Engineered cardiac tissue microsphere production through direct differentiation of hydrogel-encapsulated human pluripotent stem cells

Del Alamo, 2016, High throughput physiological screening of iPSC-derived cardiomyocytes for drug development, Biochim. Biophys. Acta, 1863, 1717, 10.1016/j.bbamcr.2016.03.003 Zhang, 2015, Cardiac regeneration and stem cells, Physiol. Rev., 95, 1189, 10.1152/physrev.00021.2014 Stevens, 2018, Human pluripotent stem cell-derived engineered tissues: clinical considerations, Cell Stem Cell, 22, 294, 10.1016/j.stem.2018.01.015 Gwathmey, 2009, Cardionomics: a new integrative approach for screening cardiotoxicity of drug candidates, Expet Opin. Drug Metabol. Toxicol., 5, 647, 10.1517/17425250902932915 Rajamohan, 2013, Current status of drug screening and disease modelling in human pluripotent stem cells, Bioessays, 35, 281, 10.1002/bies.201200053 Takahashi, 2007, Induction of pluripotent stem cells from adult human fibroblasts by defined factors, Cell, 131, 861, 10.1016/j.cell.2007.11.019 Burridge, 2014, Chemically defined generation of human cardiomyocytes, Nat. Methods, 11, 855, 10.1038/nmeth.2999 Lian, 2013, Directed cardiomyocyte differentiation from human pluripotent stem cells by modulating Wnt/β-catenin signaling under fully defined conditions, Nat. Protoc., 8, 162, 10.1038/nprot.2012.150 Kempf, 2016, Large-scale production of human pluripotent stem cell derived cardiomyocytes, Adv. Drug Deliv. Rev., 96, 18, 10.1016/j.addr.2015.11.016 Fonoudi, 2015, A universal and robust integrated platform for the scalable production of human cardiomyocytes from pluripotent stem cells, Stem Cells Transl Med, 4, 1482, 10.5966/sctm.2014-0275 Kempf, 2014, Controlling expansion and cardiomyogenic differentiation of human pluripotent stem cells in scalable suspension culture, Stem Cell Reports, 3, 1132, 10.1016/j.stemcr.2014.09.017 Halloin, 2019, Continuous WNT control enables advanced hPSC cardiac processing and prognostic surface marker identification in chemically defined suspension culture, Stem Cell Reports Rajala, 2011, Cardiac differentiation of pluripotent stem cells, Stem Cell. Int., 2011, 383709 Kehat, 2001, Human embryonic stem cells can differentiate into myocytes with structural and functional properties of cardiomyocytes, J. Clin. Invest., 108, 407, 10.1172/JCI200112131 Burridge, 2007, Improved human embryonic stem cell embryoid body homogeneity and cardiomyocyte differentiation from a novel V-96 plate aggregation system highlights interline variability, Stem Cell., 25, 929, 10.1634/stemcells.2006-0598 Osafune, 2008, Marked differences in differentiation propensity among human embryonic stem cell lines, Nat. Biotechnol., 26, 313, 10.1038/nbt1383 Laflamme, 2007, Cardiomyocytes derived from human embryonic stem cells in pro-survival factors enhance function of infarcted rat hearts, Nat. Biotechnol., 25, 1015, 10.1038/nbt1327 Huyer, 2015, Biomaterial based cardiac tissue engineering and its applications, Biomed. Mater., 10, 10.1088/1748-6041/10/3/034004 Landa, 2008, Effect of injectable alginate implant on cardiac remodeling and function after recent and old infarcts in rat, Circulation, 117, 1388, 10.1161/CIRCULATIONAHA.107.727420 Abecasis, 2020, Toward a microencapsulated 3D hiPSC-derived in vitro cardiac microtissue for recapitulation of human heart microenvironment features, Front Bioeng Biotechnol, 8, 580744, 10.3389/fbioe.2020.580744 Wendel, 2014, Functional consequences of a tissue-engineered myocardial patch for cardiac repair in a rat infarct model, Tissue Eng., 20, 1325, 10.1089/ten.tea.2013.0312 Dunn, 2014, Biomimetic materials design for cardiac tissue regeneration, Wiley Interdiscip Rev Nanomed Nanobiotechnol, 6, 15, 10.1002/wnan.1241 Kerscher, 2016, Direct hydrogel encapsulation of pluripotent stem cells enables ontomimetic differentiation and growth of engineered human heart tissues, Biomaterials, 83, 383, 