Programmed death (PD)-1-deficient mice are extremely sensitive to murine hepatitis virus strain-3 (MHV-3) infection

PLoS Pathog. 2011 Jul;7(7):e1001347. doi: 10.1371/journal.ppat.1001347. Epub 2011 Jul 7.

Abstract

The inhibitory receptor programmed death-1 (PD-1) has the capacity to maintain peripheral tolerance and limit immunopathological damage; however, its precise role in fulminant viral hepatitis (FH) has yet to be described. Here, we investigated the functional mechanisms of PD-1 as related to FH pathogenesis induced by the murine hepatitis virus strain-3 (MHV-3). High levels of PD-1-positive CD4(+), CD8(+) T cells, NK cells and macrophages were observed in liver, spleen, lymph node and thymus tissues following MHV-3 infection. PD-1-deficient mice exhibited significantly higher expression of the effector molecule which initiates fibrinogen deposition, fibrinogen-like protein 2 (FGL2), than did their wild-type (WT) littermates. As a result, more severe tissue damage was produced and mortality rates were higher. Fluorescence double-staining revealed that FGL2 and PD-1 were not co-expressed on the same cells, while quantitative RT-PCR demonstrated that higher levels of IFN-γ and TNF-α mRNA transcription occurred in PD-1-deficient mice in response to MHV-3 infection. Conversely, in vivo blockade of IFN-γ and TNF-α led to efficient inhibition of FGL2 expression, greatly attenuated the development of tissue lesions, and ultimately reduced mortality. Thus, the up-regulation of FGL2 in PD-1-deficient mice was determined to be mediated by IFN-γ and TNF-α. Taken together, our results suggest that PD-1 signaling plays an essential role in decreasing the immunopathological damage induced by MHV-3 and that manipulation of this signal might be a useful strategy for FH immunotherapy.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antibodies, Blocking / pharmacology
  • Disease Models, Animal
  • Disease Progression
  • Fibrinogen / metabolism
  • Hepatitis, Viral, Animal / immunology
  • Hepatitis, Viral, Animal / metabolism
  • Hepatitis, Viral, Animal / mortality
  • Hepatitis, Viral, Animal / pathology*
  • Host-Pathogen Interactions*
  • Interferon-gamma / immunology
  • Interferon-gamma / metabolism
  • Liver / metabolism
  • Liver / pathology
  • Liver / virology
  • Lymphoid Tissue / metabolism
  • Lymphoid Tissue / pathology
  • Lymphoid Tissue / virology
  • Mice
  • Mice, Knockout
  • Murine hepatitis virus / pathogenicity
  • Murine hepatitis virus / physiology*
  • Programmed Cell Death 1 Receptor / physiology*
  • Signal Transduction
  • Survival Rate
  • Tissue Array Analysis
  • Tumor Necrosis Factor-alpha / immunology
  • Tumor Necrosis Factor-alpha / metabolism

Substances

  • Antibodies, Blocking
  • Fgl2 protein, mouse
  • Pdcd1 protein, mouse
  • Programmed Cell Death 1 Receptor
  • Tumor Necrosis Factor-alpha
  • Interferon-gamma
  • Fibrinogen