The DOI matches its Crossref record; 13 of the 13 references it cites were found in a registry or an index.
Dynamic and Coordinated Epigenetic Regulation of Developmental Transitions in the Cardiac Lineage
Open accessAbstract
SUMMARY Heart development is exquisitely sensitive to the precise temporal regulation of thousands of genes that govern developmental decisions during differentiation. However, we currently lack a detailed understanding of how chromatin and gene expression patterns are coordinated during developmental transitions in the cardiac lineage. Here, we interrogated the transcriptome and several histone modifications across the genome during defined stages of cardiac differentiation. We find distinct chromatin patterns that are coordinated with stage-specific expression of functionally related genes, including many human disease-associated genes. Moreover, we discover a novel pre-activation chromatin pattern at the promoters of genes associated with heart development and cardiac function. We further identify stage-specific distal enhancer elements and find enriched DNA binding motifs within these regions that predict sets of transcription factors that orchestrate cardiac differentiation. Together, these findings form a basis for understanding developmentally regulated chromatin transitions during lineage commitment and the molecular etiology of 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
High-Resolution Profiling of Histone Methylations in the Human Genome
Barski, A., Cuddapah, S., Cui, K., Roh, T.-Y., Schones, D. E., Wang, Z., Wei, G., Chepelev, I., & Zhao, K. (2007) · Cell · doi:10.1016/j.cell.2007.05.009 · Cited by 6,845
GREAT improves functional interpretation of cis-regulatory regions
McLean, C. Y., Bristor, D., Hiller, M., Clarke, S. L., Schaar, B. T., Lowe, C. B., Wenger, A. M., & Bejerano, G. (2010) · Nature Biotechnology · doi:10.1038/nbt.1630 · Cited by 4,502
Genome-wide maps of chromatin state in pluripotent and lineage-committed cells
Mikkelsen, T. S., Ku, M., Jaffe, D. B., Issac, B., Lieberman, E., Giannoukos, G., Alvarez, P., Brockman, W., Kim, T.-K., Koche, R. P., et al. (2007) · Nature · doi:10.1038/nature06008 · Cited by 4,129
Heintzman, N. D., Stuart, R. K., Hon, G., Fu, Y., Ching, C. W., Hawkins, R. D., Barrera, L. O., Van Calcar, S., Qu, C., Ching, K. A., et al. (2007) · Nature Genetics · doi:10.1038/ng1966 · Cited by 3,398 · cited 1×
“Histone marks also predict noncoding DNA elements, such as distal enhancers, that regulate tissue-specific gene expression (Creyghton et al., 2010; Ernst et al., 2011; Heintzman et al., 2009; Heintzman et al., 2007; Rada-Iglesias et al., 2011; Zentner et al., 2011).”
Mapping and analysis of chromatin state dynamics in nine human cell types
Ernst, J., Kheradpour, P., Mikkelsen, T. S., Shoresh, N., Ward, L. D., Epstein, C. B., Zhang, X., Wang, L., Issner, R., Coyne, M., et al. (2011) · Nature · doi:10.1038/nature09906 · Cited by 2,898
Histone modifications at human enhancers reflect global cell-type-specific gene expression
Heintzman, N. D., Hon, G. C., Hawkins, R. D., Kheradpour, P., Stark, A., Harp, L. F., Ye, Z., Lee, L. K., Stuart, R. K., Ching, C. W., et al. (2009) · Nature · doi:10.1038/nature07829 · Cited by 2,533
Widespread transcription at neuronal activity-regulated enhancers
Kim, T.-K., Hemberg, M., Gray, J. M., Costa, A. M., Bear, D. M., Wu, J., Harmin, D. A., Laptewicz, M., Barbara-Haley, K., Kuersten, S., et al. (2010) · Nature · doi:10.1038/nature09033 · Cited by 2,450
A unique chromatin signature uncovers early developmental enhancers in humans
Rada-Iglesias, A., Bajpai, R., Swigut, T., Brugmann, S. A., Flynn, R. A., & Wysocka, J. (2011) · Nature · doi:10.1038/nature09692 · Cited by 2,233
Long Noncoding RNAs with Enhancer-like Function in Human Cells
Ørom, U. A., Derrien, T., Beringer, M., Gumireddy, K., Gardini, A., Bussotti, G., Lai, F., Zytnicki, M., Notredame, C., Huang, Q., et al. (2010) · Cell · doi:10.1016/j.cell.2010.09.001 · Cited by 1,721
Kattman, S. J., Witty, A. D., Gagliardi, M., Dubois, N. C., Niapour, M., Hotta, A., Ellis, J., & Keller, G. (2011) · Cell Stem Cell · doi:10.1016/j.stem.2010.12.008 · Cited by 1,159
Self-citation
Cited by
Modification of Enhancer Chromatin: What, How, and Why?
