-lymphocyte activation in acute severe asthma. Relationship to disease severity and atopic status. Am. Rev. Respir. Dis. 1990. 141: 970-977.
4. Corrigan, C. J., Hartnell, A. and Kay, A. B., T lymphocyte activation in acute severe asthma. Lancet 1988. 1: 1129-1132.
5. Walker, C., Kaegi, M. K., Braun, P. and Blaser, K., Activated T cells and eosinophilia in bronchoalveolar lavages from subjects with asthma correlated with disease severity. J. Allergy Clin. Immunol. 1991. 88: 935-942.
6. Wills-Karp, M., Luyimbazi, J., Xu, X., Schofield, B., Neben, T. Y., Karp, C. L. and Donaldson, D. D., Interleukin-13: central mediator of allergic asthma. Science 1998. 282: 2258-2261.
7. Coffman, R. L., Seymour, B. W., Lebman, D. A., Hiraki, D. D., Christiansen, J. A., Shrader, B., Cherwinski, H. M., Savelkoul, H. F., Finkelman, F. D., Bond, M. W. et al., The role of helper T cell products in mouse B cell differentiation and isotype regulation. Immunol. Rev. 1988. 102: 5-28.
8. McMenamin, C. and Holt, P. G., The natural immune response to inhaled soluble protein antigens involves major histocompatibility complex (MHC) class I-restricted CD8+ T cell-mediated but MHC class II-restricted CD4+ T cell-dependent immune deviation resulting in selective suppression of immunoglobulin E production. J. Exp. Med. 1993. 178: 889-899.
9. Renz, H., Lack, G., Saloga, J., Schwinzer, R., Bradley, K., Loader, J., Kupfer, A., Larsen, G. L. and Gelfand, E. W., Inhibition of IgE production and normalization of airways responsiveness by sensitized CD8 T cells in a mouse model of allergen-induced sensitization. J. Immunol. 1994. 152: 351-360.
10. Cembrzynska-Nowak, M., Szklarz, E., Ingot, A. D. and Teodorczyk-Injeyan, J. A., Elevated release of tumor necrosis factor-α and interferon-γ by bronchoalveolar leukocytes from patients with bronchial asthma. Am. Rev. Respir Dis. 1993. 147: 291-295.
11. Hansen, G., Berry, G., DeKruyff, R. H. and Umetsu, D. T., Allergen-specific Th1 cells fail to counterbalance Th2 cell-induced airway hyperreactivity but cause severe airway inflammation. J. Clin. Invest. 1999. 103: 175-183.
12. Hansen, G., McIntire, J. J., Yeung, V. P., Berry, G., Thorbecke, G. J., Chen, L., DeKruyff, R. H. and Umetsu, D. T., CD4(+) T helper cells engineered to produce latent TGF-β1 reverse allergen-induced airway hyperreactivity and inflammation. J. Clin. Invest. 2000. 105: 61-70.
13. Thomas, M. J., MacAry, P. A., Noble, A., Askenase, P. W. and Kemeny, D. M., T cytotoxic 1 and T cytotoxic 2 CD8 T cells both inhibit IgE responses. Int. Arch. Allergy Immunol. 2001. 124: 187-189.
14. Hansen, G., Yeung, V. P., Berry, G., Umetsu, D. T. and DeKruyff, R. H., Vaccination with heat-killed Listeria as adjuvant reverses established allergen-induced airway hyperreactivity and inflammation: role of CD8+ T cells and IL-18. J. Immunol. 2000. 164: 223-230.
15. Gilliet, M. and Liu, Y. J., Generation of human CD8 T regulatory cells by CD40 ligand-activated plasmacytoid dendritic cells. J. Exp. Med. 2002. 195: 695-704.
16. Hamelmann, E., Oshiba, A., Paluh, J., Bradley, K., Loader, J., Potter, T. A., Larsen, G. L. and Gelfand, E. W., Requirement for CD8+ T cells in the development of airway hyperresponsiveness in a marine model of airway sensitization. J. Exp. Med. 1996. 183: 1719-1729.
