IL-23 and IL-1β Drive Human Th17 Cell Differentiation and Metabolic Reprogramming in Absence of CD28 Costimulation

Cell Rep. 2018 Mar 6;22(10):2642-2653. doi: 10.1016/j.celrep.2018.02.044.

Abstract

Th17 cells drive autoimmune disease but also control commensal microbes. A common link among antigens from self-proteins or commensal microbiota is relatively low activation of T cell receptor (TCR) and costimulation signaling. Indeed, strong TCR/CD28 stimulation suppressed Th17 cell differentiation from human naive T cells, but not effector/memory cells. CD28 suppressed the classical Th17 transcriptional program, while inducing known Th17 regulators, and acted through an Akt-dependent mechanism. Th17 cells differentiated without CD28 were not anergic: they showed robust proliferation and maintained Th17 cytokine production following restimulation. Interleukin (IL)-23 and IL-1β promoted glucose uptake and increased glycolysis. Although modestly increased compared to CD28 costimulation, glycolysis was necessary to support Th17 differentiation, indicating that cytokine-mediated metabolic shifts were sufficient to obviate the classical requirement for CD28 in Th17 differentiation. Together, these data propose that, in humans, strength of TCR/CD28/Akt activation serves as a rheostat tuning the magnitude of Th17 development driven by IL-23 and IL-1β.

Keywords: CD28; IL-1; IL-17; IL-23; Th17; differentiation; human; metabolism.

Publication types

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

MeSH terms

  • Adult
  • CD28 Antigens / metabolism*
  • Cell Differentiation*
  • Clonal Anergy
  • Gene Expression Profiling
  • Humans
  • Interleukin-1beta / metabolism*
  • Interleukin-23 / metabolism*
  • Lymphocyte Activation / immunology
  • Proto-Oncogene Proteins c-akt / metabolism
  • Receptors, Antigen, T-Cell / metabolism
  • Th17 Cells / cytology*
  • Th17 Cells / metabolism*

Substances

  • CD28 Antigens
  • Interleukin-1beta
  • Interleukin-23
  • Receptors, Antigen, T-Cell
  • Proto-Oncogene Proteins c-akt