Abstract
Recent studies have found aberrant expression of class II antigens by bronchial epithelial cells (BECs), suggesting that these cells may also be involved in airway mucosal immunity. However, the regulation of class II antigen expression on BECs by cytokines and the functional capacity of such cells bearing class II molecules remain unknown. We investigated the effect of IFN-γ on class II antigen expression by cultured rat BECs, as well as the ability of these cells to present intact protein antigens to specifically sensitized T cells. Although primary BECs did not express class II antigens, IFN-γ readily induced their expression in a dose-dependent manner. More than 85% of the BECs treated with 1000 U/ml of IFN-γ were positive for class II antigens. In addition, when IFN-treated BECs bearing class II molecules were pulsed with ovalbumin (OVA), they significantly stimulated the proliferation of OVA-sensitized T cells, whereas cells that were not treated with IFN-γ but were pulsed with OVA did not do so. Our findings indicate that BECs bearing class II molecules are capable of presenting OVA to OVA-sensitized T cells. These results suggest that various pathological conditions causing the local production of IFN-γ may increase class II antigen expression on BECs, which in turn may modulate the airway mucosal immune response by the presentation of antigens to T cells.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Basham TY, Nickoloff BJ, Merigan TC, Morhenn VB (1984) Recombinant gamma interferon induces HLA-DR expression on cultured human keratinocytes. J Invest Dermatol 83: 88–90
Capsi RR, Roberge FG, Nussenblatt RB (1987) Organ-resident, nonlymphoid cells suppress proliferation of autoimmune T-helper lymphocytes. Science 237: 1029–1032
Churchill L, Chilton FH, Resau JH, Bascom R, Hubbard WC, Proud D (1989) Cyclooxygenase metabolism of endogenous arachidonic acid by cultured human bronchial epithelial cells. Am Rev Respir Dis 140: 449–459
Ebner SA, Stein ME, Minami M, Dorf ME, Stadecker MJ (1987) Murine thyroid follicular epithelial cells can be induced to expression class II (Ia) gene products but fail to present antigenin vitro. Cell Immunol 104: 154–168
Fierz W, Endler B, Reske K, Wekerle H, Fontana A (1985) Astrocytes an antigen-presenting cells. I. Induction of Ia antigen expression on astrocytes by T cells via immune interferon and its effect on antigen presentation. J Immunol 134: 3785–3793
Gaspari AA, Jenkins MK, Katz SI (1988) Class II MHC-bearing keratinocytes induce antigen-specific unresponsiveness in hapten-specific Th1 clones. J Immunol 141: 2216–2220
Glanville AR, Tazelaar HD, Theodore J, Imoto E, Rouse RV, Baldwin JC, Robin DE (1989) The distribution of MHC class I and II antigens on bronchial epithelium. Am Rev Respir Dis 139: 330–334
Hanafusa T, Pujol-Borrell R, Chiovato L, Russell RCG, Doniach D, Bottazzo GF (1983) Aberrant expression of HLA-DR antigen on thyrocytes in Grave’s disease: Relevance for autoimmunity. Lancet 2: 1111–1115
Harbecker RJ, Gegen NW, Struhar D, Manon R (1988) Class II molecules on rat alveolar type II epithelial cells. Cell Immunol 111: 139–147
Holt PG, Degebrodt A, O’Leary C, Krska K, Plozza T (1985) T cell activation by antigen-presenting cells from lung tissue digests: Suppression by endogenous macrophages. Clin Exp Immunol 62: 586–593
Holt PG, Oliver J, Bilyk N, McMenamin C, McMenamin PG, Kraal G, Thepen T (1993) Downregulation of the antigen presenting cell function(s) pulmonary dendritic cells in vivo by resident alveolar macrophages. J Exp Med 177: 397–407
Holt PG, Oliver J, McMenamin C, Schon-Hegrad MA (1992) Studies on the surface phenotype and functions of dendritic cells in parenchymal lung tissue of the rat. Immunology 75: 582–587
Holt PG, Schon-Hegrad MA, Oliver J (1988) MHC class II antigen-bearing dendritic cells in pulmonary tissue of the rat. J Exp Med 167: 262–274
Kalb TH, Chuang MT, Marom Z, Mayer L (1991) Evidence for accessory function by class II MHC antigen-expressing airway epithelial cells. Am J Respir Cell Mol Biol 4: 320–329 137