Calo, E., & Wysocka, J. (2013) · Molecular Cell · doi:10.1016/j.molcel.2013.01.038 · Cited by 1,457
Transcriptional enhancers: from properties to genome-wide predictions
Shlyueva, D., Stampfel, G., & Stark, A. (2014) · Nature Reviews Genetics · doi:10.1038/nrg3682 · Cited by 1,356
De novo mutations in histone-modifying genes in congenital heart disease
Zaidi, S., Choi, M., Wakimoto, H., Ma, L., Jiang, J., Overton, J. D., Romano-Adesman, A., Bjornson, R. D., Breitbart, R. E., Brown, K. K., et al. (2013) · Nature · doi:10.1038/nature12141 · Cited by 934
Contribution of rare inherited and de novo variants in 2,871 congenital heart disease probands
Jin, S. C., Homsy, J., Zaidi, S., Lu, Q., Morton, S., DePalma, S. R., Zeng, X., Qi, H., Chang, W., Sierant, M. C., et al. (2017) · Nature Genetics · doi:10.1038/ng.3970 · Cited by 875
Self-citationCore, L. J., Martins, A. L., Danko, C. G., Waters, C. T., Siepel, A., & Lis, J. T. (2014) · Nature Genetics · doi:10.1038/ng.3142 · Cited by 693
Pierpont, M. E., Brueckner, M., Chung, W. K., Garg, V., Lacro, R. V., McGuire, A. L., Mital, S., Priest, J. R., Pu, W. T., Roberts, A., et al. (2018) · Circulation · doi:10.1161/cir.0000000000000606 · Cited by 654
Chromatin modifiers and remodellers: regulators of cellular differentiation
Chen, T., & Dent, S. Y. R. (2014) · Nature Reviews Genetics · doi:10.1038/nrg3607 · Cited by 619
Rivera, C. M., & Ren, B. (2013) · Cell · doi:10.1016/j.cell.2013.09.011 · Cited by 550
Identification of Genetic Variants That Affect Histone Modifications in Human Cells
McVicker, G., van de Geijn, B., Degner, J. F., Cain, C. E., Banovich, N. E., Raj, A., Lewellen, N., Myrthil, M., Gilad, Y., & Pritchard, J. K. (2013) · Science · doi:10.1126/science.1242429 · Cited by 436
Transcriptional and Epigenetic Dynamics during Specification of Human Embryonic Stem Cells
Gifford, C. A., Ziller, M. J., Gu, H., Trapnell, C., Donaghey, J., Tsankov, A., Shalek, A. K., Kelley, D. R., Shishkin, A. A., Issner, R., et al. (2013) · Cell · doi:10.1016/j.cell.2013.04.037 · Cited by 435
Rapid and Pervasive Changes in Genome-wide Enhancer Usage during Mammalian Development
Nord, A. S., Blow, M. J., Attanasio, C., Akiyama, J. A., Holt, A., Hosseini, R., Phouanenavong, S., Plajzer-Frick, I., Shoukry, M., Afzal, V., et al. (2013) · Cell · doi:10.1016/j.cell.2013.11.033 · Cited by 375
Live-cell imaging reveals enhancer-dependent Sox2 transcription in the absence of enhancer proximity
Alexander, J. M., Guan, J., Li, B., Maliskova, L., Song, M., Shen, Y., Huang, B., Lomvardas, S., & Weiner, O. D. (2019) · eLife · doi:10.7554/elife.41769 · Cited by 346
Self-citationBroadly permissive intestinal chromatin underlies lateral inhibition and cell plasticity
Kim, T.-H., Li, F., Ferreiro-Neira, I., Ho, L.-L., Luyten, A., Nalapareddy, K., Long, H., Verzi, M., & Shivdasani, R. A. (2014) · Nature · doi:10.1038/nature12903 · Cited by 257
Self-citationCruz-Molina, S., Respuela, P., Tebartz, C., Kolovos, P., Nikolic, M., Fueyo, R., van Ijcken, W. F. J., Grosveld, F., Frommolt, P., Bazzi, H., et al. (2017) · Cell Stem Cell · doi:10.1016/j.stem.2017.02.004 · Cited by 240
Theodoris, C. V., Li, M., White, M. P., Liu, L., He, D., Pollard, K. S., Bruneau, B. G., & Srivastava, D. (2015) · Cell · doi:10.1016/j.cell.2015.02.035 · Cited by 210
Self-citationPsat1-Dependent Fluctuations in α-Ketoglutarate Affect the Timing of ESC Differentiation
