CD40 promotes MHC class II expression on adipose tissue macrophages and regulates adipose tissue CD4+ T cells with obesity

J Leukoc Biol. 2016 Jun;99(6):1107-19. doi: 10.1189/jlb.3A0115-009R. Epub 2015 Dec 11.

Abstract

Obesity activates both innate and adaptive immune responses in adipose tissue, but the mechanisms critical for regulating these responses remain unknown. CD40/CD40L signaling provides bidirectional costimulatory signals between antigen-presenting cells and CD4(+) T cells, and CD40L expression is increased in obese humans. Therefore, we examined the contribution of CD40 to the progression of obesity-induced inflammation in mice. CD40 was highly expressed on adipose tissue macrophages in mice, and CD40/CD40L signaling promoted the expression of antigen-presenting cell markers in adipose tissue macrophages. When fed a high fat diet, Cd40-deficient mice had reduced accumulation of conventional CD4(+) T cells (Tconv: CD3(+)CD4(+)Foxp3(-)) in visceral fat compared with wild-type mice. By contrast, the number of regulatory CD4(+) T cells (Treg: CD3(+)CD4(+)Foxp3(+)) in lean and obese fat was similar between wild-type and knockout mice. Adipose tissue macrophage content and inflammatory gene expression in fat did not differ between obese wild-type and knockout mice; however, major histocompatibility complex class II and CD86 expression on adipose tissue macrophages was reduced in visceral fat from knockout mice. Similar results were observed in chimeric mice with hematopoietic Cd40-deficiency. Nonetheless, neither whole body nor hematopoietic disruption of CD40 ameliorated obesity-induced insulin resistance in mice. In human adipose tissue, CD40 expression was positively correlated with CD80 and CD86 expression in obese patients with type 2 diabetes. These findings indicate that CD40 signaling in adipose tissue macrophages regulates major histocompatibility complex class II and CD86 expression to control the expansion of CD4(+) T cells; however, this is largely dispensable for the development of obesity-induced inflammation and insulin resistance in mice.

Keywords: CD40L; antigen presenting cells (APC); inflammation.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, N.I.H., Extramural

MeSH terms

  • Adipose Tissue / pathology*
  • Adiposity / drug effects
  • Animals
  • Antigen-Presenting Cells / drug effects
  • Antigen-Presenting Cells / metabolism
  • B7-1 Antigen / metabolism
  • B7-2 Antigen / metabolism
  • CD4-Positive T-Lymphocytes / drug effects
  • CD4-Positive T-Lymphocytes / metabolism*
  • CD40 Antigens / metabolism*
  • CD40 Ligand / metabolism
  • Diet, High-Fat
  • Hematopoiesis / drug effects
  • Histocompatibility Antigens Class II / metabolism*
  • Humans
  • Insulin / pharmacology
  • Macrophages / drug effects
  • Macrophages / metabolism*
  • Male
  • Mice, Inbred C57BL
  • Obesity / immunology*
  • Obesity / pathology
  • Omentum / drug effects
  • Omentum / metabolism
  • Omentum / pathology
  • Signal Transduction / drug effects

Substances

  • B7-1 Antigen
  • B7-2 Antigen
  • CD40 Antigens
  • Histocompatibility Antigens Class II
  • Insulin
  • CD40 Ligand