The DOI matches its Crossref record; 54 of the 54 references it cites were found in a registry or an index.
Single-Cell Resolution of Temporal Gene Expression during Heart Development
Open accessAbstract
Activation of complex molecular programs in specific cell lineages governs mammalian heart development, from a primordial linear tube to a four-chamber organ. To characterize lineage-specific, temporal-spatial developmental programs, we performed single-cell RNA sequencing of >1200 murine cells isolated at seven time points spanning E9.5 (primordial heart tube) to P21 (mature heart). Using unbiased transcriptional data we classified cardiomyocytes (CM), endothelial cells (EC), and fibroblast-enriched cells, thus identifying markers for temporal and chamber-specific developmental programs. Harnessing these datasets, we defined developmental ages of human and mouse pluripotent stem cell-derived CMs and characterized lineage-specific maturation defects in hearts of mice with heterozygous mutations in Nkx2.5 that cause human heart malformations. This spatial-temporal transcriptome analysis of heart development reveals lineage-specific gene programs underlying normal cardiac development and congenital heart disease.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Silhouettes: A graphical aid to the interpretation and validation of cluster analysis
Rousseeuw, P. J. (1987) · Journal of Computational and Applied Mathematics · doi:10.1016/0377-0427(87)90125-7 · Cited by 21,392
TopHat: discovering splice junctions with RNA-Seq
Trapnell, C., Pachter, L., & Salzberg, S. L. (2009) · Bioinformatics · doi:10.1093/bioinformatics/btp120 · Cited by 11,617
Trapnell, C., Cacchiarelli, D., Grimsby, J., Pokharel, P., Li, S., Morse, M., Lennon, N. J., Livak, K. J., Mikkelsen, T. S., & Rinn, J. L. (2014) · Nature Biotechnology · doi:10.1038/nbt.2859 · Cited by 7,314
Huang, D. W., Sherman, B. T., Tan, Q., Kir, J., Liu, D., Bryant, D., Guo, Y., Stephens, R., Baseler, M. W., Lane, H. C., et al. (2007) · Nucleic Acids Research · doi:10.1093/nar/gkm415 · Cited by 2,213
SC3: consensus clustering of single-cell RNA-seq data
Kiselev, V. Y., Kirschner, K., Schaub, M. T., Andrews, T., Yiu, A., Chandra, T., Natarajan, K. N., Reik, W., Barahona, M., Green, A. R., et al. (2017) · Nature Methods · doi:10.1038/nmeth.4236 · Cited by 1,500
Revisiting Cardiac Cellular Composition
Pinto, A. R., Ilinykh, A., Ivey, M. J., Kuwabara, J. T., D’Antoni, M. L., Debuque, R., Chandran, A., Wang, L., Arora, K., Rosenthal, N. A., et al. (2016) · Circulation Research · doi:10.1161/circresaha.115.307778 · Cited by 1,400
Reconstructing lineage hierarchies of the distal lung epithelium using single-cell RNA-seq
Treutlein, B., Brownfield, D. G., Wu, A. R., Neff, N. F., Mantalas, G. L., Espinoza, F. H., Desai, T. J., Krasnow, M. A., & Quake, S. R. (2014) · Nature · doi:10.1038/nature13173 · Cited by 1,342
Congenital Heart Disease Caused by Mutations in the Transcription Factor NKX2-5
Schott, J.-J., Benson, D. W., Basson, C. T., Pease, W., Silberbach, G. M., Moak, J. P., Maron, B. J., Seidman, C. E., & Seidman, J. G. (1998) · Science · doi:10.1126/science.281.5373.108 · Cited by 1,308
Self-citationSingle-cell messenger RNA sequencing reveals rare intestinal cell types
