Reprogramming cellular senescence in the tumor microenvironment augments cancer immunotherapy through multifunctional nanocrystals

Sci Adv. 2024 Nov;10(44):eadp7022. doi: 10.1126/sciadv.adp7022. Epub 2024 Nov 1.

Abstract

Harnessing the immunogenic potential of senescent tumor cells provides an opportunity to remodel tumor microenvironment (TME) and boost antitumor immunity. However, this potential needs to be sophisticatedly wielded to avoid additional immunosuppressive capacity of senescent cells. Our study shows that blocking the JAK2/STAT3 pathway enhances immunogenic efficacy of Aurora kinase inhibitor alisertib (Ali)-induced senescence by reducing immunosuppressive senescence-associated secretory phenotype (SASP) while preserving immunogenic SASP. Hypothesizing that SASP reprogramming with Ali and JAK2 inhibitor ruxolitinib (Rux) will benefit cancer immunotherapy, we create nanoparticulate crystals (Ali-Rux) composed of Ali and Rux with a fully active pharmaceutical ingredient. Immunization with Ali-Rux-orchestrated senescent cells promotes stronger activation of antigen-presenting cells, enhancing antitumor immune surveillance. This approach remodels the TME by increasing CD8+ T cell and NK recruitment and activation while decreasing MDSCs. Combined with PD-L1 blockade, Ali-Rux elicits a durable antitumor immune response, suggesting the TME reshaping approach as a potential cancer immunotherapy.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Azepines
  • CD8-Positive T-Lymphocytes / immunology
  • CD8-Positive T-Lymphocytes / metabolism
  • Cell Line, Tumor
  • Cellular Reprogramming / drug effects
  • Cellular Senescence* / drug effects
  • Humans
  • Immunotherapy* / methods
  • Janus Kinase 2 / metabolism
  • Mice
  • Nanoparticles* / chemistry
  • Neoplasms / drug therapy
  • Neoplasms / immunology
  • Neoplasms / pathology
  • Neoplasms / therapy
  • Nitriles / pharmacology
  • Pyrazoles / pharmacology
  • Pyrazoles / therapeutic use
  • Pyrimidines / pharmacology
  • STAT3 Transcription Factor / metabolism
  • Tumor Microenvironment* / drug effects
  • Tumor Microenvironment* / immunology

Substances

  • Pyrimidines
  • MLN 8237
  • Janus Kinase 2
  • ruxolitinib
  • Nitriles
  • Pyrazoles
  • STAT3 Transcription Factor
  • Azepines