Engineered Extracellular Vesicles Derived from Dermal Fibroblasts Attenuate Inflammation in a Murine Model of Acute Lung Injury

Adv Mater. 2023 Jul;35(28):e2210579. doi: 10.1002/adma.202210579. Epub 2023 Jun 5.

Abstract

Acute respiratory distress syndrome (ARDS) represents a significant burden to the healthcare system, with ≈200 000 cases diagnosed annually in the USA. ARDS patients suffer from severe refractory hypoxemia, alveolar-capillary barrier dysfunction, impaired surfactant function, and abnormal upregulation of inflammatory pathways that lead to intensive care unit admission, prolonged hospitalization, and increased disability-adjusted life years. Currently, there is no cure or FDA-approved therapy for ARDS. This work describes the implementation of engineered extracellular vesicle (eEV)-based nanocarriers for targeted nonviral delivery of anti-inflammatory payloads to the inflamed/injured lung. The results show the ability of surfactant protein A (SPA)-functionalized IL-4- and IL-10-loaded eEVs to promote intrapulmonary retention and reduce inflammation, both in vitro and in vivo. Significant attenuation is observed in tissue damage, proinflammatory cytokine secretion, macrophage activation, influx of protein-rich fluid, and neutrophil infiltration into the alveolar space as early as 6 h post-eEVs treatment. Additionally, metabolomics analyses show that eEV treatment causes significant changes in the metabolic profile of inflamed lungs, driving the secretion of key anti-inflammatory metabolites. Altogether, these results establish the potential of eEVs derived from dermal fibroblasts to reduce inflammation, tissue damage, and the prevalence/progression of injury during ARDS via nonviral delivery of anti-inflammatory genes/transcripts.

Keywords: anti-inflammatory extracellular vesicles; engineered extracellular vesicles; lung injury; nonviral gene delivery; novel nanocarriers; pulmonary inflammation.

MeSH terms

  • Acute Lung Injury* / metabolism
  • Acute Lung Injury* / therapy
  • Animals
  • Anti-Inflammatory Agents
  • Disease Models, Animal
  • Extracellular Vesicles* / metabolism
  • Fibroblasts / metabolism
  • Humans
  • Inflammation / metabolism
  • Mice
  • Respiratory Distress Syndrome* / therapy

Substances

  • Anti-Inflammatory Agents