Sphingosine-1-Phosphate Receptor Type 4 (S1P4) Is Differentially Regulated in Peritoneal B1 B Cells upon TLR4 Stimulation and Facilitates the Egress of Peritoneal B1a B Cells and Subsequent Accumulation of Splenic IRA B Cells under Inflammatory Conditions

Int J Mol Sci. 2021 Mar 27;22(7):3465. doi: 10.3390/ijms22073465.

Abstract

Background: Gram-negative infections of the peritoneal cavity result in profound modifications of peritoneal B cell populations and induce the migration of peritoneal B cells to distant secondary lymphoid organs. However, mechanisms controlling the egress of peritoneal B cells from the peritoneal cavity and their subsequent trafficking remain incompletely understood. Sphingosine-1-phosphate (S1P)-mediated signaling controls migratory processes in numerous immune cells. The present work investigates the role of S1P-mediated signaling in peritoneal B cell trafficking under inflammatory conditions.

Methods: Differential S1P receptor expression after peritoneal B cell activation was assessed semi‑quantitatively using RT-PCR in vitro. The functional implications of differential S1P1 and S1P4 expression were assessed by transwell migration in vitro, by adoptive peritoneal B cell transfer in a model of sterile lipopolysaccharide (LPS)‑induced peritonitis and in the polymicrobial colon ascendens stent peritonitis (CASP) model.

Results: The two sphingosine-1-phosphate receptors (S1PRs) expressed in peritoneal B cell subsets S1P1 and S1P4 are differentially regulated upon stimulation with the TLR4 agonist LPS, but not upon PMA/ionomycin or B cell receptor (BCR) crosslinking. S1P4 deficiency affects both the trafficking of activated peritoneal B cells to secondary lymphoid organs and the positioning of these cells within the functional compartments of the targeted organ. S1P4 deficiency in LPS-activated peritoneal B cells results in significantly reduced numbers of splenic innate response activator B cells.

Conclusions: The S1P-S1PR system is implicated in the trafficking of LPS-activated peritoneal B cells. Given the protective role of peritoneal B1a B cells in peritoneal sepsis, further experiments to investigate the impact of S1P4-mediated signaling on the severity and mortality of peritoneal sepsis are warranted.

Keywords: abdominal sepsis; innate response activator B cells (IRA B cells); lymphocyte trafficking; peritoneal B cells; sphingosine-1-phosphate.

MeSH terms

  • Animals
  • B-Lymphocytes / metabolism
  • Cell Movement
  • Female
  • Gene Expression Regulation*
  • Immunity, Innate
  • Inflammation*
  • Lipopolysaccharides / chemistry
  • Lipopolysaccharides / metabolism
  • Lymphocyte Activation
  • Mice
  • Mice, Inbred C57BL
  • Peritoneum / immunology
  • Peritoneum / metabolism
  • Peritoneum / pathology
  • Sepsis / physiopathology
  • Signal Transduction
  • Sphingosine-1-Phosphate Receptors / metabolism*
  • Spleen / metabolism*
  • Toll-Like Receptor 4 / metabolism*

Substances

  • Lipopolysaccharides
  • Sphingosine-1-Phosphate Receptors
  • Tlr4 protein, mouse
  • Toll-Like Receptor 4
  • sphingosine-1-phosphate receptor 4, mouse