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Deterministic Encapsulation of Human Cardiac Stem Cells in Variable Composition Nanoporous Gel Cocoons To Enhance Therapeutic Repair of Injured Myocardium
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    Deterministic Encapsulation of Human Cardiac Stem Cells in Variable Composition Nanoporous Gel Cocoons To Enhance Therapeutic Repair of Injured Myocardium
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    • Pushpinder Kanda
      Pushpinder Kanda
      University of Ottawa Heart Institute, Division of Cardiology, Department of Medicine, University of Ottawa, Ottawa, Canada K1Y4W7
    • Emilio I. Alarcon
      Emilio I. Alarcon
      Division of Cardiac Surgery, Department of Surgery, University of Ottawa Heart Institute, University of Ottawa, Ottawa, Canada K1Y4W7
      Department of Biochemistry, Microbiology, and Immunology, Faculty of Medicine, University of Ottawa, Ottawa, Canada K1H8M5
    • Tanya Yeuchyk
      Tanya Yeuchyk
      University of Ottawa Heart Institute, Division of Cardiology, Department of Medicine, University of Ottawa, Ottawa, Canada K1Y4W7
    • Sandrine Parent
      Sandrine Parent
      University of Ottawa Heart Institute, Division of Cardiology, Department of Medicine, University of Ottawa, Ottawa, Canada K1Y4W7
    • Robert A. de Kemp
      Robert A. de Kemp
      University of Ottawa Heart Institute, Division of Cardiology, Department of Medicine, University of Ottawa, Ottawa, Canada K1Y4W7
    • Fabio Variola
      Fabio Variola
      Department of Mechanical Engineering, University of Ottawa, Ottawa, Canada K1N6N5
      Department of Cellular and Molecular Medicine, University of Ottawa, Ottawa, Canada K1H8M5
    • David Courtman
      David Courtman
      Regenerative Medicine Program, Ottawa Hospital Research Institute, Ottawa, Canada K1H8L6
    • Duncan J. Stewart
      Duncan J. Stewart
      University of Ottawa Heart Institute, Division of Cardiology, Department of Medicine, University of Ottawa, Ottawa, Canada K1Y4W7
      Department of Cellular and Molecular Medicine, University of Ottawa, Ottawa, Canada K1H8M5
      Regenerative Medicine Program, Ottawa Hospital Research Institute, Ottawa, Canada K1H8L6
    • Darryl R. Davis*
      Darryl R. Davis
      University of Ottawa Heart Institute, Division of Cardiology, Department of Medicine, University of Ottawa, Ottawa, Canada K1Y4W7
      Department of Cellular and Molecular Medicine, University of Ottawa, Ottawa, Canada K1H8M5
      *E-mail: [email protected]
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    ACS Nano

    Cite this: ACS Nano 2018, 12, 5, 4338–4350
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    https://doi.org/10.1021/acsnano.7b08881
    Published April 16, 2018
    Copyright © 2018 American Chemical Society

    Abstract

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    Although cocooning explant-derived cardiac stem cells (EDCs) in protective nanoporous gels (NPGs) prior to intramyocardial injection boosts long-term cell retention, the number of EDCs that finally engraft is trivial and unlikely to account for salutary effects on myocardial function and scar size. As such, we investigated the effect of varying the NPG content within capsules to alter the physical properties of cocoons without influencing cocoon dimensions. Increasing NPG concentration enhanced cell migration and viability while improving cell-mediated repair of injured myocardium. Given that the latter occurred with NPG content having no detectable effect on the long-term engraftment of transplanted cells, we found that changing the physical properties of cocoons prompted explant-derived cardiac stem cells to produce greater amounts of cytokines, nanovesicles, and microRNAs that boosted the generation of new blood vessels and new cardiomyocytes. Thus, by altering the physical properties of cocoons by varying NPG content, the paracrine signature of encapsulated cells can be enhanced to promote greater endogenous repair of injured myocardium.

    Copyright © 2018 American Chemical Society

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    Supporting Information

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    The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acsnano.7b08881.

    • Additional information on cocoon’s physical properties, cell behavior within cocoons, myocardial scar formation, angio- and myogenesis, and paracrine secretion (PDF)

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    Cited By

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    Citation Statements
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    This article is cited by 26 publications.

