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AUTHOR Bannerman, Dawn and Pascual-Gil, Simon and Wu, Qinghua and Fernandes, Ian and Zhao, Yimu and Wagner, Karl T. and Okhovatian, Sargol and Landau, Shira and Rafatian, Naimeh and Bodenstein, David F. and Wang, Ying and Nash, Trevor R. and Vunjak-Novakovic, Gordana and Keller, Gordon and Epelman, Slava and Radisic, Milica
Title Heart-on-a-Chip Model of Epicardial–Myocardial Interaction in Ischemia Reperfusion Injury [Abstract]
Year 2024
Journal/Proceedings Advanced Healthcare Materials
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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.
AUTHOR Hamidzada, Homaira and Pascual-Gil, Simon and Wu, Qinghua and Kent, Gregory M. and Massé, Stéphane and Kantores, Crystal and Kuzmanov, Uros and Gomez-Garcia, M. Juliana and Rafatian, Naimeh and Gorman, Renée A. and Wauchop, Marianne and Chen, Wenliang and Landau, Shira and Subha, Tasnia and Atkins, Michael H. and Zhao, Yimu and Beroncal, Erika and Fernandes, Ian and Nanthakumar, Jared and Vohra, Shabana and Wang, Erika Y. and Valdman Sadikov, Tamilla and Razani, Babak and McGaha, Tracy L. and Andreazza, Ana C. and Gramolini, Anthony and Backx, Peter H. and Nanthakumar, Kumaraswamy and Laflamme, Michael A. and Keller, Gordon and Radisic, Milica and Epelman, Slava
Title Primitive macrophages induce sarcomeric maturation and functional enhancement of developing human cardiac microtissues via efferocytic pathways [Abstract]
Year 2024
Journal/Proceedings Nature Cardiovascular Research
Reftype Hamidzada2024
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Yolk sac macrophages are the first to seed the developing heart; however, owing to a lack of accessible tissue, there is no understanding of their roles in human heart development and function. In this study, we bridge this gap by differentiating human embryonic stem (hES) cells into primitive LYVE1+ macrophages (hESC-macrophages) that stably engraft within contractile cardiac microtissues composed of hESC-cardiomyocytes and fibroblasts. Engraftment induces a human fetal cardiac macrophage gene program enriched in efferocytic pathways. Functionally, hESC-macrophages trigger cardiomyocyte sarcomeric protein maturation, enhance contractile force and improve relaxation kinetics. Mechanistically, hESC-macrophages engage in phosphatidylserine-dependent ingestion of apoptotic cardiomyocyte cargo, which reduces microtissue stress, leading hESC-cardiomyocytes to more closely resemble early human fetal ventricular cardiomyocytes, both transcriptionally and metabolically. Inhibiting hESC-macrophage efferocytosis impairs sarcomeric protein maturation and reduces cardiac microtissue function. Together, macrophage-engineered human cardiac microtissues represent a considerably improved model for human heart development and reveal a major beneficial role for human primitive macrophages in enhancing early cardiac tissue function.
AUTHOR Wu, Qinghua and Zhang, Peikai and O'Leary, Gerard and Zhao, Yimu and Xu, Yinghao and Rafatian, Naimeh and Okhovatian, Sargol and Landau, Shira and Valiante, Taufik A. and Travas-Sejdic, Jadranka and Radisic, Milica
Title Flexible 3D printed microwires and 3D microelectrodes for heart-on-a-chip engineering [Abstract]
Year 2023
Journal/Proceedings Biofabrication
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We developed a heart-on-a-chip platform that integrates highly flexible, vertical, 3D micropillar electrodes for electrophysiological recording and elastic microwires for the tissue’s contractile force assessment. The high aspect ratio microelectrodes were 3D-printed into the device using a conductive polymer, poly(3,4-ethylenedioxythiophene): poly(styrene sulfonate) (PEDOT:PSS). A pair of flexible, quantum dots/thermoplastic elastomer nanocomposite microwires were 3D printed to anchor the tissue and enable continuous contractile force assessment. The 3D microelectrodes and flexible microwires enabled unobstructed human iPSC-based cardiac tissue formation and contraction, suspended above the device surface, under both spontaneous beating and upon pacing with a separate set of integrated carbon electrodes. Recording of extracellular field potentials using the PEDOT:PSS micropillars was demonstrated with and without epinephrine as a model drug, non-invasively, along with in situ monitoring of tissue contractile properties and calcium transients. Uniquely, the platform provides integrated profiling of electrical and contractile tissue properties, which is critical for proper evaluation of complex, mechanically and electrically active tissues, such as the heart muscle under both physiological and pathological conditions.