Regulating IL-2 Immune Signaling Function Via A Core Allosteric Structural Network

J Mol Biol. 2025 Jan 15;437(2):168892. doi: 10.1016/j.jmb.2024.168892. Epub 2024 Dec 9.

Abstract

Human interleukin-2 (IL-2) is a crucial cytokine for T cell regulation, with therapeutic potential in cancer and autoimmune diseases. However, IL-2's pleiotropic effects across different immune cell types often lead to toxicity and limited efficacy. Previous efforts to enhance IL-2's therapeutic profile have focused on modifying its receptor binding sites. Yet, the underlying dynamics and intramolecular networks contributing to IL-2 receptor recognition remain unexplored. This study presents a detailed characterization of IL-2 dynamics compared to two engineered IL-2 mutants, "superkines" S15 and S1, which exhibit biased signaling towards effector T cells. Using NMR spectroscopy and molecular dynamics simulations, we demonstrate significant variations in core dynamic pathways and conformational exchange rates across these three IL-2 variants. We identify distinct allosteric networks and minor state conformations in the superkines, despite their structural similarity to wild-type IL-2. Furthermore, we rationally design a mutation (L56A) in the S1 superkine's core network, which partially reverts its dynamics, receptor binding affinity, and T cell signaling behavior towards that of wild-type IL-2. Our results reveal that IL-2 superkine core dynamics play a critical role in their enhanced receptor binding and function, suggesting that modulating IL-2 dynamics and core allostery represents an untapped approach for designing immunotherapies with improved immune cell selectivity profiles.

Keywords: T cells; conformational exchange; interleukin-2; molecular dynamics simulations; nuclear magnetic resonance spectroscopy.

MeSH terms

  • Allosteric Regulation
  • Binding Sites
  • Humans
  • Interleukin-2* / metabolism
  • Magnetic Resonance Spectroscopy
  • Molecular Dynamics Simulation*
  • Mutation
  • Protein Binding
  • Protein Conformation*
  • Receptors, Interleukin-2 / chemistry
  • Receptors, Interleukin-2 / genetics
  • Receptors, Interleukin-2 / metabolism
  • Signal Transduction*
  • T-Lymphocytes / immunology
  • T-Lymphocytes / metabolism

Substances

  • Interleukin-2
  • IL2 protein, human
  • Receptors, Interleukin-2