Hepatitis C virus core protein triggers expansion and activation of CD4(+)CD25(+) regulatory T cells in chronic hepatitis C patients

Cell Mol Immunol. 2015 Nov;12(6):743-9. doi: 10.1038/cmi.2014.119. Epub 2014 Dec 22.

Abstract

CD4(+)CD25(+)FoxP3(+) regulatory T cells (Tregs) are increased in patients with chronic hepatitis C, which may contribute to the sustained suppression of hepatitis C virus (HCV)-specific T-cell responses and viral persistence in HCV-infected individuals. We postulated that HCV core protein (HCVc) directly contributes to the expansion of Tregs in HCV-infected patients, and we provide evidence to support this hypothesis in the report. Peripheral blood mononuclear cells (PBMCs) and sera were collected from 87 treatment-naïve chronic HCV-infected patients, CD4(+)CD25(+) Tregs were measured by flow cytometry, and HCV RNA and HCVc levels were detected using qPCR and enzyme-linked immunosorbent assay (ELISA), respectively. CD4(+), CD8(+), CD4(+)CD25(+) and CD4(+)CD25(-) T cells were purified from healthy donors and cultured with recombinant HCVc and Toll-like receptor (TLR) ligands. Flow cytometry was used to analyze cell proliferation, and ELISA was performed to measure cytokine production. In the 87 chronic HCV-infected patients, HCVc showed a significant correlation with HCV RNA and CD4(+)CD25(+) Tregs. Mechanistic studies showed that HCVc, together with anti-CD3 antibody, augmented CD4(+)CD25(+) Treg proliferation, but inhibited CD4(+)CD25(-) T-cell proliferation and IFN-γ production, in a dose-dependent and Treg-dependent manner. Moreover, unlike the TLR3 ligand (poly I:C) and the TLR4 ligand (lipopolysaccharide, LPS), the TLR2 ligand (lipoteichoic acid, LTA) and HCVc both inhibited TCR-induced CD4(+) T-cell proliferation and IFN-γ secretion in a Treg-dependent manner. These data indicate that HCVc, like other TLR2 ligands, triggers CD4(+)CD25(+) Treg activation and expansion to inhibit host immune responses, which may play a critical role in viral persistence in HCV-infected patients.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Aged
  • Antibodies / pharmacology
  • CD3 Complex / genetics
  • CD3 Complex / immunology
  • CD4 Antigens / genetics
  • CD4 Antigens / immunology
  • Cell Proliferation / drug effects
  • Female
  • Gene Expression
  • Hepacivirus / physiology*
  • Hepatitis C, Chronic / genetics
  • Hepatitis C, Chronic / immunology*
  • Host-Pathogen Interactions / immunology*
  • Humans
  • Interferon-gamma / genetics
  • Interferon-gamma / immunology
  • Interleukin-2 Receptor alpha Subunit / genetics
  • Interleukin-2 Receptor alpha Subunit / immunology
  • Lipopolysaccharides / pharmacology
  • Lymphocyte Activation / radiation effects
  • Male
  • Middle Aged
  • Poly I-C / pharmacology
  • Primary Cell Culture
  • T-Lymphocytes, Regulatory / drug effects*
  • T-Lymphocytes, Regulatory / immunology
  • T-Lymphocytes, Regulatory / virology
  • Teichoic Acids / pharmacology
  • Toll-Like Receptor 2 / agonists
  • Toll-Like Receptor 2 / genetics
  • Toll-Like Receptor 2 / immunology
  • Toll-Like Receptor 3 / agonists
  • Toll-Like Receptor 3 / genetics
  • Toll-Like Receptor 3 / immunology
  • Toll-Like Receptor 4 / agonists
  • Toll-Like Receptor 4 / genetics
  • Toll-Like Receptor 4 / immunology
  • Viral Core Proteins / pharmacology*

Substances

  • Antibodies
  • CD3 Complex
  • CD4 Antigens
  • IL2RA protein, human
  • Interleukin-2 Receptor alpha Subunit
  • Lipopolysaccharides
  • TLR2 protein, human
  • TLR3 protein, human
  • TLR4 protein, human
  • Teichoic Acids
  • Toll-Like Receptor 2
  • Toll-Like Receptor 3
  • Toll-Like Receptor 4
  • Viral Core Proteins
  • lipoteichoic acid
  • Interferon-gamma
  • Poly I-C