Stromal interaction molecules 1 and 2 are key regulators of autoreactive T cell activation in murine autoimmune central nervous system inflammation

J Immunol. 2010 Feb 1;184(3):1536-42. doi: 10.4049/jimmunol.0902161. Epub 2009 Dec 18.

Abstract

Calcium (Ca(2+)) signaling in T lymphocytes is essential for a variety of functions, including the regulation of differentiation, gene transcription, and effector functions. A major Ca(2+) entry pathway in nonexcitable cells, including T cells, is store-operated Ca(2+) entry (SOCE), wherein depletion of intracellular Ca(2+) stores upon receptor stimulation causes subsequent influx of extracellular Ca(2+) across the plasma membrane. Stromal interaction molecule (STIM) 1 is the Ca(2+) sensor in the endoplasmic reticulum, which controls this process, whereas the other STIM isoform, STIM2, coregulates SOCE. Although the contribution of STIM molecules and SOCE to T lymphocyte function is well studied in vitro, their significance for immune processes in vivo has remained largely elusive. In this study, we studied T cell function in mice lacking STIM1 or STIM2 in a model of myelin-oligodendrocyte glycoprotein (MOG(35-55))-induced experimental autoimmune encephalomyelitis (EAE). We found that STIM1 deficiency significantly impaired the generation of neuroantigen-specific T cell responses in vivo with reduced Th1/Th17 responses, resulting in complete protection from EAE. Mice lacking STIM2 developed EAE, but the disease course was ameliorated. This was associated with a reduced clinical peak of disease. Deficiency of STIM2 was associated with an overall reduced proliferative capacity of lymphocytes and a reduction of IFN-gamma/IL-17 production by neuroantigen-specific T cells. Neither STIM1 nor STIM2 deficiency altered the phenotype or function of APCs. These findings reveal a crucial role of STIM-dependent pathways for T cell function and activation under autoimmune inflammatory conditions, establishing them as attractive new molecular therapeutic targets for the treatment of inflammatory and autoimmune disorders.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Calcium Channels
  • Calcium Signaling / genetics
  • Calcium Signaling / immunology
  • Drug Delivery Systems
  • Encephalomyelitis, Autoimmune, Experimental / immunology*
  • Encephalomyelitis, Autoimmune, Experimental / mortality
  • Encephalomyelitis, Autoimmune, Experimental / pathology*
  • Encephalomyelitis, Autoimmune, Experimental / prevention & control
  • Female
  • Glycoproteins / administration & dosage
  • Glycoproteins / toxicity
  • Immunity, Innate / genetics
  • Inflammation Mediators / physiology*
  • Lymphocyte Activation / genetics
  • Lymphocyte Activation / immunology*
  • Membrane Glycoproteins / deficiency
  • Membrane Glycoproteins / physiology*
  • Mice
  • Mice, Knockout
  • Mice, Mutant Strains
  • Myelin-Oligodendrocyte Glycoprotein
  • Peptide Fragments / administration & dosage
  • Peptide Fragments / toxicity
  • Protein Isoforms / deficiency
  • Protein Isoforms / genetics
  • Protein Isoforms / physiology
  • Stromal Interaction Molecule 1
  • Stromal Interaction Molecule 2
  • T-Lymphocyte Subsets / immunology*
  • T-Lymphocyte Subsets / metabolism
  • T-Lymphocyte Subsets / pathology

Substances

  • Calcium Channels
  • Glycoproteins
  • Inflammation Mediators
  • Membrane Glycoproteins
  • Myelin-Oligodendrocyte Glycoprotein
  • Peptide Fragments
  • Protein Isoforms
  • Stim1 protein, mouse
  • Stim2 protein, mouse
  • Stromal Interaction Molecule 1
  • Stromal Interaction Molecule 2
  • myelin oligodendrocyte glycoprotein (35-55)