Ae2a,b-deficient mice develop antimitochondrial antibodies and other features resembling primary biliary cirrhosis

Gastroenterology. 2008 May;134(5):1482-93. doi: 10.1053/j.gastro.2008.02.020. Epub 2008 Feb 14.

Abstract

Background & aims: Cl(-)/HCO(3)(-) anion exchanger 2 (AE2) is involved in intracellular pH (pH(i)) regulation and transepithelial acid-base transport, including secretin-stimulated biliary bicarbonate excretion. AE2 gene expression was found to be reduced in liver biopsy specimens and blood mononuclear cells from patients with primary biliary cirrhosis (PBC), a disease characterized by chronic nonsuppurative cholangitis associated with antimitochondrial antibodies (AMA) and other autoimmune phenomena. In mice with widespread Ae2 gene disruption, we previously reported altered spermiogenesis and reduced gastric acid secretion. We now describe the hepatobiliary and immunologic changes observed in these Ae2(a.b)-deficient mice.

Methods: In this murine model, splenocyte pH(i) and T-cell populations were studied by flow cytometry. CD3-stimulated cytokine secretion was estimated using cytokine arrays. AMA were evaluated by immunoblotting and proteomics. Hepatobiliary changes were assessed by immunohistopathology, flow cytometry, and serum biochemistry. Cholangiocyte gene expression was analyzed by real-time polymerase chain reaction.

Results: Ae2(a,b)(-/-) mice exhibit splenomegaly, elevated pH(i) in splenocytes, increased production of interleukin-12p70 and interferon gamma, expanded CD8(+) T-cell population, and under represented CD4(+)FoxP3(+)/regulatory T cells. Most Ae2(a,b)(-/-) mice tested positively for AMA, showing increased serum levels of immunoglobulin M and G, and liver-specific alkaline phosphatase. About one third of Ae2(a,b)(-/-) mice had extensive portal inflammation with CD8(+) and CD4(+) T lymphocytes surrounding damaged bile ducts. Cholangiocytes isolated from Ae2(a,b)(-/-) mice showed gene expression changes compatible with oxidative stress and increased antigen presentation.

Conclusions: Ae2 deficiency alters pH(i) homeostasis in immunocytes and gene expression profile in cholangiocytes, leading to immunologic and hepatobiliary changes that resemble PBC.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Anion Transport Proteins / deficiency*
  • Anion Transport Proteins / genetics
  • Antiporters / deficiency*
  • Antiporters / genetics
  • Cytokines / metabolism
  • Dihydrolipoyllysine-Residue Acetyltransferase / immunology
  • Disease Progression
  • Electrophoresis, Polyacrylamide Gel
  • Enzyme-Linked Immunosorbent Assay
  • Flow Cytometry
  • Gene Expression*
  • Hydrogen-Ion Concentration
  • Intracellular Fluid / metabolism
  • Liver Cirrhosis, Biliary / complications
  • Liver Cirrhosis, Biliary / immunology*
  • Liver Cirrhosis, Biliary / pathology
  • Liver Cirrhosis, Experimental
  • Mice
  • Mice, Inbred BALB C
  • Mitochondria, Liver / immunology
  • Mitochondrial Proteins / immunology
  • Nerve Tissue Proteins
  • Oxidative Stress
  • Polymerase Chain Reaction
  • RNA / genetics*
  • SLC4A Proteins
  • Spleen / metabolism
  • Spleen / pathology
  • Splenomegaly / etiology
  • Splenomegaly / metabolism
  • Splenomegaly / pathology
  • T-Lymphocytes / immunology*
  • T-Lymphocytes / metabolism

Substances

  • Anion Transport Proteins
  • Antiporters
  • Cytokines
  • Mitochondrial Proteins
  • Nerve Tissue Proteins
  • SLC4A Proteins
  • RNA
  • Dihydrolipoyllysine-Residue Acetyltransferase
  • Dlat protein, mouse