Dysregulation of peritoneal cavity B1a cells and murine primary biliary cholangitis

Oncotarget. 2016 May 10;7(19):26992-7006. doi: 10.18632/oncotarget.8853.

Abstract

Primary biliary cholangitis (PBC) is a chronic autoimmune liver disease with progressive cholestasis and liver fibrosis. Similar to human patients with PBC, p40-/-IL-2Rα-/- mice spontaneously develop severe autoimmune cholangitis. Although there has been considerable work on immune regulation and autoimmunity, there is a relative paucity of work directed at the functional implications of the key peritoneal cavity (PC) B cell subset, coined B1a cells in PBC. We used flow cytometry and high-resolution microarrays to study the qualitative and quantitative characteristics of B cells, particularly B1a cells, in the PC of p40-/-IL-2Rα-/- mice compared to controls. Importantly, B1a cell proliferation was markedly lower as the expression of Ki67 decreased. Meanwhile, the apoptosis level was much higher. These lead to a reduction of B1a cells in the PC of p40-/-IL-2Rα-/- mice compared to controls. In contrast, there was a dramatic increase of CD4+ and CD8+ T cells accompanied by elevated production of IFN-γ. In addition, we found a negative correlation between the frequency of B1a cells and the presence of autoreactive CD8+ T cells in both liver and PC of p40-/-IL-2Rα-/- mice. From a functional perspective, B cells from p40-/-IL-2Rα-/- mice downregulated IL-10 production and CTLA-4 expression, leading to loss of B cell regulatory function. We suggest that the dysfunction of B1a cells in the PC in this murine model of autoimmune cholangitis results in defective regulatory function. This highlights a new potential therapeutic target in PBC.

Keywords: B1a cell; Breg; Immune response; Immunity; Immunology and Microbiology Section; autoimmune cholangitis; dysregulation; peritoneal cavity.

MeSH terms

  • Animals
  • Apoptosis / genetics
  • Apoptosis / immunology
  • Autoimmune Diseases / genetics
  • Autoimmune Diseases / immunology*
  • Autoimmune Diseases / metabolism
  • B-Lymphocyte Subsets / immunology*
  • B-Lymphocyte Subsets / metabolism
  • Humans
  • Interferon-gamma / immunology
  • Interferon-gamma / metabolism
  • Interleukin-12 Subunit p40 / genetics
  • Interleukin-12 Subunit p40 / immunology
  • Interleukin-12 Subunit p40 / metabolism
  • Interleukin-2 Receptor alpha Subunit / genetics
  • Interleukin-2 Receptor alpha Subunit / immunology
  • Interleukin-2 Receptor alpha Subunit / metabolism
  • Liver / immunology*
  • Liver / metabolism
  • Liver / pathology
  • Liver Cirrhosis, Biliary / genetics
  • Liver Cirrhosis, Biliary / immunology*
  • Liver Cirrhosis, Biliary / metabolism
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Peritoneal Cavity / pathology
  • T-Lymphocyte Subsets / immunology
  • T-Lymphocyte Subsets / metabolism
  • Transcriptome / genetics
  • Transcriptome / immunology

Substances

  • Interleukin-12 Subunit p40
  • Interleukin-2 Receptor alpha Subunit
  • Interferon-gamma