Reversing Immune Checkpoint Inhibitor-Associated Cardiotoxicity via Bioorthogonal Metabolic Engineering-Driven Extracellular Vesicle Redirecting

Adv Mater. 2024 Nov;36(45):e2412340. doi: 10.1002/adma.202412340. Epub 2024 Sep 23.

Abstract

The cardiotoxicity induced by immune checkpoint inhibitors (ICIs) is associated with high mortality rates. T cells play an important role in ICI-induced cardiac injury. The inhibition of local T-cell activity is considered an effective strategy for alleviating ICI-related cardiotoxicity. Tumor-derived extracellular vesicles (EVs) contribute to immunosuppression via PD-L1 overexpression. In this study, a bioorthogonal metabolic engineering-driven EV redirecting (Biomeder) strategy for in situ engineered EVs with myocardial-targeting peptides is developed. Accumulated tumor-derived EV (TuEVs) reverses the immune environment in the heart by increasing PD-L1 levels in cardiomyocytes and/or by directly inhibiting T-cell activity. More importantly, it is found that the redirection of TuEVs further disrupts immunosuppression in tumors, which facilitates anti-tumor activity. Thus, redirecting TuEVs to the heart simultaneously enhances the antitumor efficacy and safety of ICI-based therapy. Furthermore, the Biomeder strategy is successfully expanded to prevent ICI-induced type 1 diabetes. This Biomeder technique is a universal method for the treatment of various ICI-related adverse events.

Keywords: ICI‐induced T1D; ICI‐induced cardiotoxicity; bioorthogonal metabolic engineering; cardio‐oncology; extracellular vesicles.

MeSH terms

  • Animals
  • B7-H1 Antigen* / antagonists & inhibitors
  • B7-H1 Antigen* / metabolism
  • Cardiotoxicity* / prevention & control
  • Cell Line, Tumor
  • Diabetes Mellitus, Type 1 / drug therapy
  • Diabetes Mellitus, Type 1 / metabolism
  • Extracellular Vesicles* / metabolism
  • Humans
  • Immune Checkpoint Inhibitors* / adverse effects
  • Metabolic Engineering*
  • Mice
  • Myocytes, Cardiac / metabolism
  • Neoplasms / drug therapy
  • Neoplasms / metabolism
  • T-Lymphocytes / immunology
  • T-Lymphocytes / metabolism

Substances

  • Immune Checkpoint Inhibitors
  • B7-H1 Antigen