Grün, D., Lyubimova, A., Kester, L., Wiebrands, K., Basak, O., Sasaki, N., Clevers, H., & van Oudenaarden, A. (2015) · Nature · doi:10.1038/nature14966 · Cited by 1,234
Buettner, F., Natarajan, K. N., Casale, F. P., Proserpio, V., Scialdone, A., Theis, F. J., Teichmann, S. A., Marioni, J. C., & Stegle, O. (2015) · Nature Biotechnology · doi:10.1038/nbt.3102 · Cited by 1,136
Bruneau, B. G., Nemer, G., Schmitt, J. P., Charron, F., Robitaille, L., Caron, S., Conner, D. A., Gessler, M., Nemer, M., Seidman, C. E., et al. (2001) · Cell · doi:10.1016/s0092-8674(01)00493-7 · Cited by 1,061
Self-citationDe novo mutations in congenital heart disease with neurodevelopmental and other congenital anomalies
Homsy, J., Zaidi, S., Shen, Y., Ware, J. S., Samocha, K. E., Karczewski, K. J., DePalma, S. R., McKean, D., Wakimoto, H., Gorham, J., et al. (2015) · Science · doi:10.1126/science.aac9396 · Cited by 856
Self-citationA High-Resolution Anatomical Atlas of the Transcriptome in the Mouse Embryo
Diez-Roux, G., Banfi, S., Sultan, M., Geffers, L., Anand, S., Rozado, D., Magen, A., Canidio, E., Pagani, M., Peluso, I., et al. (2011) · PLoS Biology · doi:10.1371/journal.pbio.1000582 · Cited by 638
Evidence for an Alternative Glycolytic Pathway in Rapidly Proliferating Cells
Vander Heiden, M. G., Locasale, J. W., Swanson, K. D., Sharfi, H., Heffron, G. J., Amador-Noguez, D., Christofk, H. R., Wagner, G., Rabinowitz, J. D., Asara, J. M., et al. (2010) · Science · doi:10.1126/science.1188015 · Cited by 635
Dynamic and Coordinated Epigenetic Regulation of Developmental Transitions in the Cardiac Lineage
Wamstad, J. A., Alexander, J. M., Truty, R. M., Shrikumar, A., Li, F., Eilertson, K. E., Ding, H., Wylie, J. N., Pico, A. R., Capra, J. A., et al. (2012) · Cell · doi:10.1016/j.cell.2012.07.035 · Cited by 610
Self-citationCardiac Fibroblasts Regulate Myocardial Proliferation through β1 Integrin Signaling
Ieda, M., Tsuchihashi, T., Ivey, K. N., Ross, R. S., Hong, T.-T., Shaw, R. M., & Srivastava, D. (2009) · Developmental Cell · doi:10.1016/j.devcel.2008.12.007 · Cited by 580
Tanaka, M., Chen, Z., Bartunkova, S., Yamasaki, N., & Izumo, S. (1999) · Development · doi:10.1242/dev.126.6.1269 · Cited by 566
Biben, C., Weber, R., Kesteven, S., Stanley, E., McDonald, L., Elliott, D. A., Barnett, L., Köentgen, F., Robb, L., Feneley, M., et al. (2000) · Circulation Research · doi:10.1161/01.res.87.10.888 · Cited by 349
Cardiac homeobox gene NKX2-5mutations and congenital heart disease
Elliott, D. A., Kirk, E. P., Yeoh, T., Chandar, S., McKenzie, F., Taylor, P., Grossfeld, P., Fatkin, D., Jones, O., Hayes, P., et al. (2003) · Journal of the American College of Cardiology · doi:10.1016/s0735-1097(03)00420-0 · Cited by 267
Kuppusamy, K. T., Jones, D. C., Sperber, H., Madan, A., Fischer, K. A., Rodriguez, M. L., Pabon, L., Zhu, W.-Z., Tulloch, N. L., Yang, X., et al. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1424042112 · Cited by 267
Thomas, T., Yamagishi, H., Overbeek, P. A., Olson, E. N., & Srivastava, D. (1998) · Developmental Biology · doi:10.1006/dbio.1998.8849 · Cited by 207
Ventricular Expression of tbx5 Inhibits Normal Heart Chamber Development
