Human ISL1+ Ventricular Progenitors Self-Assemble into an In Vivo Functional Heart Patch and Preserve Cardiac Function Post Infarction

Bui, 2011, Epidemiology and risk profile of heart failure, Nat. Rev. Cardiol., 8, 30, 10.1038/nrcardio.2010.165 Lin, 2014, Strategies for cardiac regeneration and repair, Sci. Transl. Med., 6, 239rv1, 10.1126/scitranslmed.3006681 Bergmann, 2009, Evidence for cardiomyocyte renewal in humans, Science, 324, 98, 10.1126/science.1164680 Bergmann, 2015, Dynamics of cell generation and turnover in the human heart, Cell, 161, 1566, 10.1016/j.cell.2015.05.026 Senyo, 2013, Mammalian heart renewal by pre-existing cardiomyocytes, Nature, 493, 433, 10.1038/nature11682 Khan, 2015, Evaluation of changes in morphology and function of human induced pluripotent stem cell derived cardiomyocytes (HiPSC-CMs) cultured on an aligned-nanofiber cardiac patch, PLoS One, 10, e0126338, 10.1371/journal.pone.0126338 Wu, 2006, Developmental origin of a bipotential myocardial and smooth muscle cell precursor in the mammalian heart, Cell, 127, 1137, 10.1016/j.cell.2006.10.028 Moretti, 2006, Multipotent embryonic isl1+ progenitor cells lead to cardiac, smooth muscle, and endothelial cell diversification, Cell, 127, 1151, 10.1016/j.cell.2006.10.029 He, 2003, Human embryonic stem cells develop into multiple types of cardiac myocytes: action potential characterization, Circ. Res., 93, 32, 10.1161/01.RES.0000080317.92718.99 Mummery, 2003, Differentiation of human embryonic stem cells to cardiomyocytes: role of coculture with visceral endoderm-like cells, Circulation, 107, 2733, 10.1161/01.CIR.0000068356.38592.68 Tang, 2011, An antibody against SSEA-5 glycan on human pluripotent stem cells enables removal of teratoma-forming cells, Nat. Biotechnol., 29, 829, 10.1038/nbt.1947 Lee, 2013, Tumorigenicity as a clinical hurdle for pluripotent stem cell therapies, Nat. Med., 19, 998, 10.1038/nm.3267 Caspi, 2007, Transplantation of human embryonic stem cell-derived cardiomyocytes improves myocardial performance in infarcted rat hearts, J. Am. Coll. Cardiol., 50, 1884, 10.1016/j.jacc.2007.07.054 Di Giorgio, 2008, Human embryonic stem cell-derived motor neurons are sensitive to the toxic effect of glial cells carrying an ALS-causing mutation, Cell Stem Cell, 3, 637, 10.1016/j.stem.2008.09.017 Pagliuca, 2014, Generation of functional human pancreatic β cells in vitro, Cell, 159, 428, 10.1016/j.cell.2014.09.040 Spence, 2011, Directed differentiation of human pluripotent stem cells into intestinal tissue in vitro, Nature, 470, 105, 10.1038/nature09691 Lian, 2012, Robust cardiomyocyte differentiation from human pluripotent stem cells via temporal modulation of canonical Wnt signaling, Proc. Natl. Acad. Sci. USA, 109, E1848, 10.1073/pnas.1200250109 Qyang, 2007, The renewal and differentiation of Isl1+ cardiovascular progenitors are controlled by a Wnt/β-catenin pathway, Cell Stem Cell, 1, 165, 10.1016/j.stem.2007.05.018 Buikema, 2013, Wnt/β-catenin signaling directs the regional expansion of first and second heart field-derived ventricular cardiomyocytes, Development, 140, 4165, 10.1242/dev.099325 Pennica, 1995, Cardiotrophin-1. Biological activities and binding to the leukemia inhibitory factor receptor/gp130 signaling complex, J. Biol. Chem., 270, 10915, 10.1074/jbc.270.18.10915 Wollert, 1997, Cardiotrophin-1 and the role of gp130-dependent signaling pathways in cardiac growth and development, J. Mol. Med. (Berl.), 75, 492, 10.1007/s001090050134 Yang, 2008, Human cardiovascular progenitor cells develop from a KDR+ embryonic-stem-cell-derived population, Nature, 453, 524, 10.1038/nature06894 Bu, 2009, Human ISL1 heart progenitors generate diverse multipotent cardiovascular cell lineages, Nature, 460, 113, 10.1038/nature08191 Domian, 2009, Generation of functional ventricular heart muscle from mouse ventricular progenitor cells, Science, 326, 426, 10.1126/science.1177350 O’Hara, 2011, Simulation of the undiseased human cardiac ventricular action potential: model formulation and experimental validation, PLoS Comput. Biol., 7, e1002061, 10.1371/journal.pcbi.1002061 Franz, 1987, Monophasic action potential mapping in human subjects with normal electrocardiograms: direct evidence for the genesis of the T wave, Circulation, 75, 379, 10.1161/01.CIR.75.2.379 Burridge, 2014, Chemically defined generation of human cardiomyocytes, Nat. Methods, 11, 855, 10.1038/nmeth.2999 Chen, 2015, Phospholamban as a crucial determinant of the inotropic response of human pluripotent stem cell-derived ventricular cardiomyocytes and engineered 3-dimensional tissue constructs, Circ Arrhythm Electrophysiol, 8, 193, 10.1161/CIRCEP.114.002049 Liu, 2007, Functional sarcoplasmic reticulum for calcium handling of human embryonic stem cell-derived cardiomyocytes: insights for