Antigen Presentation and T-Cell Activation Are Critical for RBP4-Induced Insulin Resistance

Diabetes. 2016 May;65(5):1317-27. doi: 10.2337/db15-1696. Epub 2016 Mar 2.

Abstract

Adipose tissue (AT) inflammation contributes to impaired insulin action, which is a major cause of type 2 diabetes. RBP4 is an adipocyte- and liver-derived protein with an important role in insulin resistance, metabolic syndrome, and AT inflammation. RBP4 elevation causes AT inflammation by activating innate immunity, which elicits an adaptive immune response. RBP4-overexpressing mice (RBP4-Ox) are insulin resistant and glucose intolerant and have increased AT macrophages and T-helper 1 cells. We show that high-fat diet-fed RBP4(-/-) mice have reduced AT inflammation and improved insulin sensitivity versus wild type. We also elucidate the mechanism for RBP4-induced macrophage antigen presentation and subsequent T-cell activation. In RBP4-Ox, AT macrophages display enhanced c-Jun N-terminal kinase, extracellular signal-related kinase, and p38 phosphorylation. Inhibition of these pathways and of NF-κB reduces activation of macrophages and CD4 T cells. MyD88 is an adaptor protein involved in proinflammatory signaling. In macrophages from MyD88(-/-) mice, RBP4 fails to stimulate secretion of tumor necrosis factor, IL-12, and IL-6 and CD4 T-cell activation. In vivo blockade of antigen presentation by treating RBP4-Ox mice with CTLA4-Ig, which blocks costimulation of T cells, is sufficient to reduce AT inflammation and improve insulin resistance. Thus, MyD88 and downstream mitogen-activated protein kinase and NF-κB pathways are necessary for RBP4-induced macrophage antigen presentation and subsequent T-cell activation. Also, blocking antigen presentation with CTLA4-Ig improves RBP4-induced insulin resistance and macrophage-induced T-cell activation.

Publication types

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

MeSH terms

  • Adaptive Immunity*
  • Adipose Tissue / immunology
  • Adipose Tissue / metabolism
  • Adipose Tissue / pathology
  • Animals
  • Antigen Presentation*
  • Antigen-Presenting Cells / immunology
  • Antigen-Presenting Cells / metabolism
  • Antigen-Presenting Cells / pathology
  • Bone Marrow Cells / immunology
  • Bone Marrow Cells / metabolism
  • Bone Marrow Cells / pathology
  • CD4-Positive T-Lymphocytes / immunology*
  • CD4-Positive T-Lymphocytes / metabolism
  • CD4-Positive T-Lymphocytes / pathology
  • Cells, Cultured
  • Coculture Techniques
  • Diet, High-Fat / adverse effects
  • Glucose Intolerance / etiology
  • Glucose Intolerance / immunology
  • Glucose Intolerance / metabolism
  • Glucose Intolerance / pathology
  • Heterozygote
  • Insulin Resistance*
  • Lymphocyte Activation*
  • Macrophages / immunology
  • Macrophages / metabolism
  • Macrophages / pathology
  • Male
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Myeloid Differentiation Factor 88 / genetics
  • Myeloid Differentiation Factor 88 / metabolism
  • Obesity / etiology
  • Obesity / immunology*
  • Obesity / metabolism
  • Obesity / pathology
  • Retinol-Binding Proteins, Plasma / genetics
  • Retinol-Binding Proteins, Plasma / metabolism*
  • Spleen / immunology
  • Spleen / metabolism
  • Spleen / pathology

Substances

  • Myd88 protein, mouse
  • Myeloid Differentiation Factor 88
  • Rbp4 protein, mouse
  • Retinol-Binding Proteins, Plasma