    1. Erik Jacques, Katsuhiro Hosoyama, Brook Biniam, Cagla Eren Cimenci, Veronika Sedlakova, Alexander J. Steeves, Fabio Variola, Darryl R. Davis, Duncan J. Stewart, Erik J. Suuronen, Emilio I. Alarcon. Collagen-Based Microcapsules As Therapeutic Materials for Stem Cell Therapies in Infarcted Myocardium. ACS Biomaterials Science & Engineering 2020, 6 (8) , 4614-4622. https://doi.org/10.1021/acsbiomaterials.0c00245
    2. Berna Özkale, Oliver Lieleg. Why Biopolymer Microgels with Dynamically Switchable Properties Would be a Great Tool‐Box for the Cultivation of Stem Cells. Advanced Materials Interfaces 2024, 218 https://doi.org/10.1002/admi.202400354
    3. Wenjun Le, Zeyi Sun, Tieyan Li, Hao Cao, Chuanxue Yang, Tianxiao Mei, Laihai Zhang, Yibing Wang, Wenwen Jia, Wen Sun, Yihui Hu, Zhongmin Liu. Antioxidant Nanozyme‐Engineered Mesenchymal Stem Cells for In Vivo MRI Tracking and Synergistic Therapy of Myocardial Infarction. Advanced Functional Materials 2024, 65 https://doi.org/10.1002/adfm.202314328
    4. Ziqing Xiong, Qi An, Liqiang Chen, Yucheng Xiang, Lian Li, Yaxian Zheng. Cell or cell derivative-laden hydrogels for myocardial infarction therapy: from the perspective of cell types. Journal of Materials Chemistry B 2023, 11 (41) , 9867-9888. https://doi.org/10.1039/D3TB01411H
    5. Megan Dutcher, Simon Chewchuk, Ainara Benavente-Babace, Nicholas Soucy, Fan Wan, Kim Merrett, Darryl R Davis, James L Harden, Michel Godin. Encapsulating therapeutic cells in RGD-modified agarose microcapsules. Biomedical Materials 2023, 18 (5) , 055007. https://doi.org/10.1088/1748-605X/ace6e8
    6. Bérénice C. Collet, Darryl R. Davis. Mechanisms of Cardiac Repair in Cell Therapy. Heart, Lung and Circulation 2023, 32 (7) , 825-835. https://doi.org/10.1016/j.hlc.2023.01.019
    7. Sandrine Parent, Ramana Vaka, Yousef Risha, Clarissa Ngo, Pushpinder Kanda, Stanley Nattel, Saad Khan, David Courtman, Duncan J. Stewart, Darryl R. Davis. Prevention of atrial fibrillation after open-chest surgery with extracellular vesicle therapy. JCI Insight 2023, 8 (15) https://doi.org/10.1172/jci.insight.163297
    8. Nicholas D. Cober, Katelynn Rowe, Yupu Deng, Ainara Benavente‐Babace, David W. Courtman, Michel Godin, Duncan J. Stewart. Targeting extracellular vesicle delivery to the lungs by microgel encapsulation. Journal of Extracellular Biology 2023, 2 (6) https://doi.org/10.1002/jex2.94
    9. Raziel Hamami, Haneen Simaan-Yameen, Cesare Gargioli, Dror Seliktar. Comparison of Four Different Preparation Methods for Making Injectable Microgels for Tissue Engineering and Cell Therapy. Regenerative Engineering and Translational Medicine 2022, 8 (4) , 615-629. https://doi.org/10.1007/s40883-022-00261-2
    10. Xuejiao Han, Aqu Alu, Hongmei Liu, Yi Shi, Xiawei Wei, Lulu Cai, Yuquan Wei. Biomaterial-assisted biotherapy: A brief review of biomaterials used in drug delivery, vaccine development, gene therapy, and stem cell therapy. Bioactive Materials 2022, 17 , 29-48. https://doi.org/10.1016/j.bioactmat.2022.01.011
    11. Kashif Khan, Karina Gasbarrino, Ibtisam Mahmoud, Line Dufresne, Stella S. Daskalopoulou, Adel Schwertani, Renzo Cecere. Bioactive Scaffolds in Stem Cell-Based Therapies for Myocardial Infarction: a Systematic Review and Meta-Analysis of Preclinical Trials. Stem Cell Reviews and Reports 2022, 18 (6) , 2104-2136. https://doi.org/10.1007/s12015-021-10186-y
    12. Behnam Pournemati, Hadi Tabesh, Alireza Jenabi, Rouhollah Mehdinavaz Aghdam, Ali Hossein Rezayan, Ali Poorkhalil, Seyed Hossein Ahmadi Tafti, Khosrow Mottaghy. Injectable conductive nanocomposite hydrogels for cardiac tissue engineering: Focusing on carbon and metal-based nanostructures. European Polymer Journal 2022, 174 , 111336. https://doi.org/10.1016/j.eurpolymj.2022.111336
    13. Ramana Vaka, Darryl R. Davis. State-Of-Play for Cellular Therapies in Cardiac Repair and Regeneration. Stem Cells 2021, 39 (12) , 1579-1588. https://doi.org/10.1002/stem.3446
