Anti-TNF treatment negatively regulates human CD4+ T-cell activation and maturation in vitro, but does not confer an anergic or suppressive phenotype

Eur J Immunol. 2020 Mar;50(3):445-458. doi: 10.1002/eji.201948190. Epub 2019 Dec 3.

Abstract

TNF-blockade has shown clear therapeutic value in rheumatoid arthritis and other immune-mediated inflammatory diseases, however its mechanism of action is not fully elucidated. We investigated the effects of TNF-blockade on CD4+ T cell activation, maturation, and proliferation, and assessed whether TNF-inhibitors confer regulatory potential to CD4+ T cells. CyTOF and flow cytometry analysis revealed that in vitro treatment of human CD4+ T cells with the anti-TNF monoclonal antibody adalimumab promoted IL-10 expression in CD4+ T cells, whilst decreasing cellular activation. In line with this, analysis of gene expression profiling datasets of anti-TNF-treated IL-17 or IFN-γ-producing CD4+ T cells revealed changes in multiple pathways associated with cell cycle and proliferation. Kinetics experiments showed that anti-TNF treatment led to delayed, rather than impaired T-cell activation and maturation. Whilst anti-TNF-treated CD4+ T cells displayed some hyporesponsiveness upon restimulation, they did not acquire enhanced capacity to suppress T-cell responses or modulate monocyte phenotype. These cells however displayed a reduced ability to induce IL-6 and IL-8 production by synovial fibroblasts. Together, these data indicate that anti-TNF treatment delays human CD4+ T-cell activation, maturation, and proliferation, and this reduced activation state may impair their ability to activate stromal cells.

Keywords: CD4+ T cells; CyTOF; TNF inhibitor; adalimumab; interleukin-10.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adalimumab / pharmacology*
  • Anti-Inflammatory Agents / pharmacology*
  • CD4-Positive T-Lymphocytes / drug effects*
  • CD4-Positive T-Lymphocytes / immunology
  • Cell Differentiation / drug effects*
  • Cell Differentiation / immunology
  • Cell Proliferation / drug effects
  • Cells, Cultured
  • Clonal Anergy / drug effects
  • Clonal Anergy / immunology
  • Humans
  • Lymphocyte Activation / drug effects*
  • Lymphocyte Activation / immunology
  • Phenotype
  • Tumor Necrosis Factor-alpha / antagonists & inhibitors

Substances

  • Anti-Inflammatory Agents
  • Tumor Necrosis Factor-alpha
  • Adalimumab