Abstract
Murine monoclonal IgE interacts with B cells of BALB/c mouse spleen with greater efficiency in the presence of its specific antigen. Complexes of anti-DNP IgE and DNP-OVA not only resist elution from B lymphocytes by acid but have a substantially longer dissociation half- time when compared with monomeric IgE (440 vs. 8 min, respectively). Further, these IgE-antigen complexes induce Fc epsilon R expression in lymphoid cells more efficiently than IgE alone. Maximum levels of B cell Fc epsilon R were observed after a 24 h incubation with 1 microgram/ml IgE in the presence of 1 microgram/ml DNP-OVA, while 30 micrograms/ml monomeric IgE was needed to elicit a similar increase of Fc epsilon R expression. Most importantly, overnight incubation of B cell-enriched BALB/c spleen cells with IgE-antigen complexes resulted in an augmented membrane expression of class II MHC antigens. B cell surface expression of both I-A and I-E antigens responded to a comparable level after incubation with IgE-antigen complexes but did not occur in response to either IgE or antigen alone. The enhanced sIa expression occurred in parallel to IgE-antigen concentrations that gave rise to Fc epsilon R hyperexpression. Moreover, double staining for Fc epsilon R and surface Ia antigen shows that B cells exhibiting the highest density of Fc epsilon R also demonstrated the most surface I-A, suggesting that B lymphocytes are autonomous in their response to IgE- antigen complexes. Changes in class I MHC or sIgM were not observed after overnight incubation with IgE and antigen. These results demonstrate the importance of IgE-antigen complexes for intercellular signaling and further suggest that the IgE system plays a broader role in immune response than it has generally been credited.
Full Text
The Full Text of this article is available as a PDF (1.3 MB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Bonnefoy J. Y., Guillot O., Spits H., Blanchard D., Ishizaka K., Banchereau J. The low-affinity receptor for IgE (CD23) on B lymphocytes is spatially associated with HLA-DR antigens. J Exp Med. 1988 Jan 1;167(1):57–72. doi: 10.1084/jem.167.1.57. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Brown J. C., De Jesus D. G., Holborow E. J., Harris G. Lymphocyte-mediated transport of aggregated human gamma-globulin into germinal centre areas of normal mouse spleen. Nature. 1970 Oct 24;228(5269):367–369. doi: 10.1038/228367a0. [DOI] [PubMed] [Google Scholar]
- Cambier J. C., Monroe J. G. B cell activation. V. Differentiation signaling of B cell membrane depolarization, increased I-A expression, G0 to G1 transition, and thymidine uptake by anti-IgM and anti-IgD antibodies. J Immunol. 1984 Aug;133(2):576–581. [PubMed] [Google Scholar]
- Capron M., Capron A., Dessaint J. P., Torpier G., Johansson S. G., Prin L. Fc receptors for IgE on human and rat eosinophils. J Immunol. 1981 Jun;126(6):2087–2092. [PubMed] [Google Scholar]
- Chen S. S., Bohn J. W., Liu F. T., Katz D. H. Murine lymphocytes expressing Fc receptors for IgE (FcR epsilon). I. Conditions for inducing FcR epsilon + lymphocytes and inhibition of the inductive events by suppressive factor of allergy (SFA). J Immunol. 1981 Jul;127(1):166–173. [PubMed] [Google Scholar]
- Conrad D. H., Peterson L. H. The murine lymphocyte receptor for IgE. I. Isolation and characterization of the murine B cell Fc epsilon receptor and comparison with Fc epsilon receptors from rat and human. J Immunol. 1984 Feb;132(2):796–803. [PubMed] [Google Scholar]
- Conrad D. H., Waldschmidt T. J., Lee W. T., Rao M., Keegan A. D., Noelle R. J., Lynch R. G., Kehry M. R. Effect of B cell stimulatory factor-1 (interleukin 4) on Fc epsilon and Fc gamma receptor expression on murine B lymphocytes and B cell lines. J Immunol. 1987 Oct 1;139(7):2290–2296. [PubMed] [Google Scholar]
