Tyrosine kinase 2 modulates splenic B cells through type I IFN and TLR7 signaling

Cell Mol Life Sci. 2024 Apr 29;81(1):199. doi: 10.1007/s00018-024-05234-y.

Abstract

Tyrosine kinase 2 (TYK2) is involved in type I interferon (IFN-I) signaling through IFN receptor 1 (IFNAR1). This signaling pathway is crucial in the early antiviral response and remains incompletely understood on B cells. Therefore, to understand the role of TYK2 in B cells, we studied these cells under homeostatic conditions and following in vitro activation using Tyk2-deficient (Tyk2-/-) mice. Splenic B cell subpopulations were altered in Tyk2-/- compared to wild type (WT) mice. Marginal zone (MZ) cells were decreased and aged B cells (ABC) were increased, whereas follicular (FO) cells remained unchanged. Likewise, there was an imbalance in transitional B cells in juvenile Tyk2-/- mice. RNA sequencing analysis of adult MZ and FO cells isolated from Tyk2-/- and WT mice in homeostasis revealed altered expression of IFN-I and Toll-like receptor 7 (TLR7) signaling pathway genes. Flow cytometry assays corroborated a lower expression of TLR7 in MZ B cells from Tyk2-/- mice. Splenic B cell cultures showed reduced proliferation and differentiation responses after activation with TLR7 ligands in Tyk2-/- compared to WT mice, with a similar response to lipopolysaccharide (LPS) or anti-CD40 + IL-4. IgM, IgG, IL-10 and IL-6 secretion was also decreased in Tyk2-/- B cell cultures. This reduced response of the TLR7 pathway in Tyk2-/- mice was partially restored by IFNα addition. In conclusion, there is a crosstalk between TYK2 and TLR7 mediated by an IFN-I feedback loop, which contributes to the establishment of MZ B cells and to B cell proliferation and differentiation.

Keywords: Aged B cells; Follicular B cells; IFNα; Marginal zone B cells; TYK2-deficient mice; Toll-like receptor 7 (TLR7); Type I IFN; Tyrosine kinase 2 (TYK2); β receptor.

MeSH terms

  • Animals
  • B-Lymphocytes* / immunology
  • B-Lymphocytes* / metabolism
  • Cell Differentiation
  • Cell Proliferation
  • Cells, Cultured
  • Interferon Type I* / metabolism
  • Membrane Glycoproteins / genetics
  • Membrane Glycoproteins / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Signal Transduction*
  • Spleen* / cytology
  • Spleen* / metabolism
  • TYK2 Kinase* / genetics
  • TYK2 Kinase* / metabolism
  • Toll-Like Receptor 7* / genetics
  • Toll-Like Receptor 7* / metabolism

Substances

  • Interferon Type I
  • Membrane Glycoproteins
  • Tlr7 protein, mouse
  • Toll-Like Receptor 7
  • TYK2 Kinase
  • Tyk2 protein, mouse