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.