- Daeron M., Ishizaka K. Induction of Fc epsilon receptors on mouse macrophages and lymphocytes by homologous IgE. J Immunol. 1986 Mar 1;136(5):1612–1619. [PubMed] [Google Scholar]
- Defranco A. L., Raveche E. S., Asofsky R., Paul W. E. Frequency of B lymphocytes responsive to anti-immunoglobulin. J Exp Med. 1982 May 1;155(5):1523–1536. doi: 10.1084/jem.155.5.1523. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fritsche R., Spiegelberg H. L. Fc receptors for IgE on normal rat lymphocytes. J Immunol. 1978 Aug;121(2):471–478. [PubMed] [Google Scholar]
- Gonzalez-Molina A., Spiegelberg H. L. A subpopulation of normal human peripheral B lymphcytes that bind IgE. J Clin Invest. 1977 Apr;59(4):616–624. doi: 10.1172/JCI108679. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hellström U., Spiegelberg H. L. Characterization of human lymphocytes bearing Fc receptors for IgE isolated from blood and lymphoid organs. Scand J Immunol. 1979;9(1):75–86. doi: 10.1111/j.1365-3083.1979.tb02709.x. [DOI] [PubMed] [Google Scholar]
- Henry C., Chan E. L., Kodlin D. Expression and function of I region products on immunocompetent cells. II. I region products in T-B interaction. J Immunol. 1977 Aug;119(2):744–748. [PubMed] [Google Scholar]
- Hirashima M., Yodoi J., Ishizaka K. Regulatory role of IgE-binding factors from rat T lymphocytes. III. IgE-specific suppressive factor with IgE-binding activity. J Immunol. 1980 Oct;125(4):1442–1448. [PubMed] [Google Scholar]
- Katz D. H., Osborne D. P., Jr The allogeneic effect in inbred mice. II. Establishment of the cellular interactions required for enhancement of antibody production by the graft-versus-host reaction. J Exp Med. 1972 Sep 1;136(3):455–465. doi: 10.1084/jem.136.3.455. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kigoni E. P., Elsas P. P., Lenzi H. L., Dessein A. J. IgE antibody and resistance to infection. II. Effect of IgE suppression on the early and late skin reaction and resistance of rats to Schistosoma mansoni infection. Eur J Immunol. 1986 Jun;16(6):589–595. doi: 10.1002/eji.1830160602. [DOI] [PubMed] [Google Scholar]
- Kulczycki A., Jr, Metzger H. The interaction of IgE with rat basophilic leukemia cells. II. Quantitative aspects of the binding reaction. J Exp Med. 1974 Dec 1;140(6):1676–1695. doi: 10.1084/jem.140.6.1676. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kumagai K., Abo T., Sekizawa T., Sasaki M. Studies of surface immunoglobulins on human B lymphocytes. I. Dissociation of cell-bound immunoglobulins with acid pH or at 37 degrees C. J Immunol. 1975 Oct;115(4):982–987. [PubMed] [Google Scholar]
- Lake P., Clark E. A., Khorshidi M., Sunshine G. H. Production and characterization of cytotoxic Thy-1 antibody-secreting hybrid cell lines. Detection of T cell subsets. Eur J Immunol. 1979 Nov;9(11):875–886. doi: 10.1002/eji.1830091109. [DOI] [PubMed] [Google Scholar]
- Lee W. T., Conrad D. H. Murine B cell hybridomas bearing ligand-inducible Fc receptors for IgE. J Immunol. 1986 Jun 15;136(12):4573–4580. [PubMed] [Google Scholar]
- Lee W. T., Rao M., Conrad D. H. The murine lymphocyte receptor for IgE. IV. The mechanism of ligand-specific receptor upregulation on B cells. J Immunol. 1987 Aug 15;139(4):1191–1198. [PubMed] [Google Scholar]
- Liu F. T., Bohn J. W., Ferry E. L., Yamamoto H., Molinaro C. A., Sherman L. A., Klinman N. R., Katz D. H. Monoclonal dinitrophenyl-specific murine IgE antibody: preparation, isolation, and characterization. J Immunol. 1980 Jun;124(6):2728–2737. [PubMed] [Google Scholar]
