Opposing Functions of Microglial and Macrophagic TNFR2 in the Pathogenesis of Experimental Autoimmune Encephalomyelitis

Cell Rep. 2017 Jan 3;18(1):198-212. doi: 10.1016/j.celrep.2016.11.083.

Abstract

In multiple sclerosis (MS), soluble tumor necrosis factor (TNF) is detrimental via activation of TNF receptor 1 (TNFR1), whereas transmembrane TNF is beneficial primarily by activating TNF receptor 2 (TNFR2). Here, we investigate the role of TNFR2 in microglia and monocytes/macrophages in experimental autoimmune encephalomyelitis (EAE), a model of MS, by cell-specific gene targeting. We show that TNFR2 ablation in microglia leads to early onset of EAE with increased leukocyte infiltration, T cell activation, and demyelination in the central nervous system (CNS). Conversely, TNFR2 ablation in monocytes/macrophages results in EAE suppression with impaired peripheral T cell activation and reduced CNS T cell infiltration and demyelination. Our work uncovers a dichotomy of function for TNFR2 in myeloid cells, with microglial TNFR2 providing protective signals to contain disease and monocyte/macrophagic TNFR2 driving immune activation and EAE initiation. This must be taken into account when targeting TNFR2 for therapeutic purposes in neuroinflammatory diseases.

Keywords: TNF signaling; cytokines; macrophages; microglia; multiple sclerosis; neuroinflammation; tumor necrosis factor.

Publication types

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

MeSH terms

  • Animals
  • CX3C Chemokine Receptor 1 / metabolism
  • Cell Proliferation
  • Chronic Disease
  • Demyelinating Diseases / genetics
  • Demyelinating Diseases / metabolism
  • Demyelinating Diseases / pathology
  • Encephalomyelitis, Autoimmune, Experimental / etiology*
  • Encephalomyelitis, Autoimmune, Experimental / genetics
  • Encephalomyelitis, Autoimmune, Experimental / metabolism*
  • Encephalomyelitis, Autoimmune, Experimental / pathology
  • Gene Deletion
  • Gene Expression Regulation
  • Homeostasis / genetics
  • Inflammation / pathology
  • Macrophages / metabolism*
  • Mice, Inbred C57BL
  • Microglia / metabolism*
  • Myelin Sheath / metabolism
  • Neuroprotection
  • Phenotype
  • Receptors, Tumor Necrosis Factor, Type I / metabolism
  • Receptors, Tumor Necrosis Factor, Type II / metabolism*
  • Sequence Analysis, RNA
  • Spinal Cord / pathology
  • T-Lymphocytes / cytology
  • T-Lymphocytes / immunology
  • Transcriptome / genetics

Substances

  • CX3C Chemokine Receptor 1
  • Cx3cr1 protein, mouse
  • Receptors, Tumor Necrosis Factor, Type I
  • Receptors, Tumor Necrosis Factor, Type II