Liberatore, C. M., Searcy-Schrick, R. D., & Yutzey, K. E. (2000) · Developmental Biology · doi:10.1006/dbio.2000.9748 · Cited by 195
Cooperative and antagonistic interactions between Sall4 and Tbx5 pattern the mouse limb and heart
Koshiba-Takeuchi, K., Takeuchi, J. K., Arruda, E. P., Kathiriya, I. S., Mo, R., Hui, C.-C., Srivastava, D., & Bruneau, B. G. (2006) · Nature Genetics · doi:10.1038/ng1707 · Cited by 170
Self-citationEvolutionary Diversity of the Mitochondrial Calcium Uniporter
Bick, A. G., Calvo, S. E., & Mootha, V. K. (2012) · Science · doi:10.1126/science.1214977 · Cited by 165
Self-citationIntegration of Bmp and Wnt signaling by Hopx specifies commitment of cardiomyoblasts
Jain, R., Li, D., Gupta, M., Manderfield, L. J., Ifkovits, J. L., Wang, Q., Liu, F., Liu, Y., Poleshko, A., Padmanabhan, A., et al. (2015) · Science · doi:10.1126/science.aaa6071 · Cited by 161
Cardiac and Extracardiac Expression of Csx/Nkx2.5 Homeodomain Protein
Kasahara, H., Bartunkova, S., Schinke, M., Tanaka, M., & Izumo, S. (1998) · Circulation Research · doi:10.1161/01.res.82.9.936 · Cited by 157
Evolution and development of the building plan of the vertebrate heart
Jensen, B. K., Wang, T., Christoffels, V. M., & Moorman, A. F. M. (2012) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2012.10.004 · Cited by 155
Tian, Y., Yuan, L., Goss, A., Wang, T., Yang, J., Lepore, J. J., Zhou, D. D., Schwartz, R. J., Patel, V. V., Cohen, E. D., et al. (2010) · Developmental Cell · doi:10.1016/j.devcel.2010.01.008 · Cited by 141
Genomic imbalances associated with müllerian aplasia
Cheroki, C., Krepischi, A. C. V., Szuhai, K., Brenner, V., Kim, C. A., Otto, P. A., & Rosenberg, C. (2007) · Journal of Medical Genetics · doi:10.1136/jmg.2007.051839 · Cited by 136
Dahle, Ø., Kumar, A., & Kuehn, M. R. (2010) · Science Signaling · doi:10.1126/scisignal.2000841 · Cited by 122
A crucial role of a high mobility group protein HMGA2 in cardiogenesis
Monzen, K., Ito, Y., Naito, A. T., Kasai, H., Hiroi, Y., Hayashi, D., Shiojima, I., Yamazaki, T., Miyazono, K., Asashima, M., et al. (2008) · Nature Cell Biology · doi:10.1038/ncb1719 · Cited by 89
Sarcomeric Gene Expression and Contractility in Myofibroblasts
Mayer, D. C. G., & Leinwand, L. A. (1997) · The Journal of Cell Biology · doi:10.1083/jcb.139.6.1477 · Cited by 82
Essential Regulation of Lung Surfactant Homeostasis by the Orphan G Protein-Coupled Receptor GPR116
Yang, M., Hilton, M. B., Seaman, S., Haines, D. C., Nagashima, K., Burks, C., Tessarollo, L., Ivanova, P. T., Brown, H. A., Umstead, T. M., et al. (2013) · Cell Reports · doi:10.1016/j.celrep.2013.04.019 · Cited by 82
Microfibril-associated Glycoprotein 2 (MAGP2) Loss of Function Has Pleiotropic Effects in Vivo
Combs, M. D., Knutsen, R. H., Broekelmann, T. J., Toennies, H. M., Brett, T. J., Miller, C. A., Kober, D. L., Craft, C. S., Atkinson, J. J., Shipley, J. M., et al. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.497727 · Cited by 77
Desplantez, T., McCain, M. L., Beauchamp, P., Rigoli, G., Rothen‐Rutishauser, B., Parker, K. K., & Kléber, A. G. (2012) · Cardiovascular Research · doi:10.1093/cvr/cvs025 · Cited by 76
The mouse Gene Expression Database (GXD): 2014 update
