Novel design of potent anti-tumour activity of IL-2 prodrug by FAPα-mediated activation

Int J Biol Macromol. 2025 Jan;284(Pt 1):138120. doi: 10.1016/j.ijbiomac.2024.138120. Epub 2024 Nov 26.

Abstract

Interleukin-2 (IL-2) is a T cell growth factor that is essential for the proliferation of T cells and the generation of effector and memory cells. The antitumor activity of high-dose IL-2 therapy requires maintaining the affinity between IL-2 and IL2-Rα, which can also bring serious toxic side effects. To address this issue, we designed ZGP-Cysteamine-IL-2-K64C and (ZGP-Cysteamine)2-IL-2-(K43C, K64C) based on the strategy of FAPα enzyme-activated prodrugs, and investigated their anti-tumour activity and side effects. In vitro FAPα enzyme cleavage results indicated that the side-chain modified ZGP-Cysteamine moiety could be precisely recognized and cleaved by FAPα, thereby restoring the activity of native IL-2 capable of binding to IL-2Rα in the tumour microenvironment, where it promotes the expansion of CD8+ T cells. Meanwhile, surface plasmon resonance analysis revealed that, compared to wt-IL-2, both ZGP-Cysteamine-IL-2-K64C and (ZGP-Cysteamine)2-IL-2-(K43C, K64C) exhibited significantly reduced affinity for IL-2Rα, while their affinity for IL-2Rβγ remained unchanged. Remarkably, ZGP-Cysteamine-IL-2-K64C and (ZGP-Cysteamine)2-IL-2-(K43C, K64C) almost completely eliminated the pulmonary edema and vascular permeability. Furthermore, the combination of ZGP-Cysteamine-IL-2-K64C and PD-1 blockade showed robust anti-tumour activity in mice tumour models. Our study provides new insights into the structural design of IL-2 prodrug with low side effect and robust anti-tumour efficacy.

MeSH terms

  • Animals
  • Antineoplastic Agents* / chemistry
  • Antineoplastic Agents* / pharmacology
  • CD8-Positive T-Lymphocytes / drug effects
  • CD8-Positive T-Lymphocytes / immunology
  • Cell Line, Tumor
  • Cell Proliferation / drug effects
  • Drug Design
  • Endopeptidases / chemistry
  • Humans
  • Interleukin-2* / metabolism
  • Membrane Proteins
  • Mice
  • Prodrugs* / chemistry
  • Prodrugs* / pharmacology
  • Tumor Microenvironment / drug effects

Substances

  • Interleukin-2
  • Prodrugs
  • Antineoplastic Agents
  • fibroblast activation protein alpha
  • Endopeptidases
  • Membrane Proteins