Population and Single-Cell Analysis of Human Cardiogenesis Reveals Unique LGR5 Ventricular Progenitors in Embryonic Outflow Tract

Developmental Cell - Tập 48 - Trang 475-490.e7 - 2019
Makoto Sahara1,2, Federica Santoro1, Jesper Sohlmér1, Chikai Zhou1, Nevin Witman1,2, Chuen Yan Leung2, Mimmi Mononen2, Kristine Bylund2, Peter Gruber3, Kenneth R. Chien1,2
1Department of Cell and Molecular Biology, Karolinska Institutet, Stockholm 171 77, Sweden
2Department of Medicine-Cardiology, Karolinska Institutet, Stockholm 141 86, Sweden
3Department of Surgery, Yale University, New Haven, CT USA

Tài liệu tham khảo

Barker, 2010, Leucine-rich repeat-containing G-protein-coupled receptors as markers of adult stem cells, Gastroenterology, 138, 1681, 10.1053/j.gastro.2010.03.002 Barker, 2007, Identification of stem cells in small intestine and colon by marker gene Lgr5, Nature, 449, 1003, 10.1038/nature06196 Bax, 2009, Platelet-derived growth factor is involved in the differentiation of second heart field-derived cardiac structures in chicken embryos, Dev. Dyn., 238, 2658, 10.1002/dvdy.22073 Birket, 2013, PGC-1alpha and reactive oxygen species regulate human embryonic stem cell-derived cardiomyocyte function, Stem Cell Rep., 1, 560, 10.1016/j.stemcr.2013.11.008 Birket, 2015, Expansion and patterning of cardiovascular progenitors derived from human pluripotent stem cells, Nat. Biotechnol., 33, 970, 10.1038/nbt.3271 Bondue, 2010, Mesp1: a key regulator of cardiovascular lineage commitment, Circ. Res., 107, 1414, 10.1161/CIRCRESAHA.110.227058 Brennecke, 2013, Accounting for technical noise in single-cell RNA-seq experiments, Nat. Methods, 10, 1093, 10.1038/nmeth.2645 Bu, 2009, Human ISL1 heart progenitors generate diverse multipotent cardiovascular cell lineages, Nature, 460, 113, 10.1038/nature08191 Burridge, 2014, Chemically defined generation of human cardiomyocytes, Nat. Methods, 11, 855, 10.1038/nmeth.2999 Cambier, 2014, Nkx2-5 regulates cardiac growth through modulation of Wnt signaling by R-spondin3, Development, 141, 2959, 10.1242/dev.103416 Chong, 2013, Progenitor cells identified by PDGFR-alpha expression in the developing and diseased human heart, Stem Cells Dev., 22, 1932, 10.1089/scd.2012.0542 Christiaen, 2009, Spatio-temporal intersection of Lhx3 and Tbx6 defines the cardiac field through synergistic activation of Mesp, Dev. Biol., 328, 552, 10.1016/j.ydbio.2009.01.033 Cong, 2013, Multiplex genome engineering using CRISPR/Cas systems, Science, 339, 819, 10.1126/science.1231143 Cui, 2013, Wdpcp, a PCP protein required for ciliogenesis, regulates directional cell migration and cell polarity by direct modulation of the actin cytoskeleton, PLoS Biol., 11, e1001720, 10.1371/journal.pbio.1001720 DeLaughter, 2016, Single-cell resolution of temporal gene expression during heart development, Dev. Cell, 39, 480, 10.1016/j.devcel.2016.10.001 Dobin, 2013, STAR: ultrafast universal RNA-seq aligner, Bioinformatics, 29, 15, 10.1093/bioinformatics/bts635 Friedman, 2018, Single-cell transcriptomic analysis of cardiac differentiation from human PSCs reveals HOPX-dependent cardiomyocyte maturation, Cell Stem Cell, 23, 586, 10.1016/j.stem.2018.09.009 Galdos, 2017, Cardiac regeneration: lessons from development, Circ. Res., 120, 941, 10.1161/CIRCRESAHA.116.309040 Guigo, 2003, Comparison of mouse and human genomes followed by experimental verification yields an estimated 1,019 additional genes, Proc. Natl. Acad. Sci. USA, 100, 1140, 10.1073/pnas.0337561100 Haghverdi, 2015, Diffusion maps for high-dimensional single-cell analysis of differentiation data, Bioinformatics, 31, 2989, 10.1093/bioinformatics/btv325 Han, 2011, A WNT/beta-catenin signaling activator, R-spondin, plays positive regulatory roles during skeletal myogenesis, J. Biol. Chem., 286, 10649, 10.1074/jbc.M110.169391 Hashem, 2013, Shox2 regulates the pacemaker gene program in embryoid bodies, Stem Cells Dev., 22, 2915, 10.1089/scd.2013.0123 Hovanes, 2001, Beta-catenin-sensitive isoforms of