Smith, C. M., Finger, J. H., Hayamizu, T. F., McCright, I. J., Xu, J., Berghout, J., Campbell, J., Corbani, L. E., Forthofer, K. L., Frost, P. J., et al. (2014) · Nucleic Acids Research · doi:10.1093/nar/gkt954 · Cited by 75
PAX3 Expression in Normal Skin Melanocytes and Melanocytic Lesions (Naevi and Melanomas)
Medic, S., & Ziman, M. R. (2010) · PLoS ONE · doi:10.1371/journal.pone.0009977 · Cited by 71
Liang, B., Soka, M. J., Christensen, A. H., OLESEN, M. S., Larsen, A. P., Knop, F. K., Wang, F., Nielsen, J. B., Andersen, M. N., Humphreys, D. T., et al. (2014) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2013.12.014 · Cited by 71
Signal transduction in early heart development (I): cardiogenic induction and heart tube formation.
Wagner, M. A., & Siddiqui, M. A. Q. (2007) · PubMed · Cited by 68
Loss of RNA expression and allele-specific expression associated with congenital heart disease
McKean, D. M., Homsy, J. G., Wakimoto, H., Patel, N., Gorham, J., DePalma, S. R., Ware, J. S., Zaidi, S., Ma, W., Patel, N., et al. (2016) · Nature Communications · doi:10.1038/ncomms12824 · Cited by 68
Self-citationYuan, F., Qiu, X., Li, R., Qu, X., Wang, J., Xu, Y., Liu, X., Fang, W., Yang, Y., & De-ning, L. (2014) · International Journal of Molecular Medicine · doi:10.3892/ijmm.2014.2029 · Cited by 67
Luo, M. H., Li, Y. S., & Yang, K. (2006) · Cardiology · doi:10.1159/000095501 · Cited by 58
Bouveret, R., Waardenberg, A. J., Schonrock, N., Ramialison, M., Doan, T., de Jong, D., Bondue, A., Kaur, G., Mohamed, S., Fonoudi, H., et al. (2015) · eLife · doi:10.7554/elife.06942 · Cited by 57
Gpr116 Receptor Regulates Distinctive Functions in Pneumocytes and Vascular Endothelium
Niaudet, C., Hofmann, J. J., Mäe, M. A., Jung, B., Gaengel, K., Vanlandewijck, M., Ekvärn, E., Salvado, M. D., Mehlem, A., Sayegh, S. A., et al. (2015) · PLoS ONE · doi:10.1371/journal.pone.0137949 · Cited by 57
Ashraf, H. M., Pradhan, L., Chang, E. I., Terada, R., Ryan, N. J., Briggs, L. E., Chowdhury, R. R., Zárate, M. A., Sugi, Y., Nam, H.-J., et al. (2014) · Circulation Cardiovascular Genetics · doi:10.1161/circgenetics.113.000281 · Cited by 54
Myocardium and BMP signaling are required for endocardial differentiation
Desai, S. P., Rost, M. S., Schumacher, J. A., Ton, Q. V., Craig, M. P., Baltrunaite, K., Koenig, A. L., Wang, J., Poss, K. D., Chi, N. C., et al. (2015) · Development · doi:10.1242/dev.118687 · Cited by 52
DeLaughter, D. M., Christodoulou, D. C., Robinson, J. Y., Seidman, C. E., Baldwin, H. S., Seidman, J. G., & Barnett, J. V. (2013) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2013.03.016 · Cited by 44
Self-citationTEF-1 and C/EBPβ are major p38α MAPK-regulated transcription factors in proliferating cardiomyocytes
Ambrosino, C., Iwata, T., Scafoglio, C., Mallardo, M., Klein, R., & Nebreda, Á. R. (2006) · Biochemical Journal · doi:10.1042/bj20051502 · Cited by 42
RNA-Mediated Regulation of HMGA1 Function
Benecke, A., & Eilebrecht, S. (2015) · Biomolecules · doi:10.3390/biom5020943 · Cited by 38
Bex1 knock out mice show altered skeletal muscle regeneration
Koo, J. H., Smiley, M. A., Lovering, R. M., & Margolis, F. L. (2007) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2007.08.186 · Cited by 35
How deep is enough in single-cell RNA-seq?
