A novel splenic B1 regulatory cell subset suppresses allergic disease through phosphatidylinositol 3-kinase-Akt pathway activation

J Allergy Clin Immunol. 2016 Oct;138(4):1170-1182.e9. doi: 10.1016/j.jaci.2015.12.1319. Epub 2016 Mar 2.

Abstract

Background: IL-10-producing regulatory B (B10) cells potently suppress allergic diseases, such as contact hypersensitivity (CHS). Splenic B10 cells share overlapping phenotypic markers with CD5+ B1 B cells, CD1dhiCD21+CD23- marginal zone (MZ) B cells, and CD1dhiCD21+CD23+ T2-MZ precursor B cells but do not exclusively belong to either subset.

Objective: In this study we investigated the signaling mechanisms and a novel phenotypic parameter of B10 cells.

Method: We performed microarray analysis comparing IL-10+ and IL-10- B cells. B cell-specific phosphatase and tensin homolog (PTEN)-deficient mice, which exhibit aberrant activation of the phosphatidylinositol 3-kinase (PI3K)-Akt pathway in B cells, were examined.

Results: Microarray analysis revealed that the PI3K-Akt pathway is important for IL-10 production in B cells. PI3K-Akt pathway inhibitors reduced B10 cell numbers in vitro. B10 cell numbers were significantly increased in B cell-specific PTEN-deficient mice. The CHS response was significantly diminished in PTEN-deficient mice. Unexpectedly, splenic B10 cells in these mice were found within the B1 B-cell subset but not within the MZ B-cell subset. In wild-type mice not only MZ B10 cells but also B1-B10 cells were identified in the spleen. In addition, these 2 B10 cell subsets were predominantly found within the CD9+CD80+ B-cell fraction.

Conclusion: A novel splenic B1 regulatory cell subset (B1-B10 cells) was identified. Our findings show that the PI3K-Akt pathway in B cells is critical for B10 cell development and CHS response and that CD9/CD80 coexpression is a novel phenotypic parameter for both MZ-B10 and B1-B10 cells.

Keywords: B cells; B1 B cell; IL-10; Rodent; autoimmunity; marginal zone B cell; phosphatase and tensin homolog; phosphatidylinositol 3-kinase; regulatory B cell.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • B-Lymphocytes / classification
  • B-Lymphocytes / drug effects
  • B-Lymphocytes / immunology*
  • Enzyme Activation / drug effects
  • Enzyme Inhibitors / pharmacology
  • Humans
  • Hypersensitivity / enzymology*
  • Hypersensitivity / immunology
  • Interleukin-10 / metabolism
  • Lymphocyte Subsets / drug effects
  • Lymphocyte Subsets / immunology
  • Mice
  • Microarray Analysis
  • Phosphatidylinositol 3-Kinase / immunology*
  • Proto-Oncogene Proteins c-akt / immunology*
  • Signal Transduction / drug effects
  • Spleen / cytology
  • Spleen / immunology

Substances

  • Enzyme Inhibitors
  • Interleukin-10
  • Phosphatidylinositol 3-Kinase
  • Proto-Oncogene Proteins c-akt