Effects and regulation of autoreactive CD8+ T cells in a transgenic mouse model of autoimmune hepatitis

Gastroenterology. 2010 Sep;139(3):975-86, 986.e1-3. doi: 10.1053/j.gastro.2010.05.075. Epub 2010 Jun 2.

Abstract

Background & aims: Autoimmune hepatitis (AIH) is a chronic inflammatory liver disease of unknown etiology. Autoreactive T cells are thought to mediate liver injury, but the pathogenesis of AIH is poorly understood because of the lack of suitable animal models. We established a mouse model to investigate liver-specific T-cell responses and assess the effects and regulation of autoreactive CD8(+) T cells in the pathogenesis of AIH.

Methods: We generated transgenic mice expressing the influenza virus hemagglutinin (HA) autoantigen under control of mouse albumin regulatory elements and alpha-fetoprotein enhancers (Alb) specifically in the liver (Alb-HA mice); they were crossed with mice that express a specific T-cell receptor (TCR) (CL4-TCR). CL4-TCR transgenic CD8(+) T cells were also adoptively transferred into Alb-HA mice. We investigated immunologic mechanisms of CD8(+) T cell-induced liver damage and of counteracting peripheral tolerance.

Results: The double-transgenic mice (Alb-HA/CL4-TCR) spontaneously developed chronic, autoimmune-mediated hepatitis, characterized by necroinflammatory lesions, hepatic fibrosis, and increased levels of aminotransferase; these features resembled those of AIH. Interestingly, most liver-infiltrating, HA-specific CD8(+) T cells had an anergic phenotype; regulatory CD4(+)CD25(+)Foxp3(+) T cells accumulated in the inflamed liver.

Conclusions: The continuous development of a few, HA-specific CD8(+) effector T cells is sufficient to induce chronic hepatitis. Peripheral tolerance mechanisms such as induction of T-cell anergy and accumulation of regulatory CD4(+)CD25(+)Foxp3(+) T cells protect the liver from severe damage. Our mouse model that spontaneously develops chronic autoimmune-mediated hepatitis provides a new tool to investigate autoantigen-specific T-cell responses and regulatory mechanisms involved in the prevention and pathogenesis of AIH.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adoptive Transfer
  • Albumins / genetics
  • Animals
  • Autoantigens / genetics
  • Autoantigens / immunology
  • Autoimmunity*
  • CD8-Positive T-Lymphocytes / immunology*
  • CD8-Positive T-Lymphocytes / transplantation
  • Chronic Disease
  • Disease Models, Animal
  • Female
  • Forkhead Transcription Factors / metabolism
  • Genotype
  • Hemagglutinin Glycoproteins, Influenza Virus / genetics
  • Hepatitis, Autoimmune / genetics
  • Hepatitis, Autoimmune / immunology*
  • Hepatitis, Autoimmune / pathology
  • Hepatitis, Autoimmune / prevention & control
  • Immune Tolerance
  • Liver / immunology*
  • Liver / pathology
  • Male
  • Mice
  • Mice, Inbred BALB C
  • Mice, Transgenic
  • Phenotype
  • Receptors, Antigen, T-Cell / genetics
  • Sex Factors
  • T-Lymphocytes, Regulatory / immunology
  • Thymus Gland / immunology
  • Time Factors
  • alpha-Fetoproteins / genetics

Substances

  • Albumins
  • Autoantigens
  • FOXP3 protein, human
  • Forkhead Transcription Factors
  • Hemagglutinin Glycoproteins, Influenza Virus
  • Receptors, Antigen, T-Cell
  • alpha-Fetoproteins