B Cell Fcγ Receptor IIb Modulates Atherosclerosis in Male and Female Mice by Controlling Adaptive Germinal Center and Innate B-1-Cell Responses

Arterioscler Thromb Vasc Biol. 2019 Jul;39(7):1379-1389. doi: 10.1161/ATVBAHA.118.312272. Epub 2019 May 16.

Abstract

Objective- Investigate the impact of modulating B cell FcγRIIb (Fcγ receptor IIb) expression on atherosclerosis. Approach and Results- Western diet-induced atherosclerosis was assessed in Ldlr-/- or Apoe-/- mice with B cell-specific overexpression of FcγRIIb or with an FcγRIIb promoter mutation that alters FcγRIIb expression in germinal center (GC) B cells. In males, overexpression of FcγRIIb on B cells severely reduced activated, class switched B cell responses, as indicated by reductions in GC B cells, plasma cells, and serum IgG but not IgM antibodies. Male mice overexpressing FcγRIIb developed less atherosclerosis, suggesting a pathogenic role for GC B cell IgG responses. In support of this hypothesis, male mice with a promoter polymorphism-driven reduction in FcγRIIb on GC B cells but not plasma cells have a converse phenotype of enhanced GC responses and IgG2c antibodies and enhanced atherosclerosis. IgG2c significantly enhanced TNF (tumor necrosis factor) secretion by CD11b+ CD11c+ cells expressing the high-affinity receptor FcγRIV. In females, overexpression of FcγRIIb on B cells not only reduced GC B cell responses but also substantially reduced B-1 cells and IgM antibodies, which translated into acceleration of atherosclerosis. Promoter-driven reduction in FcγRIIb did not alter GC B cell responses in females and, therefore, had no impact on atherosclerosis. Conclusions- B cell FcγRIIb differentially alters proatherogenic adaptive GC B cell and atheroprotective innate B-1 responses in male and female mice fed a western diet. Our results highlight the importance of a better understanding and ability to selectively target B cell responses in future immunotherapeutic approaches against human cardiovascular disease. Visual Overview- An online visual overview is available for this article.

Keywords: atherosclerosis; cardiovascular diseases; germinal center; inflammation; plasma cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Apolipoproteins E / physiology
  • Atherosclerosis / immunology*
  • B-Lymphocytes / immunology*
  • Female
  • Germinal Center / immunology*
  • Immunity, Innate
  • Immunoglobulin M / biosynthesis
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Receptors, IgG / physiology*
  • Tumor Necrosis Factor-alpha / biosynthesis

Substances

  • Apolipoproteins E
  • Fc gamma receptor IIB
  • Immunoglobulin M
  • Receptors, IgG
  • Tumor Necrosis Factor-alpha