10.1016/j.biomaterials.2015.12.011 Kerscher, 2016, Direct production of human cardiac tissues by pluripotent stem cell encapsulation in gelatin methacryloyl, ACS Biomater. Sci. Eng., 3, 1499, 10.1021/acsbiomaterials.6b00226 Almany, 2005, Biosynthetic hydrogel scaffolds made from fibrinogen and polyethylene glycol for 3D cell cultures, Biomaterials, 26, 2467, 10.1016/j.biomaterials.2004.06.047 Jenkins, 2015, Human pluripotent stem cell-derived products: advances towards robust, scalable and cost-effective manufacturing strategies, Biotechnol. J., 10, 83, 10.1002/biot.201400348 Trattnig, 2015, Morphological and compositional monitoring of a new cell-free cartilage repair hydrogel technology - GelrinC by MR using semi-quantitative MOCART scoring and quantitative T2 index and new zonal T2 index calculation, Osteoarthritis Cartilage, 23, 2224, 10.1016/j.joca.2015.07.007 Shinnawi, 2015, Monitoring human-induced pluripotent stem cell-derived cardiomyocytes with genetically encoded calcium and voltage fluorescent reporters, Stem Cell Reports, 5, 582, 10.1016/j.stemcr.2015.08.009 DeLong, 2005, Covalently immobilized gradients of bFGF on hydrogel scaffolds for directed cell migration, Biomaterials, 26, 3227, 10.1016/j.biomaterials.2004.09.021 Dikovsky, 2006, The effect of structural alterations of PEG-fibrinogen hydrogel scaffolds on 3-D cellular morphology and cellular migration, Biomaterials, 27, 1496, 10.1016/j.biomaterials.2005.09.038 Seeto, 2019, Rapid production of cell-laden microspheres using a flexible microfluidic encapsulation platform, Small, 15 Kinney, 2014, Engineering three-dimensional stem cell morphogenesis for the development of tissue models and scalable regenerative therapeutics, Ann. Biomed. Eng., 42, 352, 10.1007/s10439-013-0953-9 Kim, 2010, Investigation of mechanical properties of soft hydrogel microcapsules in relation to protein delivery using a MEMS force sensor, J. Biomed. Mater. Res., 92, 103, 10.1002/jbm.a.32338 Hodge, 2016, Enhanced stem cell-derived cardiomyocyte differentiation in suspension culture by delivery of nitric oxide using S-nitrosocysteine, Biotechnol. Bioeng., 113, 882, 10.1002/bit.25849 Seeto, 2017, Encapsulation of equine endothelial colony forming cells in highly uniform, injectable hydrogel microspheres for local cell delivery, Tissue Eng. Part C, Methods, 23, 815, 10.1089/ten.tec.2017.0233 Lian, 2012, Robust cardiomyocyte differentiation from human pluripotent stem cells via temporal modulation of canonical Wnt signaling, Proc. Natl. Acad. Sci. U. S. A., 109, E1848, 10.1073/pnas.1200250109 Shadrin, 2017, Cardiopatch platform enables maturation and scale-up of human pluripotent stem cell-derived engineered heart tissues, Nat. Commun., 8, 1825, 10.1038/s41467-017-01946-x Saunders, 2010, SEM investigation of heart tissue samples, J. Phys. Conf., 241, 10.1088/1742-6596/241/1/012023 Feric, 2016, Maturing human pluripotent stem cell-derived cardiomyocytes in human engineered cardiac tissues, Adv. Drug Deliv. Rev., 96, 110, 10.1016/j.addr.2015.04.019 Huebsch, 2015, Automated video-based analysis of contractility and calcium flux in human-induced pluripotent stem cell-derived cardiomyocytes cultured over different spatial scales, Tissue Eng. Part C, Methods, 21, 467, 10.1089/ten.tec.2014.0283 Bratt-Leal, 2009, Engineering the embryoid body microenvironment to direct embryonic stem cell differentiation, Biotechnol. Prog., 25, 43, 10.1002/btpr.139 Pettinato, 2014, Formation of well-defined embryoid bodies from dissociated human induced pluripotent stem cells using microfabricated cell-repellent microwell arrays, Sci. Rep., 4, 7402, 10.1038/srep07402 Branco, 2019, Transcriptomic analysis of 3D cardiac differentiation of human induced pluripotent stem cells reveals faster cardiomyocyte maturation compared to 2D culture, Sci. Rep., 9, 9229, 10.1038/s41598-019-45047-9 Ng, 2005, Forced aggregation of defined numbers of human