    14. Patrick Vigneault, Sandrine Parent, Pushpinder Kanda, Connor Michie, Darryl R. Davis, Stanley Nattel. Electrophysiological engineering of heart-derived cells with calcium-dependent potassium channels improves cell therapy efficacy for cardioprotection. Nature Communications 2021, 12 (1) https://doi.org/10.1038/s41467-021-25180-8
    15. Syed Baseeruddin Alvi, Salmman Ahmed, Divya Sridharan, Zahra Naseer, Nooruddin Pracha, Henry Wang, Konstantinos Dean Boudoulas, Wuqiang Zhu, Nazish Sayed, Mahmood Khan. De novo Drug Delivery Modalities for Treating Damaged Hearts: Current Challenges and Emerging Solutions. Frontiers in Cardiovascular Medicine 2021, 8 https://doi.org/10.3389/fcvm.2021.742315
    16. Junlang Li, Shiqi Hu, Dashuai Zhu, Ke Huang, Xuan Mei, Blanca López de Juan Abad, Ke Cheng. All Roads Lead to Rome (the Heart): Cell Retention and Outcomes From Various Delivery Routes of Cell Therapy Products to the Heart. Journal of the American Heart Association 2021, 10 (8) https://doi.org/10.1161/JAHA.120.020402
    17. Rajiv Kumar, Kiran Gulia. The convergence of nanotechnology‐stem cell, nanotopography‐mechanobiology, and biotic‐abiotic interfaces: Nanoscale tools for tackling the top killer, arteriosclerosis, strokes, and heart attacks. Nano Select 2021, 2 (4) , 655-687. https://doi.org/10.1002/nano.202000192
    18. Cecilie Hoeeg, Alireza Dolatshahi-Pirouz, Bjarke Follin. Injectable Hydrogels for Improving Cardiac Cell Therapy—In Vivo Evidence and Translational Challenges. Gels 2021, 7 (1) , 7. https://doi.org/10.3390/gels7010007
    19. Leonidas Kandilogiannakis, Eirini Filidou, George Kolios, Vasilis Paspaliaris. Ad-Dressing Stem Cells: Hydrogels for Encapsulation. Processes 2021, 9 (1) , 11. https://doi.org/10.3390/pr9010011
    20. Pushpinder Kanda, Ainara Benavente-Babace, Sandrine Parent, Michie Connor, Nicholas Soucy, Alexander Steeves, Aizhu Lu, Nicholas David Cober, David Courtman, Fabio Variola, Emilio I. Alarcon, Wenbin Liang, Duncan J. Stewart, Michel Godin, Darryl R. Davis. Deterministic paracrine repair of injured myocardium using microfluidic-based cocooning of heart explant-derived cells. Biomaterials 2020, 247 , 120010. https://doi.org/10.1016/j.biomaterials.2020.120010
    21. Darryl R Davis, Eduardo Marbán. Heart-derived cells for therapeutics. 2020, 217-243. https://doi.org/10.1016/B978-0-12-813706-2.00011-7
    22. Seth Mount, Pushpinder Kanda, Sandrine Parent, Saad Khan, Connor Michie, Liliana Davila, Vincent Chan, Ross A. Davies, Haissam Haddad, David Courtman, Duncan J. Stewart, Darryl R. Davis. Physiologic expansion of human heart-derived cells enhances therapeutic repair of injured myocardium. Stem Cell Research & Therapy 2019, 10 (1) https://doi.org/10.1186/s13287-019-1418-3
    23. Pushpinder Kanda, Sandrine Parent, Darryl R. Davis. Immortalized factories of therapeutic vesicles. Nature Biomedical Engineering 2019, 3 (9) , 676-677. https://doi.org/10.1038/s41551-019-0453-9
    24. Xinlong Wang, Nancy Rivera‐Bolanos, Bin Jiang, Guillermo A. Ameer. Advanced Functional Biomaterials for Stem Cell Delivery in Regenerative Engineering and Medicine. Advanced Functional Materials 2019, 29 (23) https://doi.org/10.1002/adfm.201809009
    25. Ainara Benavente‐Babace, Kristina Haase, Duncan J. Stewart, Michel Godin. Strategies for controlling egress of therapeutic cells from hydrogel microcapsules. Journal of Tissue Engineering and Regenerative Medicine 2019, 13 (4) , 612-624. https://doi.org/10.1002/term.2818
    26. Ghazaleh Rafatian, Darryl R. Davis. Concise Review: Heart-Derived Cell Therapy 2.0: Paracrine Strategies to Increase Therapeutic Repair of Injured Myocardium. Stem Cells 2018, 36 (12) , 1794-1803. https://doi.org/10.1002/stem.2910

    ACS Nano

    Cite this: ACS Nano 2018, 12, 5, 4338–4350
    Click to copy citationCitation copied!
    https://doi.org/10.1021/acsnano.7b08881
    Published April 16, 2018
    Copyright © 2018 American Chemical Society

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