- Ly I. A., Mishell R. I. Separation of mouse spleen cells by passage through columns of sephadex G-10. J Immunol Methods. 1974 Aug;5(3):239–247. doi: 10.1016/0022-1759(74)90108-2. [DOI] [PubMed] [Google Scholar]
- Marcelletti J. F., Katz D. H. FcR epsilon+ lymphocytes and regulation of the IgE antibody system. I. A new class of molecules, termed IgE-induced regulants (EIR), which modulate FcR epsilon expression by lymphocytes. J Immunol. 1984 Dec;133(6):2821–2828. [PubMed] [Google Scholar]
- Marcelletti J. F., Katz D. H. FcR epsilon+ lymphocytes and regulation of the IgE antibody system. II. FcR epsilon+ B lymphocytes initiate a cascade of cellular and molecular interactions that control FcR epsilon expression and IgE production. J Immunol. 1984 Dec;133(6):2829–2836. [PubMed] [Google Scholar]
- Marcelletti J. F., Katz D. H. FcR epsilon+ lymphocytes and regulation of the IgE antibody system. IV. Delineation of target cells and mechanisms of action of SFA and EFA in inhibiting in vitro induction of FcR epsilon expression. J Immunol. 1984 Dec;133(6):2845–2851. [PubMed] [Google Scholar]
- Monroe J. G., Havran W. L., Cambier J. C. Enrichment of viable lymphocytes in defined cycle phases by sorting on the basis of pulse width of axial light extinction. Cytometry. 1982 Jul;3(1):24–27. doi: 10.1002/cyto.990030107. [DOI] [PubMed] [Google Scholar]
- Segal D. M., Hurwitz E. Binding of affinity cross-linked oligomers of IgG to cells bearing Fc receptors. J Immunol. 1977 Apr;118(4):1338–1337. [PubMed] [Google Scholar]
- Spiegelberg H. L., O'Connor R. D., Simon R. A., Mathison D. A. Lymphocytes with immunoglobulin E Fc receptors in patients with atopic disorders. J Clin Invest. 1979 Sep;64(3):714–720. doi: 10.1172/JCI109514. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sterk A. R., Ishizaka T. Binding properties of IgE receptors on normal mouse mast cells. J Immunol. 1982 Feb;128(2):838–843. [PubMed] [Google Scholar]
- Uede T., Sandberg K., Bloom B. R., Ishizaka K. IgE-binding factors from mouse T lymphocytes. I. Formation of IgE-binding factors by stimulation with homologous IgE and interferon. J Immunol. 1983 Feb;130(2):649–654. [PubMed] [Google Scholar]
- Vander-Mallie R., Ishizaka T., Ishizaka K. Lymphocytes bearing Fc receptor for IgE. VIII. Affinity of mouse IgE for Fc epsilon R on Mouse B lymphocytes. J Immunol. 1982 May;128(5):2306–2312. [PubMed] [Google Scholar]
- Virgin H. W., 4th, Wittenberg G. F., Unanue E. R. Immune complex effects on murine macrophages. I. Immune complexes suppress interferon-gamma induction of Ia expression. J Immunol. 1985 Dec;135(6):3735–3743. [PubMed] [Google Scholar]
- Yodoi J., Hirashima M., Ishizaka K. Lymphocytes bearing Fc receptors for IgE. V. Effect of tunicamycin on the formation of IgE-potentiating factor and IgE-suppressive factor by con A-activated lymphocytes. J Immunol. 1981 Mar;126(3):877–882. [PubMed] [Google Scholar]
- Yodoi J., Hirashima M., Ishizaka K. Regulatory role of IgE-binding factors from rat T lymphocytes. II. Glycoprotein nature and source of IgE-potentiating factor. J Immunol. 1980 Oct;125(4):1436–1441. [PubMed] [Google Scholar]
- Yodoi J., Ishizaka K. Lymphocytes bearing Fc receptors for IgE. I. Presence of human and rat T lymphocytes with Fc epsilon receptors. J Immunol. 1979 Jun;122(6):2577–2583. [PubMed] [Google Scholar]
- Yodoi J., Ishizaka K. Lymphocytes bearing receptors for IgE. III. Transition of Fc gamma R(+) cells to Fc epsilon R(4) cells by IgE. J Immunol. 1979 Nov;123(5):2004–2010. [PubMed] [Google Scholar]
- Yodoi J., Ishizaka T., Ishizaka K. Lymphocytes bearing Fc receptors for IgE. II. Induction of Fcepsilon-receptor bearing rat lymphocytes by IgE. J Immunol. 1979 Jul;123(1):455–462. [PubMed] [Google Scholar]
