A20 regulates lymphocyte adhesion in murine neuroinflammation by restricting endothelial ICOSL expression in the CNS

J Clin Invest. 2023 Dec 15;133(24):e168314. doi: 10.1172/JCI168314.

Abstract

A20 is a ubiquitin-modifying protein that negatively regulates NF-κB signaling. Mutations in A20/TNFAIP3 are associated with a variety of autoimmune diseases, including multiple sclerosis (MS). We found that deletion of A20 in central nervous system (CNS) endothelial cells (ECs) enhances experimental autoimmune encephalomyelitis (EAE), a mouse model of MS. A20ΔCNS-EC mice showed increased numbers of CNS-infiltrating immune cells during neuroinflammation and in the steady state. While the integrity of the blood-brain barrier (BBB) was not impaired, we observed a strong activation of CNS-ECs in these mice, with dramatically increased levels of the adhesion molecules ICAM-1 and VCAM-1. We discovered ICOSL to be expressed by A20-deficient CNS-ECs, which we found to function as adhesion molecules. Silencing of ICOSL in CNS microvascular ECs partly reversed the phenotype of A20ΔCNS-EC mice without reaching statistical significance and delayed the onset of EAE symptoms in WT mice. In addition, blocking of ICOSL on primary mouse brain microvascular ECs impaired the adhesion of T cells in vitro. Taken together, we propose that CNS EC-ICOSL contributes to the firm adhesion of T cells to the BBB, promoting their entry into the CNS and eventually driving neuroinflammation.

Keywords: Autoimmunity; Endothelial cells; Mouse models; Multiple sclerosis; Neuroscience.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Blood-Brain Barrier / metabolism
  • Central Nervous System / metabolism
  • Encephalomyelitis, Autoimmune, Experimental*
  • Endothelial Cells / metabolism
  • Inducible T-Cell Co-Stimulator Ligand / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Multiple Sclerosis / metabolism
  • Neuroinflammatory Diseases* / metabolism
  • T-Lymphocytes / metabolism
  • Tumor Necrosis Factor alpha-Induced Protein 3* / metabolism

Substances

  • Tnfaip3 protein, mouse
  • Icosl protein, mouse
  • Inducible T-Cell Co-Stimulator Ligand
  • Tumor Necrosis Factor alpha-Induced Protein 3