A DNA-Modularized STING Agonist with Macrophage-Selectivity and Programmability for Enhanced Anti-Tumor Immunotherapy

Adv Sci (Weinh). 2024 Aug;11(32):e2400149. doi: 10.1002/advs.202400149. Epub 2024 Jun 19.

Abstract

The activation of cyclic GMP-AMP (cGAMP) synthase (cGAS) and its adaptor, stimulator of interferon genes (STING), is known to reprogram the immunosuppressive tumor microenvironment for promoting antitumor immunity. To enhance the efficiency of cGAS-STING pathway activation, macrophage-selective uptake, and programmable cytosolic release are crucial for the delivery of STING agonists. However, existing polymer- or lipid-based delivery systems encounter difficulty in integrating multiple functions meanwhile maintaining precise control and simple procedures. Herein, inspired by cGAS being a natural DNA sensor, a modularized DNA nanodevice agonist (DNDA) is designed that enable macrophage-selective uptake and programmable activation of the cGAS-STING pathway through precise self-assembly. The resulting DNA nanodevice acts as both a nanocarrier and agonist. Upon local administration, it demonstrates the ability of macrophage-selective uptake, endosomal escape, and cytosolic release of the cGAS-recognizing DNA segment, leading to robust activation of the cGAS-STING pathway and enhanced antitumor efficacy. Moreover, DNDA elicits a synergistic therapeutic effect when combined with immune checkpoint blockade. The study broadens the application of DNA nanotechnology as an immune stimulator for cGAS-STING activation.

Keywords: DNA nanotechnology; aptamer; cGAS‐STING; cancer immunotherapy; drug delivery; tumor‐associated macrophages.

MeSH terms

  • Animals
  • DNA* / immunology
  • Disease Models, Animal
  • Humans
  • Immunotherapy* / methods
  • Macrophages* / drug effects
  • Macrophages* / immunology
  • Macrophages* / metabolism
  • Membrane Proteins* / agonists
  • Membrane Proteins* / metabolism
  • Mice
  • Neoplasms / drug therapy
  • Neoplasms / immunology
  • Neoplasms / therapy
  • Nucleotidyltransferases* / metabolism
  • Tumor Microenvironment / drug effects
  • Tumor Microenvironment / immunology

Substances

  • Membrane Proteins
  • DNA
  • Nucleotidyltransferases
  • STING1 protein, human
  • Sting1 protein, mouse
  • cGAS protein, mouse