Hwang, I.-Y., Kwak, S., Lee, S., Kim, H., Lee, S. E., Kim, J.-H., Kim, Y. A., Jeon, Y. K., Chung, D. H., Jin, X., et al. (2016) · Cell Metabolism · doi:10.1016/j.cmet.2016.06.014 · Cited by 180
Glucose inhibits cardiac muscle maturation through nucleotide biosynthesis
Nakano, H., Minami, I., Braas, D., Pappoe, H., Wu, X., Sagadevan, A., Vergnes, L., Fu, K., Morselli, M., Dunham, C., et al. (2017) · eLife · doi:10.7554/elife.29330 · Cited by 195
Lai, B., Lee, J.-E., Jang, Y., Wang, L., Peng, W., & Ge, K. (2017) · Nucleic Acids Research · doi:10.1093/nar/gkx234 · Cited by 191
Circadian Entrainment Triggers Maturation of Human In Vitro Islets
Alvarez-Dominguez, J. R., Donaghey, J., Rasouli, N., Kenty, J. H. R., Helman, A., Charlton, J., Straubhaar, J. R., Meissner, A., & Melton, D. A. (2020) · Cell Stem Cell · doi:10.1016/j.stem.2019.11.011 · Cited by 189
Evidence for additive and synergistic action of mammalian enhancers during cell fate determination
Choi, J., Lysakovskaia, K., Stik, G., Demel, C., Söding, J., Tian, T. V., Graf, T., & Cramer, P. (2021) · eLife · doi:10.7554/elife.65381 · Cited by 117
Genetic and epigenetic regulation of cardiomyocytes in development, regeneration and disease
Cui, M., Wang, Z., Bassel-Duby, R., & Olson, E. N. (2018) · Development · doi:10.1242/dev.171983 · Cited by 92
ERRγ enhances cardiac maturation with T-tubule formation in human iPSC-derived cardiomyocytes
Miki, K., Deguchi, K., Nakanishi-Koakutsu, M., Lucena-Cacace, A., Kondo, S., Fujiwara, Y., Hatani, T., Sasaki, M., Naka, Y., Okubo, C., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-23816-3 · Cited by 76
Genetic Networks Governing Heart Development
Waardenberg, A. J., Ramialison, M., Bouveret, R., & Harvey, R. P. (2014) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a013839 · Cited by 59
Zhu, J.-Y., Fu, Y., Nettleton, M., Richman, A., & Han, Z. (2017) · eLife · doi:10.7554/elife.22617 · Cited by 53
Yuan, X., Song, M., Devine, P., Bruneau, B. G., Scott, I. C., & Wilson, M. D. (2018) · Nature Communications · doi:10.1038/s41467-018-07451-z · Cited by 51
Self-citationWidespread Chromatin Accessibility at Repetitive Elements Links Stem Cells with Human Cancer
Gomez, N. C., Hepperla, A. J., Dumitru, R., Simon, J. M., Fang, F., & Davis, I. J. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.10.011 · Cited by 41
Navigating the non-coding genome in heart development and Congenital Heart Disease
Chahal, G., Tyagi, S., & Ramialison, M. (2019) · Differentiation · doi:10.1016/j.diff.2019.05.001 · Cited by 31
Gong, W., Koyano-Nakagawa, N., Li, T., & Garry, D. J. (2015) · BMC Bioinformatics · doi:10.1186/s12859-015-0460-0 · Cited by 26
Zhao, W., Yuan, W., Dong, T., Qi, W., Feng, Z., Li, C., & Sun, Y. (2025) · Communications Biology · doi:10.1038/s42003-025-08160-2 · Cited by 16
Epigenetic preparation of future gene induction kinetics
Xiong, J., & Zhu, B. (2025) · Annual Review of Genetics · doi:10.1146/annurev-genet-012825-093148 · Cited by 12
Metadata
- Authors
- 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., Erwin, G., Kattman, S. J., Keller, G. M., Srivastava, D., Levine, S. S., Pollard, K. S., Holloway, A. K., Boyer, L. A., & Bruneau, B. G.
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2012-09
- Volume
- 151
- Issue
- 1
- Pages
- 206-220
- ISSN
- 0092-8674 (ISSN-L)
- OpenAlex
- W2075928340
- Cited by
- 610
- References
- 13
- FWCI
- 20.91
- 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.