B-cell linker protein expression contributes to controlling allergic and autoimmune diseases by mediating IL-10 production in regulatory B cells

J Allergy Clin Immunol. 2013 Jun;131(6):1674-82. doi: 10.1016/j.jaci.2013.01.044. Epub 2013 Mar 25.

Abstract

Background: Regulatory B cells that exhibit the cell-surface CD1d(hi)CD5(+) phenotype and produce IL-10 are termed B10 cells. Although B10 cells exert potent suppressive functions in patients with various allergic and autoimmunity disorders, the precise signaling mechanisms required for B10 cell functions remain unknown. B-cell linker protein (BLNK) is an essential component of the B-cell antigen receptor signaling pathway and is required for optimal B-cell development.

Objective: We sought to elucidate the signaling pathways that are responsible for IL-10 production in B10 cells and in vivo mechanisms of how impaired B10 cell functions influence allergic and autoimmune responses.

Method: For in vitro assays, splenic CD1d(hi)CD5(+) B cells from BLNK-deficient (BLNK(-/-)) mice were analyzed for intracellular signaling pathways and cytokine production. Contact hypersensitivity (CHS) and experimental autoimmune encephalomyelitis were examined by using BLNK(-/-) mice.

Results: Although the CD1d(hi)CD5(+) B-cell population was present in BLNK(-/-) mice, IL-10 production was impaired both in vitro and in vivo. BLNK(-/-) mice had exaggerated CHS and experimental autoimmune encephalomyelitis responses, which were normalized by adoptive transfer of splenic CD1d(hi)CD5(+) B cells from wild-type mice. In mice with CHS, BLNK(-/-) mice exhibited decreased B-cell and regulatory T-cell percentages and increased CD8(+) T-cell percentages in the skin and lymph nodes. In vitro BLNK was required for LPS-induced signal transducer and activator of transcription 3 phosphorylation in CD1d(hi)CD5(+) B cells. Finally, secreted IL-10 leads to autocrine expansion of IL-10-producing B cells.

Conclusion: BLNK serves as a critical signaling component for B10 cell function by mediating IL-10 production.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Signal Transducing / deficiency
  • Adaptor Proteins, Signal Transducing / genetics*
  • Animals
  • Antigens, CD1d / metabolism
  • Autocrine Communication
  • Autoimmune Diseases / genetics*
  • Autoimmune Diseases / immunology*
  • B-Lymphocytes, Regulatory / immunology*
  • B-Lymphocytes, Regulatory / metabolism
  • CD5 Antigens / metabolism
  • CD8-Positive T-Lymphocytes / immunology
  • CD8-Positive T-Lymphocytes / metabolism
  • Cytokines / biosynthesis
  • Dermatitis, Contact / genetics
  • Dermatitis, Contact / immunology
  • Disease Models, Animal
  • Encephalomyelitis, Autoimmune, Experimental / genetics
  • Encephalomyelitis, Autoimmune, Experimental / immunology
  • Gene Expression
  • Hypersensitivity / genetics*
  • Hypersensitivity / immunology*
  • Interleukin-10 / biosynthesis*
  • Janus Kinases / metabolism
  • Lipopolysaccharides / immunology
  • Lymphocyte Count
  • Mice
  • Mice, Knockout
  • NF-kappa B / metabolism
  • Phosphorylation
  • STAT3 Transcription Factor / metabolism
  • Signal Transduction

Substances

  • Adaptor Proteins, Signal Transducing
  • Antigens, CD1d
  • B cell linker protein
  • CD5 Antigens
  • Cytokines
  • Lipopolysaccharides
  • NF-kappa B
  • STAT3 Transcription Factor
  • Interleukin-10
  • Janus Kinases