Combining antimiR-25 and cGAMP Nanocomplexes Enhances Immune Responses via M2 Macrophage Reprogramming

Int J Mol Sci. 2024 Nov 28;25(23):12787. doi: 10.3390/ijms252312787.

Abstract

Glioblastoma (GBM) is an aggressive brain cancer with a highly immunosuppressive tumor microenvironment (TME), invariably infiltrated by tumor-associated macrophages (TAMs). These TAMs resemble M2 macrophages, which promote tumor growth and suppress immune responses. GBM cells secrete extracellular vesicles (EVs) containing microRNA-25, which inhibits the cGAS-STING pathway and prevents TAMs from adopting a pro-inflammatory M1 phenotype. This study characterizes antimiR-25/cGAMP nanocomplexes (NCs) for potential therapeutic applications. A particle size analysis revealed a significant reduction upon complexation with antimiR-25, resulting in smaller, more stable nanoparticles. Stability tests across pH levels (4-6) and temperatures (25-37 °C) demonstrated their resilience in various biological environments. Biological assays showed that antimiR-25 NCs interacted strongly with transferrin (Tf), suggesting potential for blood-brain barrier passage. The use of cGAMP NCs activated the cGAS-STING pathway in macrophages, leading to increased type I IFN (IFN-β) production and promoting a shift from the M2 to M1 phenotype. The combined use of cGAMP and antimiR-25 NCs also increased the expression of markers involved in M1 polarization. These findings offer insights into optimizing antimiR-25/cGAMP NCs for enhancing immune responses in GBM.

Keywords: EVs; PAMAM; STING pathway; antagomir-25; antimiR-25; cGAMP; cancer immunotherapy; extracellular vesicles; nanomedicine; polymeric nanoparticles.

MeSH terms

  • Animals
  • Brain Neoplasms / immunology
  • Brain Neoplasms / metabolism
  • Brain Neoplasms / pathology
  • Cell Line, Tumor
  • Extracellular Vesicles / immunology
  • Extracellular Vesicles / metabolism
  • Glioblastoma* / immunology
  • Glioblastoma* / metabolism
  • Glioblastoma* / pathology
  • Humans
  • Macrophages* / drug effects
  • Macrophages* / immunology
  • Macrophages* / metabolism
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism
  • MicroRNAs* / genetics
  • Nanoparticles / chemistry
  • Nucleotides, Cyclic* / metabolism
  • Nucleotides, Cyclic* / pharmacology
  • Nucleotidyltransferases / metabolism
  • Signal Transduction / drug effects
  • Tumor Microenvironment / drug effects
  • Tumor-Associated Macrophages / drug effects
  • Tumor-Associated Macrophages / immunology
  • Tumor-Associated Macrophages / metabolism

Substances

  • MicroRNAs
  • cyclic guanosine monophosphate-adenosine monophosphate
  • Nucleotides, Cyclic
  • MIRN25 microRNA, human
  • Membrane Proteins
  • cGAS protein, human
  • Nucleotidyltransferases
  • STING1 protein, human