Inhibitory molecules that regulate expansion and restoration of HCV-specific CD4+ T cells in patients with chronic infection

Gastroenterology. 2011 Oct;141(4):1422-31, 1431.e1-6. doi: 10.1053/j.gastro.2011.07.004. Epub 2011 Jul 18.

Abstract

Background & aims: Inhibitory receptors such as programmed death 1 (PD-1) and cytotoxic T lymphocyte-associated antigen (CTLA)-4 mediate CD8+ T-cell exhaustion during chronic viral infection, but little is known about roles in dysfunction of CD4+ T cells.

Methods: We investigated the functions of inhibitory molecules on hepatitis C virus (HCV)-, influenza-, and Epstein-Barr virus (EBV)-specific CD4+ T cells in patients with chronic infections compared with patients with resolved HCV infection and healthy donors. Expression of PD-1, CTLA-4, CD305, and CD200R were analyzed on HCV-specific CD4+ T cells, isolated from peripheral blood using major histocompatibility complex class II tetramers. We investigated the effects of in vitro inhibition of various inhibitory pathways on proliferation and cytokine production by CD4+ T cells, and we compared these effects with those from inhibition of interleukin (IL)-10 and transforming growth factor (TGF)-β1.

Results: PD-1 and CTLA-4 were up-regulated on virus-specific CD4+ T cells from patients with chronic HCV infections. PD-1 expression was lower on influenza- than on HCV-specific CD4+ T cells from subjects with chronic HCV infection, whereas CTLA-4 was expressed at similar levels, independent of their specificity. CD305 and CD200R were up-regulated in HCV resolvers. Blockade of PD-L1/2, IL-10, and TGF-β1 increased expansion of CD4+ T cells in patients with chronic HCV, whereas inhibition of IL-10 and TGF-β1 was most effective in restoring HCV-specific production of interferon gamma, IL-2, and tumor necrosis factor α.

Conclusions: We characterized expression of inhibitory molecules on HCV-, influenza-, and EBV-specific CD4+ T cells and the effects of in vitro blockade on CD4+ T-cell expansion and cytokine production. Inhibition of PD-1, IL-10, and TGF-β1 is most efficient in restoration of HCV-specific CD4+ T cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Antibodies, Neutralizing
  • Antigens, CD / immunology
  • Antigens, CD / metabolism*
  • Antigens, Surface / metabolism
  • CD4-Positive T-Lymphocytes / immunology*
  • CD4-Positive T-Lymphocytes / virology
  • CTLA-4 Antigen / metabolism
  • Case-Control Studies
  • Cell Proliferation*
  • Cells, Cultured
  • Female
  • Deutschland
  • Hepacivirus / genetics
  • Hepacivirus / immunology*
  • Hepatitis C, Chronic / diagnosis
  • Hepatitis C, Chronic / immunology*
  • Herpesvirus 4, Human / immunology
  • Humans
  • Interferon-gamma / metabolism
  • Interleukin-10 / immunology
  • Interleukin-10 / metabolism
  • Interleukin-2 / metabolism
  • Lymphocyte Activation*
  • Male
  • Middle Aged
  • Orexin Receptors
  • Orthomyxoviridae / immunology
  • Programmed Cell Death 1 Receptor / metabolism
  • RNA, Viral / blood
  • Receptors, Cell Surface / metabolism
  • Transforming Growth Factor beta1 / immunology
  • Transforming Growth Factor beta1 / metabolism
  • Tumor Necrosis Factor-alpha / metabolism
  • Viral Load

Substances

  • Antibodies, Neutralizing
  • Antigens, CD
  • Antigens, Surface
  • CD200R1 protein, human
  • CTLA-4 Antigen
  • IL10 protein, human
  • IL2 protein, human
  • Interleukin-2
  • Orexin Receptors
  • PDCD1 protein, human
  • Programmed Cell Death 1 Receptor
  • RNA, Viral
  • Receptors, Cell Surface
  • TGFB1 protein, human
  • Transforming Growth Factor beta1
  • Tumor Necrosis Factor-alpha
  • Interleukin-10
  • Interferon-gamma