Tim-1 is essential for induction and maintenance of IL-10 in regulatory B cells and their regulation of tissue inflammation

J Immunol. 2015 Feb 15;194(4):1602-8. doi: 10.4049/jimmunol.1402632. Epub 2015 Jan 12.

Abstract

T cell Ig and mucin domain (Tim)-1 identifies IL-10-producing regulatory B cells (Bregs). Mice on the C57BL/6 background harboring a loss-of-function Tim-1 mutant showed progressive loss of IL-10 production in B cells and with age developed severe multiorgan tissue inflammation. We demonstrate that Tim-1 expression and signaling in Bregs are required for optimal production of IL-10. B cells with Tim-1 defects have impaired IL-10 production but increased proinflammatory cytokine production, including IL-1 and IL-6. Tim-1-deficient B cells promote Th1 and Th17 responses but inhibit the generation of regulatory T cells (Foxp3(+) and IL-10-producing type 1 regulatory T cells) and enhance the severity of experimental autoimmune encephalomyelitis. Mechanistically, Tim-1 on Bregs is required for apoptotic cell (AC) binding to Bregs and for AC-induced IL-10 production in Bregs. Treatment with ACs reduces the severity of experimental autoimmune encephalomyelitis in hosts with wild-type but not Tim-1-deficient Bregs. Collectively, these findings suggest that in addition to serving as a marker for identifying IL-10-producing Bregs, Tim-1 is also critical for maintaining self-tolerance by regulating IL-10 production in Bregs.

Publication types

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

MeSH terms

  • Animals
  • B-Lymphocytes, Regulatory / immunology*
  • Encephalomyelitis, Autoimmune, Experimental / immunology
  • Flow Cytometry
  • Hepatitis A Virus Cellular Receptor 1
  • Inflammation / immunology*
  • Interleukin-10 / immunology*
  • Lymphocyte Activation / immunology
  • Membrane Proteins / immunology*
  • Mice
  • Mice, Inbred C57BL
  • Mice, Mutant Strains
  • Real-Time Polymerase Chain Reaction
  • Self Tolerance / immunology

Substances

  • Havcr1 protein, mouse
  • Hepatitis A Virus Cellular Receptor 1
  • IL10 protein, mouse
  • Membrane Proteins
  • Interleukin-10