Hepatic overexpression of cAMP-responsive element modulator α induces a regulatory T-cell response in a murine model of chronic liver disease

Gut. 2017 May;66(5):908-919. doi: 10.1136/gutjnl-2015-311119. Epub 2016 Sep 29.

Abstract

Objective: Th17 cells are a subset of CD4+ T-helper cells characterised by interleukin 17 (IL-17) production, a cytokine that plays a crucial role in inflammation-associated diseases. The cyclic AMP-responsive element modulator-α (CREMα) is a central mediator of T-cell pathogenesis, which contributes to increased IL-17 expression in patients with autoimmune disorders. Since an increased Th17 response is associated with a poor prognosis in patients with chronic liver injury, we investigated the relevance of Th17 cells for chronic liver disease (CLD) and hepatocarcinogenesis.

Design: Transgenic mice overexpressing CREMα were crossed with hepatocyte-specific Nemo knockout mice (NemoΔhepa) to generate NemoΔhepa/CREMαTg mice. The impact of CREMαTg on CLD progression was examined. Additionally, soft agar colony formation assays, in vitro studies, adoptive transfer of bone marrow-derived cells (BMDCs) and T cells, and gene arrays in T cells were performed.

Results: 8-week-old NemoΔhepa/CREMαTg mice presented significantly decreased transaminase levels, concomitant with reduced numbers of CD11b+ dendritic cells and CD8+ T cells. CREMαTg overexpression in NemoΔhepa mice was associated with significantly reduced hepatic fibrogenesis and carcinogenesis at 52 weeks. Interestingly, hepatic stellate cell-derived retinoic acid induced a regulatory T-cell (Treg) phenotype in CREMαTg hepatic T cells. Moreover, simultaneous adoptive transfer of BMDCs and T cells from CREMαTg into NemoΔhepa mice ameliorated markers of liver injury and hepatitis.

Conclusions: Our results demonstrate that overexpression of CREMα in T cells changes the inflammatory milieu, attenuating initiation and progression of CLD. Unexpectedly, our study indicates that CREMα transgenic T cells shift chronic inflammation in NemoΔhepa livers towards a protective Treg response.

Keywords: CHRONIC LIVER DISEASE; HEPATOCELLULAR CARCINOMA; LIVER; NUCLEAR FACTOR KAPPA B; T LYMPHOCYTES.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alanine Transaminase / blood
  • Animals
  • Aspartate Aminotransferases / blood
  • CD4-Positive T-Lymphocytes / immunology
  • CD8-Positive T-Lymphocytes
  • Cell Line, Tumor
  • Cell Transformation, Neoplastic
  • Chronic Disease
  • Cyclic AMP Response Element Modulator / genetics*
  • Cyclic AMP Response Element Modulator / metabolism
  • Dendritic Cells / immunology
  • Disease Models, Animal
  • Disease Progression
  • Forkhead Transcription Factors / metabolism
  • Hepatitis / genetics
  • Hepatitis / immunology*
  • Intracellular Signaling Peptides and Proteins / genetics
  • Liver Cirrhosis / immunology
  • Liver Neoplasms / immunology*
  • Lymphocyte Count
  • Mice
  • Mice, Knockout
  • Mice, Transgenic
  • T-Lymphocytes / immunology*
  • T-Lymphocytes / metabolism
  • T-Lymphocytes, Regulatory / immunology
  • Th17 Cells / immunology*

Substances

  • Forkhead Transcription Factors
  • Foxp3 protein, mouse
  • Intracellular Signaling Peptides and Proteins
  • NEMO protein, mouse
  • Cyclic AMP Response Element Modulator
  • Aspartate Aminotransferases
  • Alanine Transaminase