driven maturation, Stem Cells, 25, 3038, 10.1634/stemcells.2007-0549 Louch, 2015, Calcium signalling in developing cardiomyocytes: implications for model systems and disease, J. Physiol., 593, 1047, 10.1113/jphysiol.2014.274712 Weng, 2014, A simple, cost-effective but highly efficient system for deriving ventricular cardiomyocytes from human pluripotent stem cells, Stem Cells Dev., 23, 1704, 10.1089/scd.2013.0509 Ziman, 2010, Excitation-contraction coupling changes during postnatal cardiac development, J. Mol. Cell. Cardiol., 48, 379, 10.1016/j.yjmcc.2009.09.016 O’Brien, 1993, Positional specification of ventricular myosin light chain 2 expression in the primitive murine heart tube, Proc. Natl. Acad. Sci. USA, 90, 5157, 10.1073/pnas.90.11.5157 Forbes, 2014, Preparing the ground for tissue regeneration: from mechanism to therapy, Nat. Med., 20, 857, 10.1038/nm.3653 Webber, 2015, A perspective on the clinical translation of scaffolds for tissue engineering, Ann. Biomed. Eng., 43, 641, 10.1007/s10439-014-1104-7 Vunjak-Novakovic, 2011, Bioengineering heart muscle: a paradigm for regenerative medicine, Annu. Rev. Biomed. Eng., 13, 245, 10.1146/annurev-bioeng-071910-124701 Wang, 2006, Cardiomyopathy associated with microcirculation dysfunction in laminin α4 chain-deficient mice, J. Biol. Chem., 281, 213, 10.1074/jbc.M505061200 Bassat, 2017, The extracellular matrix protein agrin promotes heart regeneration in mice, Nature, 547, 179, 10.1038/nature22978 Zangi, 2013, Modified mRNA directs the fate of heart progenitor cells and induces vascular regeneration after myocardial infarction, Nat. Biotechnol., 31, 898, 10.1038/nbt.2682 Gerbin, 2015, Enhanced electrical integration of engineered human myocardium via intramyocardial versus epicardial delivery in infarcted rat hearts, PLoS One, 10, e0131446, 10.1371/journal.pone.0131446 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 Burchfield, 2008, Role of paracrine factors in stem and progenitor cell mediated cardiac repair and tissue fibrosis, Fibrogenesis Tissue Repair, 1, 4, 10.1186/1755-1536-1-4 Gnecchi, 2005, Paracrine action accounts for marked protection of ischemic heart by Akt-modified mesenchymal stem cells, Nat. Med., 11, 367, 10.1038/nm0405-367 Ginis, 2004, Differences between human and mouse embryonic stem cells, Dev. Biol., 269, 360, 10.1016/j.ydbio.2003.12.034 Williams, 1988, Myeloid leukaemia inhibitory factor maintains the developmental potential of embryonic stem cells, Nature, 336, 684, 10.1038/336684a0 Sartiani, 2007, Developmental changes in cardiomyocytes differentiated from human embryonic stem cells: a molecular and electrophysiological approach, Stem Cells, 25, 1136, 10.1634/stemcells.2006-0466 Menasché, 2015, Human embryonic stem cell-derived cardiac progenitors for severe heart failure treatment: first clinical case report, Eur. Heart J., 36, 2011, 10.1093/eurheartj/ehv189 Takeda, 2018, Identification of cardiomyocyte-fated progenitors from human-induced pluripotent stem cells marked with CD82, Cell Rep., 22, 546, 10.1016/j.celrep.2017.12.057 Lian, 2013, Insulin inhibits cardiac mesoderm, not mesendoderm, formation during cardiac differentiation of human pluripotent stem cells and modulation of canonical Wnt signaling can rescue this inhibition, Stem Cells, 31, 447, 10.1002/stem.1289 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 Elliott, 2011, NKX2-5(eGFP/w) hESCs for isolation of human cardiac progenitors and cardiomyocytes, Nat. Methods, 8, 1037, 10.1038/nmeth.1740 D’Amour, 2005, Efficient differentiation of human embryonic stem cells to definitive endoderm, Nat. Biotechnol., 23, 1534, 10.1038/nbt1163 Fu, 2010, Na+/Ca2+ exchanger is a determinant of excitation-contraction coupling in human embryonic stem cell-derived ventricular cardiomyocytes, Stem Cells Dev., 19, 773, 10.1089/scd.2009.0184 Chow, 2013, Human pluripotent stem cell-derived cardiomyocytes for heart regeneration, drug discovery and disease modeling: from the genetic, epigenetic, and tissue modeling perspectives, Stem Cell Res. Ther., 4, 97, 10.1186/scrt308 Smith, 2004, Advances in functional and structural MR image analysis and implementation as FSL, Neuroimage, 23, S208, 10.1016/j.neuroimage.2004.07.051 Loening, 2003, AMIDE: a free software tool for multimodality medical image analysis, Mol. Imaging, 2, 131, 10.1162/153535003322556877 Heiberg, 2010, Design and validation of Segment--freely available software for cardiovascular image analysis, BMC Med. Imaging, 10, 1, 10.1186/1471-2342-10-1 Cerqueira, 2002, Standardized myocardial segmentation and nomenclature for tomographic imaging of the heart. A statement for healthcare professionals from the Cardiac Imaging Committee of the Council on Clinical Cardiology of the American Heart Association, Circulation, 105, 539, 10.1161/hc0402.102975