embryonic stem cells into embryoid bodies fosters robust, reproducible hematopoietic differentiation, Blood, 106, 1601, 10.1182/blood-2005-03-0987 Ungrin, 2008, Reproducible, ultra high-throughput formation of multicellular organization from single cell suspension-derived human embryonic stem cell aggregates, PloS One, 3, e1565, 10.1371/journal.pone.0001565 Beauchamp, 2015, Development and characterization of a scaffold-free 3D spheroid model of induced pluripotent stem cell-derived human cardiomyocytes, Tissue Eng. Part C, Methods, 21, 852, 10.1089/ten.tec.2014.0376 Pradhan, 2017, A three-dimensional spheroidal cancer model based on PEG-fibrinogen hydrogel microspheres, Biomaterials, 115, 141, 10.1016/j.biomaterials.2016.10.052 Jing, 2010, Cardiac cell generation from encapsulated embryonic stem cells in static and scalable culture systems, Cell Transplant., 19, 1397, 10.3727/096368910X513955 Madden, 2010, Proangiogenic scaffolds as functional templates for cardiac tissue engineering, Proc. Natl. Acad. Sci. U. S. A., 107, 15211, 10.1073/pnas.1006442107 Tulloch, 2011, Growth of engineered human myocardium with mechanical loading and vascular coculture, Circ. Res., 109, 47, 10.1161/CIRCRESAHA.110.237206 Reis, 2016, Biomaterials in myocardial tissue engineering, J. Tissue Eng. Regen. Med., 10, 11, 10.1002/term.1944 Habib, 2011, A combined cell therapy and in-situ tissue-engineering approach for myocardial repair, Biomaterials, 32, 7514, 10.1016/j.biomaterials.2011.06.049 Shao, 2015, On human pluripotent stem cell control: the rise of 3D bioengineering and mechanobiology, Biomaterials, 52, 26, 10.1016/j.biomaterials.2015.01.078 Guyette, 2016, Bioengineering human myocardium on native extracellular matrix, Circ. Res., 118, 56, 10.1161/CIRCRESAHA.115.306874 Bratt-Leal, 2011, Incorporation of biomaterials in multicellular aggregates modulates pluripotent stem cell differentiation, Biomaterials, 32, 48, 10.1016/j.biomaterials.2010.08.113 Spearman, 2015, Conductive interpenetrating networks of polypyrrole and polycaprolactone encourage electrophysiological development of cardiac cells, Acta Biomater., 28, 109, 10.1016/j.actbio.2015.09.025 Shin, 2013, Carbon-nanotube-embedded hydrogel sheets for engineering cardiac constructs and bioactuators, ACS Nano, 7, 2369, 10.1021/nn305559j Paul, 2014, Injectable graphene oxide/hydrogel-based angiogenic gene delivery system for vasculogenesis and cardiac repair, ACS Nano, 8, 8050, 10.1021/nn5020787 Kim, 2010, Nanoscale cues regulate the structure and function of macroscopic cardiac tissue constructs, Proc. Natl. Acad. Sci. U. S. A., 107, 565, 10.1073/pnas.0906504107 Sugiura, 2016, Dynamic three-dimensional micropatterned cell co-cultures within photocurable and chemically degradable hydrogels, J. Tissue Eng. Regen. Med., 10, 690, 10.1002/term.1843 Nunes, 2013, Biowire: a platform for maturation of human pluripotent stem cell-derived cardiomyocytes, Nat. Methods, 10, 781, 10.1038/nmeth.2524 Ronaldson-Bouchard, 2018, Advanced maturation of human cardiac tissue grown from pluripotent stem cells, Nature, 556, 239, 10.1038/s41586-018-0016-3 Young, 2011, Hydrogels with time-dependent material properties enhance cardiomyocyte differentiation in vitro, Biomaterials, 32, 1002, 10.1016/j.biomaterials.2010.10.020 Hazeltine, 2014, Temporal impact of substrate mechanics on differentiation of human embryonic stem cells to cardiomyocytes, Acta Biomater., 10, 604, 10.1016/j.actbio.2013.10.033 Davidson, 2007, Measuring Mechanical Properties of Embryos and Embryonic Tissues, 83, 425 Ferri, 2013, Drug attrition during pre-clinical and clinical development: understanding and managing drug-induced cardiotoxicity, Pharmacol. Ther., 138, 470, 10.1016/j.pharmthera.2013.03.005 Fermini, 2018, Clinical trials in a dish: a perspective on the coming revolution in drug development, SLAS Discov, 23, 765, 10.1177/2472555218775028 Burridge, 2011, A