Allergen-directed expression of Fc receptors for IgE (CD23) on human T lymphocytes is modulated by interleukin 4 and interferon-gamma.
T lymphocytes bearing Fc receptors (FcR) for immunoglobulins are known to have immunoglobulin class-specific regulatory functions. Here we report that expression on T cells of the low-affinity FcR for IgE (Fc epsilon RII/CD23) is preferentially induced by stimulation with antigens that cause an IgE response. T cells from eight patients allergic to the hemoglobin of Chironomus thummi thummi mosquito larvae (CHIT I) were analyzed for reactivity with the anti-FcERII/CD23 monoclonal antibody (mAb) M-L25 under various conditions. No Fc epsilon RII/CD23+ T cells were observed among freshly isolated, resting peripheral blood mononuclear cells (PBMC). Stimulation of PBMC with CHIT I, however, induced a marked although transient Fc epsilon RII/CD23 expression on a large portion of the allergen-activated T lymphocytes. It reached a maximum of 37.2 +/- 4.6% Fc epsilon RII/CD23+ T cell blasts on day 5 of culture. The selectivity of this expression became evident when compared to non-allergenic control antigens: after stimulation of PBMC with tetanus toxoid or purified protein derivative from tuberculin a maximum of 4.6% +/- 1.4% and 4.2% +/- 1.1% T cell blasts was found to express Fc epsilon RII/CD23, respectively. Activation by an anti-CD3 mAb was insufficient to induce Fc epsilon RII/CD23 on T cells. The allergen-stimulated Fc epsilon RII/CD23+ T cells exclusively belonged to the CD4+CD29+ helper inducer T cell subset. Using a cDNA probe coding for the B cell Fc epsilon RII/CD23, Northern blot analysis revealed a 1.7-kb Fc epsilon RII/CD23 mRNA in extracts of highly purified allergen-stimulated T cells. It was of the same size as Fc epsilon RII/CD23 mRNA of the lymphoblastoid B cell line WI-L2. Of several cytokines tested [interleukin (IL) 1 to IL 6, interferon-gamma (IFN-gamma), tumor necrosis factor-alpha] only IL 4 and IFN-gamma significantly modified allergen-induced Fc epsilon RII/CD23 expression on T cells. The latter was enhanced nearly twofold in the presence of IL 4, and was almost completely abrogated by IFN-gamma. IL 4, however, could not increase the number of Fc epsilon RII/CD23+ T lymphocytes either alone or in combination with an anti-CD3 mAb. Taken together, the selective induction of Fc epsilon RII/CD23 on T cells by allergen and its inclusion in the regulatory network of cytokines point to an important role of Fc epsilon RII/CD23+ T lymphocytes in the human IgE response.
Prinz
J C
JC
Institute for Immunology, Ludwig-Maximilians-University, Munich, FRG.
Baur
X
X
Mazur
G
G
Rieber
E P
EP
D000485:Allergens / Q000276:immunology*; D000818:Animals; D015703:Antigens, CD / Q000096:biosynthesis*; D000944:Antigens, Differentiation, B-Lymphocyte / Q000096:biosynthesis*; D001685:Biological Factors / Q000502:physiology; D002454:Cell Differentiation / Q000276:immunology; D002683:Chironomidae; D016207:Cytokines; D005786:Gene Expression Regulation / Q000276:immunology; D006454:Hemoglobins / Q000276:immunology; D006801:Humans; D007073:Immunoglobulin E / Q000378:metabolism; D007371:Interferon-gamma / Q000502:physiology*; D015847:Interleukin-4 / Q000502:physiology*; D010641:Phenotype; D014176:Protein Biosynthesis; D012333:RNA, Messenger / Q000096:biosynthesis; D011961:Receptors, Fc / Q000096:biosynthesis*; D017455:Receptors, IgE; D013601:T-Lymphocytes / Q000276:immunology*; D014158:Transcription, Genetic
D000485:Allergens; D015703:Antigens, CD; D000944:Antigens, Differentiation, B-Lymphocyte; D001685:Biological Factors; D016207:Cytokines; D006454:Hemoglobins; D012333:RNA, Messenger; D011961:Receptors, Fc; D017455:Receptors, IgE; D015847:Interleukin-4; D007073:Immunoglobulin E; D007371:Interferon-gamma