Hepatitis C virus-specific T-cell-derived transforming growth factor beta is associated with slow hepatic fibrogenesis

Hepatology. 2012 Dec;56(6):2094-105. doi: 10.1002/hep.25951.

Abstract

Hepatitis C virus (HCV)-specific immune effector responses can cause liver damage in chronic infection. Hepatic stellate cells (HSC) are the main effectors of liver fibrosis. TGFβ, produced by HCV-specific CD8(+) T cells, is a key regulatory cytokine modulating HCV-specific effector T cells. Here we studied TGFβ as well as other factors produced by HCV-specific intrahepatic lymphocytes (IHL) and peripheral blood cells in hepatic inflammation and fibrogenesis. This was a cross-sectional study of two well-defined groups of HCV-infected subjects with slow (≤ 0.1 Metavir units/year, n = 13) or rapid (n = 6) liver fibrosis progression. HCV-specific T-cell responses were studied using interferon-gamma (IFNγ)-ELISpot ±monoclonal antibodies (mAbs) blocking regulatory cytokines, along with multiplex, enzyme-linked immunosorbent assay (ELISA) and multiparameter fluorescence-activated cell sorting (FACS). The effects of IHL stimulated with HCV-core peptides on HSC expression of profibrotic and fibrolytic genes were determined. Blocking regulatory cytokines significantly raised detection of HCV-specific effector (IFNγ) responses only in slow fibrosis progressors, both in the periphery (P = 0.003) and liver (P = 0.01). Regulatory cytokine blockade revealed HCV-specific IFNγ responses strongly correlated with HCV-specific TGFβ, measured before blockade (R = 0.84, P = 0.0003), with only a trend to correlation with HCV-specific IL-10. HCV-specific TGFβ was produced by CD8 and CD4 T cells. HCV-specific TGFβ, not interleukin (IL)-10, inversely correlated with liver inflammation (R = -0.63, P = 0.008) and, unexpectedly, fibrosis (R = -0.46, P = 0.05). In addition, supernatants from HCV-stimulated IHL of slow progressors specifically increased fibrolytic gene expression in HSC and treatment with anti-TGFβ mAb abrogated such expression.

Conclusion: Although TGFβ is considered a major profibrogenic cytokine, local production of TGFβ by HCV-specific T cells appeared to have a protective role in HCV-infected liver, together with other T-cell-derived factors, ameliorating HCV liver disease progression.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Adult
  • Aged
  • CD8-Positive T-Lymphocytes / immunology
  • CD8-Positive T-Lymphocytes / metabolism*
  • Collagen Type I / genetics
  • Collagen Type I, alpha 1 Chain
  • Cross-Sectional Studies
  • Disease Progression
  • Female
  • Gene Expression
  • Hepacivirus / immunology*
  • Hepatic Stellate Cells / metabolism*
  • Hepatitis C, Chronic / immunology
  • Hepatitis C, Chronic / metabolism*
  • Hepatitis C, Chronic / pathology
  • Humans
  • Interferon-gamma / metabolism
  • Interleukin-10 / metabolism
  • Liver / immunology
  • Liver / metabolism
  • Liver Cirrhosis / immunology*
  • Liver Cirrhosis / metabolism
  • Liver Cirrhosis / pathology
  • Male
  • Matrix Metalloproteinase 1 / genetics
  • Middle Aged
  • T-Lymphocytes, Regulatory / immunology
  • T-Lymphocytes, Regulatory / metabolism*
  • Transforming Growth Factor beta / metabolism*
  • Viral Core Proteins / immunology

Substances

  • Collagen Type I
  • Collagen Type I, alpha 1 Chain
  • Transforming Growth Factor beta
  • Viral Core Proteins
  • Interleukin-10
  • Interferon-gamma
  • Matrix Metalloproteinase 1