JAK1 signaling in dendritic cells promotes peripheral tolerance in autoimmunity through PD-L1-mediated regulatory T cell induction

Cell Rep. 2022 Feb 22;38(8):110420. doi: 10.1016/j.celrep.2022.110420.

Abstract

Dendritic cells (DCs) induce peripheral T cell tolerance, but cell-intrinsic signaling cascades governing their stable tolerogenesis remain poorly defined. Janus Kinase 1 (JAK1) transduces cytokine-receptor signaling, and JAK inhibitors (Jakinibs), including JAK1-specific filgotinib, break inflammatory cycles in autoimmunity. Here, we report in heterogeneous DC populations of multiple secondary lymphoid organs that JAK1 promotes peripheral T cell tolerance during experimental autoimmune encephalomyelitis (EAE). Mice harboring DC-specific JAK1 deletion exhibit elevated peripheral CD4+ T cell expansion, less regulatory T cells (Tregs), and worse EAE outcomes, whereas adoptive DC transfer ameliorates EAE pathogenesis by inducing peripheral Tregs, programmed cell death ligand 1 (PD-L1) dependently. This tolerogenic program is substantially reduced upon the transfer of JAK1-deficient DCs. DC-intrinsic IFN-γ-JAK1-STAT1 signaling induces PD-L1, which is required for DCs to convert CD4+ T cells into Tregs in vitro and attenuated upon JAK1 deficiency and filgotinib treatment. Thus, DC-intrinsic JAK1 promotes peripheral tolerance, suggesting potential unwarranted DC-mediated effects of Jakinibs in autoimmune diseases.

Keywords: JAK1; autoimmunity; dendritic cells; peripheral tolerance; regulatory T cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Autoimmunity
  • B7-H1 Antigen* / immunology
  • B7-H1 Antigen* / metabolism
  • Dendritic Cells / metabolism
  • Encephalomyelitis, Autoimmune, Experimental*
  • Immune Tolerance
  • Janus Kinase 1* / immunology
  • Janus Kinase 1* / metabolism
  • Mice
  • Peripheral Tolerance
  • T-Lymphocytes, Regulatory*

Substances

  • B7-H1 Antigen
  • Cd274 protein, mouse
  • Jak1 protein, mouse
  • Janus Kinase 1