17. Coyle, A. J., Erard, F., Bertrand, C., Walti, S., Pircher, H. and Le Gros, G., Virus-specific CD8+ cells can switch to interleukin 5 production and induce airway eosinophilia. J. Exp. Med. 1995. 181: 1229-1233.
18. Schwarze, J., Makela, M., Cieslewicz, G., Dakhama, A., Lahn, M., Ikemura, T., Joetham, A. and Gelfand, E. W., Transfer of the enhancing effect of respiratory syncytial virus infection on subsequent allergic airway sensitization by T lymphocytes, J. Immunol. 1999. 163: 5729-5734.
19. Croft, M., Carter, L., Swain, S. L. and Dutton, R. W., Generation of polarized antigen-specific CD8 effector populations: reciprocal action of interleukin (IL)-4 and IL-12 in promoting type 2 versus type 1 cytokine profiles. J. Exp. Med. 1994. 180: 1715-1728.
20. Erard, F., Wild, M. T., Garcia-Sanz, J. A. and Le Gros, G., Switch of CD8 T cells to noncytolytic CD8-CD4- cells that make TH2 cytokines and help B cells. Science 1993. 260: 1802-1805.
21. Seder, R. A. and Le Gros, G. G., The functional role of CD8+ T helper type 2 cells. J. Exp. Med. 1995. 181: 5-7.
22. Paganelli, R., Scala, E., Ansotegui, I. J., Ausiello, C. M., Halapi, E., Fanales-Belasio, E., D'Offizi, G., Mezzaroma, I., Pandolfi, F., Fiorilli, M. et al., CD8+ T lymphocytes provide helper activity for IgE synthesis in human immunodeficiency virus-infected patients with hyper-IgE. J. Exp. Med. 1995. 181: 423-428.
23. Maggi, E., Giudizi, M. G., Biagiotti, R., Annunziato, F., Manetti, R., Piccinni, M. P., Parronchi, P., Sampognaro, S., Giannarini, L., Zuccati, G. et al., Th2-like CD8+ T cells showing B cell helper function and reduced cytolytic activity in human immunodeficiency virus type 1 infection. J. Exp. Med. 1994. 180: 489-495.
24. Noble, A., Macary, P. A. and Kemeny, D. M., IFN-γ and IL-4 regulate the growth and differentiation of CD8+ T cells into subpopulations with distinct cytokine profiles. J. Immunol. 1995. 155: 2928-2937.
25. Weninger, W., Crowley, M. A., Manjunath, N. and von Andrian, U. H., Migratory properties of naive, effector, and memory CD8(+) T cells. J. Exp. Med. 2001. 194: 953-966.
26. Kagi, D., Vignaux, F., Ledermann, B., Burki, K., Depraetere, V., Nagata, S., Hengartner, H. and Golstein, P., Fas and perforin pathways as major mechanisms of T cell-mediated cytotoxicity. Science 1994. 265: 528-530.
27. Makela, M. J., Kanehiro, A., Borish, L., Dakhama, A., Loader, J., Joetham, A., Xing, Z., Jordana, M., Larsen, G. L. and Gelfand, E. W., IL-10 is necessary for the expression of airway hyperresponsiveness but not pulmonary inflammation after allergic sensitization. Proc. Natl. Acad. Sci. U S A 2000. 97: 6007-6012.
28. Levings, M. K. and Roncarolo, M. G., T-regulatory 1 cells: a novel subset of CD4 T cells with immunoregulatory properties. J. Allergy Clin. Immunol. 2000. 106: S109-S112.
29. Akdis, C. A., Blesken, T., Akdis, M., Wuthrich, B. and Blaser, K., Role of interleukin 10 in specific immunotherapy. J. Clin. Invest. 1998. 102: 98-106.
30. Oh, J. W., Seroogy, C. M., Meyer, E. H., Akbari, O., Berry, G., Fathman, C. G., Dekruyff, R. H. and Umetsu, D. T., CD4 T-helper cells engineered to produce IL-10 prevent allergen-induced airway hyperreactivity and inflammation. J. Allergy Clin. Immunol. 2002. 110: 460-468.
