Heart-on-a-Chip Model of Epicardial-Myocardial Interaction in Ischemia Reperfusion Injury

Adv Healthc Mater. 2024 Aug;13(21):e2302642. doi: 10.1002/adhm.202302642. Epub 2024 May 9.

Abstract

Epicardial cells (EPIs) form the outer layer of the heart and play an important role in development and disease. Current heart-on-a-chip platforms still do not fully mimic the native cardiac environment due to the absence of relevant cell types, such as EPIs. Here, using the Biowire II platform, engineered cardiac tissues with an epicardial outer layer and inner myocardial structure are constructed, and an image analysis approach is developed to track the EPI cell migration in a beating myocardial environment. Functional properties of EPI cardiac tissues improve over two weeks in culture. In conditions mimicking ischemia reperfusion injury (IRI), the EPI cardiac tissues experience less cell death and a lower impact on functional properties. EPI cell coverage is significantly reduced and more diffuse under normoxic conditions compared to the post-IRI conditions. Upon IRI, migration of EPI cells into the cardiac tissue interior is observed, with contributions to alpha smooth muscle actin positive cell population. Altogether, a novel heart-on-a-chip model is designed to incorporate EPIs through a formation process that mimics cardiac development, and this work demonstrates that EPI cardiac tissues respond to injury differently than epicardium-free controls, highlighting the importance of including EPIs in heart-on-a-chip constructs that aim to accurately mimic the cardiac environment.

Keywords: cardiomyocyte; epicardium; epithelium; heart‐on‐a‐chip; ischemia; myocardium.

MeSH terms

  • Animals
  • Cell Movement
  • Lab-On-A-Chip Devices*
  • Myocardial Reperfusion Injury / metabolism
  • Myocardial Reperfusion Injury / pathology
  • Myocardium / metabolism
  • Myocardium / pathology
  • Pericardium* / metabolism
  • Reperfusion Injury / metabolism
  • Reperfusion Injury / pathology
  • Tissue Engineering / methods