A hierarchy of affinities between cytokine receptors and the common gamma chain leads to pathway cross-talk

Sci Signal. 2018 Apr 3;11(524):eaal1253. doi: 10.1126/scisignal.aal1253.

Abstract

Cytokines belonging to the common gamma chain (γc) family depend on the shared γc receptor subunit for signaling. We report the existence of a fast, cytokine-induced pathway cross-talk acting at the receptor level, resulting from a limiting amount of γc on the surface of T cells. We found that this limited abundance of γc reduced interleukin-4 (IL-4) and IL-21 responses after IL-7 preexposure but not vice versa. Computational modeling combined with quantitative experimental assays indicated that the asymmetric cross-talk resulted from the ability of the "private" IL-7 receptor subunits (IL-7Rα) to bind to many of the γc molecules even before stimulation with cytokine. Upon exposure of T cells to IL-7, the high affinity of the IL-7Rα:IL-7 complex for γc further reduced the amount of free γc in a manner dependent on the concentration of IL-7. Measurements of bioluminescence resonance energy transfer (BRET) between IL-4Rα and γc were reduced when IL-7Rα was overexpressed. Furthermore, in a system expressing IL-7Rα, IL-4Rα, and γc, BRET between IL-4Rα and γc increased after IL-4 binding and decreased when cells were preexposed to IL-7, supporting the assumption that IL-7Rα and the IL-7Rα:IL-7 complex limit the accessibility of γc for other cytokine receptor complexes. We propose that in complex inflammatory environments, such asymmetric cross-talk establishes a hierarchy of cytokine responsiveness.

Publication types

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

MeSH terms

  • Animals
  • Binding, Competitive
  • Cells, Cultured
  • Cytokines / metabolism*
  • Humans
  • Interleukin Receptor Common gamma Subunit / genetics
  • Interleukin Receptor Common gamma Subunit / metabolism*
  • Kinetics
  • Mice, Knockout
  • Mice, Transgenic
  • Protein Binding
  • Receptor Cross-Talk
  • Receptors, Interleukin-7 / genetics
  • Receptors, Interleukin-7 / metabolism*
  • Signal Transduction*
  • T-Lymphocytes / metabolism*

Substances

  • Cytokines
  • IL2RG protein, human
  • Interleukin Receptor Common gamma Subunit
  • Receptors, Interleukin-7
  • interleukin-7 receptor, alpha chain