Transgenic expression of insulin receptor substrate 2 in murine B cells alters the cell density-dependence of IgE production in vitro and enhances IgE production in vivo

J Immunol. 2004 Mar 1;172(5):2803-10. doi: 10.4049/jimmunol.172.5.2803.

Abstract

Previous studies have shown that insulin receptor substrate (IRS)1 and IRS2 mediate proliferative and antiapoptotic signaling through the IL-4R in 32D cells; however their role in regulating normal B cell responses is not clear. To investigate the role of IRS2 in normal B cell function, we developed IRS2 transgenic (Tg) mice on the C57BL/6 background. Western blot analysis revealed a 2-fold elevation in IRS2 protein levels in Tg(+) mice compared with littermate controls and a 3-fold increase in basal tyrosine phosphorylated IRS2 in the absence of IL-4 stimulation. IL-4-induced tyrosine phosphorylation of IRS2 was elevated in Tg(+) B cells, whereas IL-4-induced phosphorylation of STAT6 was similar between Tg(+) and Tg(-) B cells. Tg expression of IRS2 had little effect on IL-4-mediated proliferation and no effect on protection from apoptosis. However, production of IgE and IgG1 by Tg(+) B cells using standard in vitro conditions was diminished 50-60%. Because Ig production in vitro is known to be highly cell concentration-dependent, we performed experiments at different cell concentrations. Interestingly, at very low B cell concentrations (1000-5000 B cells/well), IgE and IgG1 production by Tg(+) B cells was greater than that of controls, whereas at higher cell concentrations (10,000-20,000 cells/well) Ig production by Tg(+) B cells was less than controls. Furthermore, in vivo immunization with OVA-alum or goat anti-IgD resulted in elevated serum IgE levels in the Tg(+) mice. These results indicate that overexpression of IRS2 alters the B cell intrinsic density-dependence of IgE and IgG1 production in vitro and enhances IgE responses in vivo.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Adjuvants, Immunologic / biosynthesis
  • Adjuvants, Immunologic / genetics
  • Adjuvants, Immunologic / physiology*
  • Animals
  • B-Lymphocyte Subsets / cytology
  • B-Lymphocyte Subsets / immunology*
  • B-Lymphocyte Subsets / metabolism*
  • Cell Line
  • Crosses, Genetic
  • Female
  • Gene Expression Regulation / immunology*
  • Humans
  • Immunoglobulin E / biosynthesis*
  • Immunoglobulin E / blood
  • Immunoglobulin G / biosynthesis
  • Insulin Receptor Substrate Proteins
  • Interleukin-4 / pharmacology
  • Intracellular Signaling Peptides and Proteins
  • Lymphocyte Count
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Phosphoproteins / biosynthesis*
  • Phosphoproteins / genetics*
  • Phosphoproteins / physiology
  • Receptor, Insulin / physiology
  • STAT6 Transcription Factor
  • Signal Transduction / genetics
  • Signal Transduction / immunology
  • Trans-Activators / physiology
  • Transgenes / immunology*

Substances

  • Adjuvants, Immunologic
  • IRS2 protein, human
  • Immunoglobulin G
  • Insulin Receptor Substrate Proteins
  • Intracellular Signaling Peptides and Proteins
  • Irs2 protein, mouse
  • Phosphoproteins
  • STAT6 Transcription Factor
  • STAT6 protein, human
  • Stat6 protein, mouse
  • Trans-Activators
  • Interleukin-4
  • Immunoglobulin E
  • Receptor, Insulin