universal system for highly efficient cardiac differentiation of human induced pluripotent stem cells that eliminates interline variability, PloS One, 6, 10.1371/journal.pone.0018293 Pioner, 2019, Optical investigation of action potential and calcium handling maturation of hiPSC-cardiomyocytes on biomimetic substrates, Int. J. Mol. Sci., 20, 10.3390/ijms20153799 Don, 2013, Improving survival and efficacy of pluripotent stem cell-derived cardiac grafts, J. Cell Mol. Med., 17, 1355, 10.1111/jcmm.12147 Gerbin, 2015, Enhanced electrical integration of engineered human myocardium via intramyocardial versus epicardial delivery in infarcted rat hearts, PloS One, 10, 10.1371/journal.pone.0131446 Carpenter, 2012, Efficient differentiation of human induced pluripotent stem cells generates cardiac cells that provide protection following myocardial infarction in the rat, Stem Cell. Dev., 21, 977, 10.1089/scd.2011.0075 Chong, 2014, Human embryonic-stem-cell-derived cardiomyocytes regenerate non-human primate hearts, Nature, 510, 273, 10.1038/nature13233 Lundy, 2014, Pluripotent stem cell derived cardiomyocytes for cardiac repair, Curr. Treat. Options Cardiovasc. Med., 16, 319, 10.1007/s11936-014-0319-0 Mirotsou, 2011, Paracrine mechanisms of stem cell reparative and regenerative actions in the heart, J. Mol. Cell. Cardiol., 50, 280, 10.1016/j.yjmcc.2010.08.005 Hodgkinson, 2016, Emerging concepts in paracrine mechanisms in regenerative cardiovascular medicine and biology, Circ. Res., 118, 95, 10.1161/CIRCRESAHA.115.305373 Blin, 2010, A purified population of multipotent cardiovascular progenitors derived from primate pluripotent stem cells engrafts in postmyocardial infarcted nonhuman primates, J. Clin. Invest., 120, 1125, 10.1172/JCI40120 Bellamy, 2015, Long-term functional benefits of human embryonic stem cell-derived cardiac progenitors embedded into a fibrin scaffold, J. Heart Lung Transplant., 34, 1198, 10.1016/j.healun.2014.10.008 Joanne, 2016, Nanofibrous clinical-grade collagen scaffolds seeded with human cardiomyocytes induces cardiac remodeling in dilated cardiomyopathy, Biomaterials, 80, 157, 10.1016/j.biomaterials.2015.11.035 Menasche, 2018, Transplantation of human embryonic stem cell-derived cardiovascular progenitors for severe ischemic left ventricular dysfunction, J. Am. Coll. Cardiol., 71, 429, 10.1016/j.jacc.2017.11.047 Menasche, 2018, Cell therapy trials for heart regeneration - lessons learned and future directions, Nat. Rev. Cardiol., 15, 659, 10.1038/s41569-018-0013-0 El-Kirat-Chatel, 2015, Forces in yeast flocculation, Nanoscale, 7, 1760, 10.1039/C4NR06315E Kang, 2016, A 3D bioprinting system to produce human-scale tissue constructs with structural integrity, Nat. Biotechnol., 34, 312, 10.1038/nbt.3413 Ouyang, 2015, Three-dimensional bioprinting of embryonic stem cells directs highly uniform embryoid body formation, Biofabrication, 7, 10.1088/1758-5090/7/4/044101 Ma, 2015, Bioprinting 3D cell-laden hydrogel microarray for screening human periodontal ligament stem cell response to extracellular matrix, Biofabrication, 7, 10.1088/1758-5090/7/4/044105 Kupfer, 2020 Chan, 2016 Zhao, 2016, Injectable stem cell-laden photocrosslinkable microspheres fabricated using microfluidics for rapid generation of osteogenic tissue constructs, Adv. Funct. Mater. Jiang, 2017, A microfluidic-based cell encapsulation platform to achieve high long-term cell viability in photopolymerized PEGNB hydrogel microspheres, J. Mater. Chem. B Mater Biol Med, 5, 173, 10.1039/C6TB02551J Gal, 2020, Injectable cardiac cell microdroplets for tissue regeneration, Small, 10.1002/smll.201904806 Rossow, 2017, Cell microencapsulation by droplet microfluidic templating, Macromol. Chem. Phys., 218, 1600380, 10.1002/macp.201600380 Chang, 2020, Emulsion-based encapsulation of pluripotent stem cells in hydrogel microspheres for cardiac differentiation, Biotechnol. Prog., 10.1002/btpr.2986