Targeting PD-1+ T cells with small-format immunocytokines enhances IL-12 antitumor activity

Mol Ther. 2025 Jan 8;33(1):297-316. doi: 10.1016/j.ymthe.2024.11.027. Epub 2024 Nov 19.

Abstract

Immunostimulatory cytokines and immune checkpoint inhibitors hold promise as cancer therapeutics; however, their use is often limited by reduced efficacy and significant toxicity. In this study, we developed small-format immunocytokines (ICKs) based on interleukin-12 (IL-12) and blocking nanobodies (Nbs) targeting mouse and human programmed cell death 1 (PD-1) and programmed cell death ligand 1 (PD-L1). Both PD-1- and PD-L1-targeted ICKs demonstrated similar in vitro performance, significantly increasing IL-12 tethering to immune cells and enhancing T cell cytotoxic activity compared with IL-12 alone. The antitumor efficacy of ICKs was evaluated by intratumoral delivery using self-amplifying RNA-based vectors or as recombinant proteins in mice. Despite effective PD-L1-mediated tumor anchoring and promising in vitro results, IL-12 antitumor activity was significantly enhanced only when specific targeting to intratumoral T cells was achieved via anti-PD-1 Nb. This effect was also observed when the PD-1 specific ICK was delivered by electroporation of a DNA/RNA layered vector. Our findings suggest that targeting the appropriate type of cell within the tumor microenvironment could outperform tumor-anchoring strategies in the context of IL-12 therapy. Human versions of these ICKs were also developed, which showed to be active in human immune cells, opening an opportunity for clinical translation.

Keywords: Alphavirus; PD-1/PD-L1; checkpoint blockade; immunocytokine; interleukin-12; nanobody; self-amplifying RNA.

MeSH terms

  • Animals
  • B7-H1 Antigen / antagonists & inhibitors
  • B7-H1 Antigen / metabolism
  • Cell Line, Tumor
  • Female
  • Humans
  • Interleukin-12* / metabolism
  • Mice
  • Neoplasms / immunology
  • Neoplasms / metabolism
  • Neoplasms / therapy
  • Programmed Cell Death 1 Receptor* / antagonists & inhibitors
  • Programmed Cell Death 1 Receptor* / metabolism
  • Single-Domain Antibodies / pharmacology
  • T-Lymphocytes / immunology
  • T-Lymphocytes / metabolism
  • Tumor Microenvironment / immunology

Substances

  • Interleukin-12
  • Programmed Cell Death 1 Receptor
  • B7-H1 Antigen
  • Single-Domain Antibodies
  • PDCD1 protein, human