31. Akbari, O., Freeman, G. J., Meyer, E. H., Greenfield, E. A., Chang, T. T., Sharpe, A. H., Berry, G., DeKruyff, R. H. and Umetsu, D. T., Antigen-specific regulatory T cells develop via the ICOS-ICOS-ligand pathway and inhibit allergen-induced airway hyperreactivity. Nat. Med. 2002. 8: 1024-1032.
32. Seder, R. A., Boulay, J. L., Finkelman, F., Barbier, S., Ben-Sasson, S. Z., Le Gros, G. and Paul, W. E., CD8+ T cells can be primed in vitro to produce IL-4. J. Immunol. 1992. 148: 1652-1656.
33. Masopust, D., Vezys, V., Marzo, A. L. and Lefrancois, L., Preferential localization of effector memory cells in nonlymphoid tissue. Science 2001. 291: 2413-2417.
34. Dhodapkar, M. V., Steinman, R. M., Krasovsky, J., Munz, C. and Bhardwaj, N., Antigen-specific inhibition of effector T cell function in humans after injection of immature dendritic cells. J. Exp. Med. 2001. 193: 233-238.
35. Denis, M., Cormier, Y., Laviolette, M. and Ghadirian, E., T cells in hypersensitivity pneumonitis: effects of in vivo depletion of T cells in a mouse model. Am. J. Respir. Cell Mol. Biol. 1992. 6: 183-189.
36. Curtis, J. L., Byrd, P. K., Warnock, M. L., Beck, J. M. and Kaltraider, H. B., Pulmonary lymphocyte recruitment: depletion of CD8+ T cells does not impair the pulmonary immune response to intratracheal antigen. Am. J. Respir. Cell Mol. Biol. 1993. 9: 90-98.
37. Schuyler, M., Gott, K., Edwards, B. and Nikula, K. J., Experimental hypersensitivity pneumonitis: effect of Thy1.2+ and CD8+ cell depletion. Am. J. Respir. Crit. Care Med. 1995. 151: 1834-1842.
38. Cordell, J. L., Falini, B., Erber, W. N., Ghosh, A. K., Abdulaziz, Z., MacDonald, S., Pulford, K. A., Stein, H. and Mason, D. Y., Immunoenzymatic labeling of monoclonal antibodies using immune complexes of alkaline phosphatase and monoclonal anti-alkaline phosphatase (APAAP complexes). J. Histochem. Cytochem. 1984. 32: 219-229.
39. Holt, P. G., Degebrodt, A., Venaille, T., O'Leary, C., Krska, K., Flexman, J., Farrell, H., Shellam, G., Young, P., Penhale, J. et al., Preparation of interstitial lung cells by enzymatic digestion of tissue slices: preliminary characterization by morphology and performance in functional assays. Immunology 1985. 54: 139-147.
40. Lyons, A. B. and Parish, C. R., Determination of lymphocyte division by flow cytometry. J. Immunol. Methods 1994. 171: 131-137.
41. Assenmacher, M., Schmitz, J. and Radbruch, A., Flow cytometric determination of cytokines in activated murine T helper lymphocytes: expression of interleukin-10 in interferon-gamma and in interleukin-4-expressing cells. Eur. J. Immunol. 1994. 24: 1097-1010.
42. Livak, K. J., Flood, S. J., Marmaro, J., Giusti, W. and Deetz, K., Oligonucleotides with fluorescent dyes at opposite ends provide a quenched probe system useful for detecting PCR product and nucleic acid hybridization. PCR Methods Appl. 1995. 4: 357-362.
43. Hamelmann, E., Schwarze, J., Takeda, K., Oshiba, A., Larsen, G. L., Irvin, C. G. and Gelfand, E. W., Noninvasive measurement of airway responsiveness in allergic mice using barometric plethysmography. Am. J. Respir. Crit. Care Med. 1997. 156: 766-775.