CAR-Macrophage Therapy Alleviates Myocardial Ischemia-Reperfusion Injury

Circ Res. 2024 Dec 6;135(12):1161-1174. doi: 10.1161/CIRCRESAHA.124.325212. Epub 2024 Oct 28.

Abstract

Background: Given the growing acknowledgment of the detrimental effects of excessive myocardial fibrosis on pathological remodeling after myocardial ischemia-reperfusion injury (I/R), targeting the modulation of myocardial fibrosis may offer protective and therapeutic advantages. However, effective clinical interventions and therapies that target myocardial fibrosis remain limited. As a promising chimeric antigen receptor (CAR) cell therapy, whether CAR macrophages (CAR-Ms) can be used to treat I/R remains unclear.

Methods: The expression of FAP (fibroblast activation protein) was studied in mouse hearts after I/R. FAP CAR-Ms were generated to target FAP-expressing cardiac fibroblasts in mouse hearts after I/R. The phagocytosis activity of FAP CAR-Ms was tested in vitro. The efficacy and safety of FAP CAR-Ms in treating I/R were evaluated in vivo.

Results: FAP was significantly upregulated in activated cardiac fibroblasts as early as 3 days after I/R. Upon demonstrating their ability to engulf FAP-overexpressing fibroblasts, we intravenously administered FAP CAR-Ms to mice at 3 days after I/R and found that FAP CAR-Ms significantly improved cardiac function and reduced myocardial fibrosis in mice after I/R. No toxicities associated with FAP CAR-Ms were detected in the heart or other organs at 2 weeks after I/R. Finally, we found that FAP CAR-Ms conferred long-term cardioprotection against I/R.

Conclusions: Our proof-of-concept study demonstrates the therapeutic potential of FAP CAR-Ms in alleviating myocardial I/R and potentially opens new avenues for the treatment of a range of heart diseases that include a fibrotic phenotype.

Keywords: cardiomyopathies; fibrosis; macrophages; myocardial reperfusion injury; receptors, chimeric antigen.

MeSH terms

  • Animals
  • Cells, Cultured
  • Endopeptidases* / metabolism
  • Fibroblasts* / metabolism
  • Fibroblasts* / pathology
  • Fibrosis*
  • Gelatinases / metabolism
  • Macrophages* / metabolism
  • Male
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism
  • Mice
  • Mice, Inbred C57BL*
  • Myocardial Reperfusion Injury* / metabolism
  • Myocardial Reperfusion Injury* / pathology
  • Myocardial Reperfusion Injury* / prevention & control
  • Myocardial Reperfusion Injury* / therapy
  • Myocardium / metabolism
  • Myocardium / pathology
  • Phagocytosis
  • Receptors, Chimeric Antigen / metabolism
  • Serine Endopeptidases / metabolism

Substances

  • fibroblast activation protein alpha
  • Endopeptidases
  • Receptors, Chimeric Antigen
  • Membrane Proteins
  • Gelatinases
  • Serine Endopeptidases