Koyama S, Rennard SI, Leikauf GD, Robbins RA (1991) Bronchial epithelial cells release monocyte chemotactic activity in response to smoke and endotoxin. J Immunol 147: 972–979
Lampert IA, Suitters AJ, Chrisholm PM (1981) Expression of Ia antigen on epidermal keratinocytes in graft-versus-host disease. Nature 293: 149–150
Londei M, Bottazzo GF, Feldman M (1984) Epithelial cells expressing aberrant MHC class II determinants can present antigen cloned human T cells. Nature 312: 639–641
Markmann J, Lo D, Naji A, Palmiter RD, Brinster RL, Heber-Katz E (1988) Antigen presenting function of class II MHC expressing pancreatic beta cells. Nature 336: 476–479
Matsumoto Y, Ohnori K, Fujiwara M (1992) Immune regulation by brain cells in the central nervous system: Microglia but not astrocytes present myelin basic protein to encephalitogenic T cells underin vivo-mimicking conditions. Immunology 76: 209–216
Mattoli S, Colotta F, Fincato G, Mezzetti M, Mantovani A, Patalano F, Fasoli A (1991) Time course of IL-1 and IL-6 synthesis and release in human bronchial epithelial cell culture exposed to toluene diisocyanate. J Cell Physiol 149: 260–268
Mayer L, Eisenhardt D, Salomon P, Bauer W, Pious R, Piccinini L (1991) Expression of class II molecules on intestinal epithelial cells in humans. Differences between normal and inflammatory bowel disease. Gastroenterology 100: 3–12
Minami M, Ebner SA, Stadecker MJ, Dorf ME (1987) The effects of phorbol ester on alloantigen presentation. J Immunol 138: 393–400
Nakamura H, Yoshimura K, Jaffe AH, Crystal RG (1991) Interleukin-8 gene expression in human bronchial epithelial cells. J Biol Chem 266: 19611–19617
Platzer M, Neufeld DS, Piccinini LA, Davies TF (1987) Induction of rat thyroid cell MHC class II antigen by thyrotropin and γ-interferon. Endocrinology 121: 2087–2092
Poston RN, Chanez P, Lacoste YJ, Litchfield T, Lee TH, Bousquet J (1992) Immunohistochemical characterization of the cellular infiltration in asthmatic bronchi. Am Rev Respir Dis 145: 918–921
Rochester CL, Goodell EM, Stoltenborg JK, Bowers WE (1988) Dendritic cells from rat lung are potent accessory cells. Am Rev Respir Dis 138: 121–128
Rossi GA, Sacco O, Balbi B, Oddera S, Mattioni T, Corte G, Ravazzoni C, Allegra L (1990) Human ciliated bronchial epithelial cells: Expression of the-HLA-DR antigens and the HLA-DR alpha gene, modulation of the HLA-DR antigens by gamma-interferon and antigen-presenting function in the mixed leukocyte reaction. Am J Respir Cell Mol Biol 3: 431–439
Schon-Hegrad MA, Oliver J, McMenamin PG, Holt PG (1991) Studies on the density, distribution, and surface phenotype of intraepithelial class II major histocompatibility complex antigen (Ia)-bearing dendritic cells (DC) in the conducting airways. J Exp Med 173: 1345–1356
Sertl K, Takemura T, Tschachler E, Ferrans VJ, Kaliner MA, Shevach EM (1986) Dendritic cells with antigen-presenting capability reside in airway epithelium, lung parenchyma, and visceral pleura. J Exp Med 163: 436–451
Sigillito RJ, Miller S, Tokuda N, Levy RB (1989) Rat thyroid epithelial cells provide limited accessory function but fail to present allo antigensin vitro.. Regional Immunol 2: 275–289
Simecka JW, Davis IK, Cassell GH (1986) Distribution of Ia antigens and T lymphocytes subpopulations in rat lungs. Immunology 57: 93–98
Smith SM, Lee DKP, Lacy J, Coleman DL (1990) Rat tracheal epithelial cells produce granulocyte/macrophage colony-stimulating factor. Am J Respir Cell Mol Biol 2: 59–68
Tabibzadeh SS, Gerber MA, Satyaswaroop PG (1986) Induction of HLA-DR antigen expression in human endometrial epithelial cellsin vitro by recombinant γ-IFN. Am J Pathol 125: 90–96
Wu R, Smith D (1982) Continuous multiplication of rabbit tracheal epithelial cells in a defined, hormone-supplemented medium. In Vitro 18: 800–812
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Suda, T., Sato, A., Sugiura, W. et al. Induction of MHC class II antigens on rat bronchial epithelial cells by interferon-gamma and its effect on antigen presentation. Lung 173, 127–137 (1995). https://doi.org/10.1007/BF02981472
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF02981472