Interferon-gamma-mediated tissue factor expression contributes to T-cell-mediated hepatitis through induction of hypercoagulation in mice

Hepatology. 2013 Jan;57(1):362-72. doi: 10.1002/hep.26027.

Abstract

Concanavalin A (Con A) treatment induces severe hepatitis in mice in a manner dependent on T cells, interferon (IFN)-gamma, and tumor necrosis factor (TNF). Treatment with the anticoagulant heparin protects against hepatitis, despite healthy production of IFN-γ and TNF. Here, we investigated molecular and cellular mechanisms for hypercoagulation-mediated hepatitis. After Con A challenge, liver of wild-type (WT) mice showed prompt induction of Ifnγ and Tnf, followed by messenger RNA expression of tissue factor (TF) and plasminogen activator inhibitor-1 (PAI-1), which initiate blood coagulation and inhibit clot lysis, respectively. Mice developed dense intrahepatic fibrin deposition and massive liver necrosis. In contrast, Ifnγ(-/-) mice and Ifnγ(-/-) Tnf(-/-) mice neither induced Pai1 or Tf nor developed hepatitis. In WT mice TF blockade with an anti-TF monoclonal antibody protected against Con A-induced hepatitis, whereas Pai1(-/-) mice were not protected. Both hepatic macrophages and sinusoidal endothelial cells (ECs) expressed Tf after Con A challenge. Macrophage-depleted WT mice reconstituted with hematopoietic cells, including macrophages deficient in signal transducer and activator of transcription-1 (STAT1) essential for IFN-γ signaling, exhibited substantial reduction of hepatic Tf and of liver injuries. This was also true for macrophage-depleted Stat1(-/-) mice reconstituted with WT macrophages. Exogenous IFN-γ and TNF rendered T-cell-null, Con A-resistant mice deficient in recombination-activating gene 2, highly susceptible to Con A-induced liver injury involving TF.

Conclusions: Collectively, these results strongly suggest that proinflammatory signals elicited by IFN-γ, TNF, and Con A in both hepatic macrophages and sinusoidal ECs are necessary and sufficient for the development of hypercoagulation-mediated hepatitis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Concanavalin A
  • Endothelial Cells / metabolism
  • Fibrin / metabolism
  • Hepatitis, Animal / etiology*
  • Hepatitis, Animal / metabolism
  • Hepatitis, Animal / pathology
  • Interferon-gamma* / metabolism
  • Liver / immunology
  • Liver / metabolism*
  • Liver / pathology
  • Macrophages / metabolism
  • Mice
  • Mice, Knockout
  • Mitogens
  • Necrosis
  • Plasminogen Activator Inhibitor 1 / metabolism
  • STAT1 Transcription Factor / metabolism
  • Signal Transduction
  • T-Lymphocytes / physiology
  • Thrombophilia / chemically induced
  • Thrombophilia / complications*
  • Thromboplastin / metabolism
  • Tumor Necrosis Factor-alpha / metabolism*

Substances

  • Mitogens
  • Plasminogen Activator Inhibitor 1
  • STAT1 Transcription Factor
  • Stat1 protein, mouse
  • Tumor Necrosis Factor-alpha
  • Concanavalin A
  • Interferon-gamma
  • Fibrin
  • Thromboplastin