lymphoid enhancer factor-1 are selectively expressed in colon cancer, Nat. Genet., 28, 53, 10.1038/ng0501-53 Hrvatin, 2014, MARIS: method for analyzing RNA following intracellular sorting, PLoS One, 9, e89459, 10.1371/journal.pone.0089459 Jain, 2015, Heart DEVELOPMENT. Integration of Bmp and Wnt signaling by Hopx specifies commitment of cardiomyoblasts, Science, 348, aaa6071, 10.1126/science.aaa6071 Jansson, 2015, Making sense of Wnt signaling-linking hair cell regeneration to development, Front. Cell. Neurosci., 9, 66, 10.3389/fncel.2015.00066 Jha, 2017, Downregulation of LGR5 expression inhibits cardiomyocyte differentiation and potentiates endothelial differentiation from human pluripotent stem cells, Stem Cell Rep., 9, 513, 10.1016/j.stemcr.2017.07.006 Jin, 2017, Contribution of rare inherited and de novo variants in 2,871 congenital heart disease probands, Nat. Genet., 49, 1593, 10.1038/ng.3970 Junttila, 2015, Targeting LGR5+ cells with an antibody-drug conjugate for the treatment of colon cancer, Sci. Transl. Med., 7, 314ra186, 10.1126/scitranslmed.aac7433 Kapoor, 2013, Direct conversion of quiescent cardiomyocytes to pacemaker cells by expression of Tbx18, Nat. Biotechnol., 31, 54, 10.1038/nbt.2465 Klaus, 2007, Distinct roles of Wnt/beta-catenin and Bmp signaling during early cardiogenesis, Proc. Natl. Acad. Sci. USA, 104, 18531, 10.1073/pnas.0703113104 Laugwitz, 2005, Postnatal isl1+ cardioblasts enter fully differentiated cardiomyocyte lineages, Nature, 433, 647, 10.1038/nature03215 Lian, 2013, Directed cardiomyocyte differentiation from human pluripotent stem cells by modulating Wnt/beta-catenin signaling under fully defined conditions, Nat. Protoc., 8, 162, 10.1038/nprot.2012.150 Macosko, 2015, Highly parallel genome-wide expression profiling of individual cells using nanoliter droplets, Cell, 161, 1202, 10.1016/j.cell.2015.05.002 Mayer, 1997, Sarcomeric gene expression and contractility in myofibroblasts, J. Cell Biol., 139, 1477, 10.1083/jcb.139.6.1477 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 Petropoulos, 2016, Single-cell RNA-Seq reveals lineage and X chromosome dynamics in human preimplantation embryos, Cell, 165, 1012, 10.1016/j.cell.2016.03.023 Picelli, 2013, Smart-seq2 for sensitive full-length transcriptome profiling in single cells, Nat. Methods, 10, 1096, 10.1038/nmeth.2639 Reller, 2008, Prevalence of congenital heart defects in metropolitan Atlanta, 1998-2005, J. Pediatr., 153, 807, 10.1016/j.jpeds.2008.05.059 Saga, 1999, MesP1 is expressed in the heart precursor cells and required for the formation of a single heart tube, Development, 126, 3437, 10.1242/dev.126.15.3437 Sahara, 2014, Manipulation of a VEGF-Notch signaling circuit drives formation of functional vascular endothelial progenitors from human pluripotent stem cells, Cell Res., 24, 820, 10.1038/cr.2014.59 Sahara, 2015, Programming and reprogramming a human heart cell, EMBO J., 34, 710, 10.15252/embj.201490563 Soibam, 2015, Genome-wide identification of MESP1 targets demonstrates primary regulation over mesendoderm gene activity, Stem Cells, 33, 3254, 10.1002/stem.2111 Takahashi, 2012, Myocardial progenitors in the pharyngeal regions migrate to distinct conotruncal regions, Dev. Dyn., 241, 284, 10.1002/dvdy.23714 Treutlein, 2014, Reconstructing lineage hierarchies of the distal lung epithelium using single-cell RNA-seq, Nature, 509, 371, 10.1038/nature13173 Vander Heiden, 2010, Evidence for an alternative glycolytic pathway in rapidly proliferating cells, Science, 329, 1492, 10.1126/science.1188015 Vincent, 2010, How to make a heart: the origin and regulation of cardiac progenitor cells, Curr. Top. Dev. Biol., 90, 1, 10.1016/S0070-2153(10)90001-X Watanabe, 2012, Fibroblast growth factor 10 gene regulation in the second heart field by Tbx1, Nkx2-5, and Islet1 reveals a genetic switch for down-regulation in the myocardium, Proc. Natl. Acad. Sci. USA, 109, 18273, 10.1073/pnas.1215360109 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