Functions of liver natural killer cells are dependent on the severity of liver inflammation and fibrosis in chronic hepatitis C

PLoS One. 2014 Apr 23;9(4):e95614. doi: 10.1371/journal.pone.0095614. eCollection 2014.

Abstract

During chronic hepatitis C virus (HCV) infection, the role of intra-hepatic (IH) natural killer (NK) cells is still controversial. To clarify their functions, we investigated anti-viral and cytotoxic activity of NK cells in human fresh liver biopsies. We compared the functions of IH-NK cells in HCV-infected and NASH patients in physiological conditions as well as after stimulation using flow cytometric and immunohistochemical analyses. Interestingly, few IH-NK cells produced anti-viral cytokine IFN-γ in HCV-infected patients similarly as in non-infected individuals. Spontaneous degranulation activity was extremely low in peripheral NK cells compared to IH-NK cells, and was significantly higher in IH-NK cells from HCV-infected patients compared to non-infected individuals. Immunohistochemical analysis revealed that perforin granules were polarized at the apical pole of IH-NK cells. The presence of CD107a and perforin in IH-NK cells demonstrated that NK cells exerted a cytolytic activity at the site of infection. Importantly, IH-NK cell functions from HCV-infected patients were inducible by specific exogenous stimulations. Upon ex vivo K562 target cell stimulations, the number of degranulating NK cells was significantly increased in the pool of IH-NK cells compared to circulating NK cells. Interestingly, after stimulation, the frequency of IFN-γ-producing IH-NK cells in HCV-infected patients was significantly higher at early stage of inflammation whereas the spontaneous IH-NK cell degranulation activity was significantly impaired in patients with highest inflammation and fibrosis Metavir scores. Our study highlights that some IH-NK cells in HCV-infected patients are able to produce INF-γ and degranulate and that those two activities depend on liver environment including the severity of liver injury. Thus, we conclude that critical roles of IH-NK cells have to be taken into account in the course of the liver pathogenesis associated to chronic HCV infection.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cell Line
  • Flow Cytometry
  • Hepatitis C, Chronic / immunology*
  • Hepatitis C, Chronic / metabolism
  • Hepatitis C, Chronic / pathology*
  • Humans
  • Immunohistochemistry
  • Interferon-gamma / metabolism
  • Interleukin-12 / metabolism
  • Interleukin-18 / metabolism
  • Killer Cells, Natural / metabolism*
  • Liver / immunology*
  • Liver / metabolism
  • Liver / pathology*
  • Liver Cirrhosis / immunology
  • Liver Cirrhosis / metabolism
  • Liver Cirrhosis / pathology*
  • Prospective Studies

Substances

  • Interleukin-18
  • Interleukin-12
  • Interferon-gamma

Grants and funding

This work was supported by grants from Institut National de la Santé et de la Recherche Médicale (INSERM), the Agence Nationale pour la Recherche sur le Sida (ANRS) n°AO 2009 - 2, CSS7. EF and ZMJ received financial support from Centre National de la Recherche Scientifique (CNRS) and Fundation Finovi; AD from ALPHA VAC of the “Pôle de Compétitivité Lyon Biopole”, and NVC was the recipient of a grant from the Rhône- Alpes Region Cluster 10 “Infectiologie”. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.