Streets, A., & Huang, Y. (2014) · Nature Biotechnology · doi:10.1038/nbt.3039 · Cited by 33
Identification of cardiovascular lineage descendants at single-cell resolution
Li, G., Plonowska‐Hirschfeld, K. A., Rajarajan, K., Sturzu, A. C., & Wu, S. M. (2015) · Development · doi:10.1242/dev.116897 · Cited by 27
Braybrook, C., Warry, G., Howell, G. R., Árnason, A., Björnsson, Á., Moore, G. E., Ross, M. T., & Stanier, P. (2001) · Genomics · doi:10.1006/geno.2000.6478 · Cited by 23
Nash, D. B., Arrington, C. B., Kennedy, B., Yandell, M. D., Wu, W., Zhang, W., Ware, S. M., Jorde, L. B., Gruber, P. J., Yost, H. J., et al. (2015) · PLoS ONE · doi:10.1371/journal.pone.0131514 · Cited by 22
Cited by
Integrating single-cell transcriptomic data across different conditions, technologies, and species
Butler, A., Hoffman, P., Smibert, P., Papalexi, E., & Satija, R. (2018) · Nature Biotechnology · doi:10.1038/nbt.4096 · Cited by 13,174
Cardiomyocyte Maturation: New Phase in Development
Guo, Y., & Pu, W. T. (2020) · Circulation Research · doi:10.1161/circresaha.119.315862 · Cited by 653
Self-citationMills, R. J., Titmarsh, D. M., Koenig, X., Parker, B. L., Ryall, J. G., Quaife-Ryan, G. A., Voges, H. K., Hodson, M. P., Ferguson, C., Drowley, L., et al. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1707316114 · Cited by 478
Friedman, C. E., Nguyen, Q., Lukowski, S. W., Helfer, A., Chiu, H. S., Miklas, J., Levy, S., Suo, S., Han, J.-D. J., Osteil, P., et al. (2018) · Cell Stem Cell · doi:10.1016/j.stem.2018.09.009 · Cited by 258
Churko, J. M., Garg, P., Treutlein, B., Venkatasubramanian, M., Wu, H., Lee, J., Wessells, Q. N., Chen, S.-Y., Chen, W.-Y., Chetal, K., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-07333-4 · Cited by 207
Metadata
- Authors
- DeLaughter, D. M., Bick, A. G., Wakimoto, H., McKean, D., Gorham, J. M., Kathiriya, I. S., Hinson, J. T., Homsy, J., Gray, J., Pu, W., Bruneau, B. G., Seidman, J. G., & Seidman, C. E.
- Venue
- Developmental Cell
- Publisher
- Elsevier BV
- Published
- 2016-11
- Volume
- 39
- Issue
- 4
- Pages
- 480-490
- ISSN
- 1534-5807 (ISSN-L)
- OpenAlex
- W2556548281
- Cited by
- 423
- References
- 54
- FWCI
- 18.96
- Type
- journal article
- Language
- en
- Open access
- bronze
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
Data sources
Bibliographic data: Semantic Scholar, OpenAlex, Crossref.
Contains information from the Semantic Scholar Academic Graph Datasets, made available under the ODC Attribution License (ODC-BY 1.0).
Semantic Scholar’s data is described in: Kinney, R., et al. (2023). The Semantic Scholar Open Data Platform. arXiv:2301.10140.