Epigenetic restriction of extraembryonic lineages mirrors the somatic transition to cancer
Open accessAbstract
In mammals, the canonical somatic DNA methylation landscape is established upon specification of the embryo proper and subsequently disrupted within many cancer types. However, the underlying mechanisms that direct this genome-scale transformation remain elusive, with no clear model for its systematic acquisition or potential developmental utility. Here, we analysed global remethylation from the mouse preimplantation embryo into the early epiblast and extraembryonic ectoderm. We show that these two states acquire highly divergent genomic distributions with substantial disruption of bimodal, CpG density-dependent methylation in the placental progenitor. The extraembryonic epigenome includes specific de novo methylation at hundreds of embryonically protected CpG island promoters, particularly those that are associated with key developmental regulators and are orthologously methylated across most human cancer types. Our data suggest that the evolutionary innovation of extraembryonic tissues may have required co-option of DNA methylation-based suppression as an alternative to regulation by Polycomb-group proteins, which coordinate embryonic germ-layer formation in response to extraembryonic cues. Moreover, we establish that this decision is made deterministically, downstream of promiscuously used-and frequently oncogenic-signalling pathways, via a novel combination of epigenetic cofactors. Methylation of developmental gene promoters during tumorigenesis may therefore reflect the misappropriation of an innate trajectory and the spontaneous reacquisition of a latent, developmentally encoded epigenetic landscape.
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
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.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The similarity between tumor and placenta methylomes suggests that tumorigenesis may represent a latent developmental epigenomic program.
“The similarity between tumor and placenta methylomes suggests that tumorigenesis may represent a latent developmental epigenomic program.”
From Dynamic DNA methylation: In the right place at the right time (2018) · cites this paper as [46]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Hallmarks of Cancer: The Next Generation
Hanahan, D., & Weinberg, R. A. (2011) · Cell · doi:10.1016/j.cell.2011.02.013 · Cited by 66,590 · see citing works
An integrated encyclopedia of DNA elements in the human genome
The ENCODE Project Consortium (2012) · Nature · doi:10.1038/nature11247 · Cited by 18,072 · see citing works
Buenrostro, J. D., Giresi, P. G., Zaba, L. C., Chang, H. Y., & Greenleaf, W. J. (2013) · Nature Methods · doi:10.1038/nmeth.2688 · Cited by 6,422 · see citing works
Integrative analysis of 111 reference human epigenomes
Roadmap Epigenomics Consortium, Kundaje, A., Meuleman, W., Ernst, J., Bilenky, M., Yen, A., Heravi-Moussavi, A., Kheradpour, P., Zhang, Z., Wang, J., et al. (2015) · Nature · doi:10.1038/nature14248 · Cited by 6,368 · see citing works
Self-citationFull-length RNA-seq from single cells using Smart-seq2
Picelli, S., Faridani, O. R., Björklund, Å. K., Winberg, G., Sagasser, S., & Sandberg, R. (2014) · Nature Protocols · doi:10.1038/nprot.2014.006 · Cited by 4,137 · see citing works
Wang, H., Yang, H., Shivalila, C. S., Dawlaty, M. M., Cheng, A. W., Zhang, F., & Jaenisch, R. (2013) · Cell · doi:10.1016/j.cell.2013.04.025 · Cited by 3,495 · see citing works
The ground state of embryonic stem cell self-renewal
Ying, Q.-L., Wray, J., Nichols, J., Batlle-Morera, L., Doble, B., Woodgett, J., Cohen, P., & Smith, A. (2008) · Nature · doi:10.1038/nature06968 · Cited by 3,442 · see citing works
CpG islands and the regulation of transcription
Deaton, A. M., & Bird, A. (2011) · Genes & Development · doi:10.1101/gad.2037511 · Cited by 3,187 · see citing works
DNA methylation: roles in mammalian development
Smith, Z. D., & Meissner, A. (2013) · Nature Reviews Genetics · doi:10.1038/nrg3354 · Cited by 3,045 · see citing works
Self-citationGenome-scale DNA methylation maps of pluripotent and differentiated cells
Meissner, A., Mikkelsen, T. S., Gu, H., Wernig, M., Hanna, J., Sivachenko, A., Zhang, X., Bernstein, B. E., Nusbaum, C., Jaffe, D. B., et al. (2008) · Nature · doi:10.1038/nature07107 · Cited by 2,536 · see citing works
Self-citationBen‐Porath, I., Thomson, M., Carey, V. J., Ge, R., Bell, G. W., Regev, A., & Weinberg, R. A. (2008) · Nature Genetics · doi:10.1038/ng.127 · Cited by 2,523 · see citing works
Irizarry, R. A., Ladd-Acosta, C., Wen, B., Wu, Z., Montano, C., Onyango, P., Cui, H., Gabo, K., Rongione, M., Webster, M., et al. (2009) · Nature Genetics · doi:10.1038/ng.298 · Cited by 2,177 · see citing works
Ying, Q.-L., Nichols, J., Chambers, I., & Smith, A. G. (2003) · Cell · doi:10.1016/s0092-8674(03)00847-x · Cited by 2,114 · see citing works
<i>DNMT3A</i> Mutations in Acute Myeloid Leukemia
Ley, T. J., Ding, L., Walter, M. J., McLellan, M. D., Lamprecht, T., Larson, D. E., Kandoth, C., Payton, J. E., Baty, J., Welch, J., et al. (2010) · New England Journal of Medicine · doi:10.1056/nejmoa1005143 · Cited by 1,983 · see citing works
The epigenetic progenitor origin of human cancer
Feinberg, A. P., OHLSSON, R. I., & Henikoff, S. (2005) · Nature Reviews Genetics · doi:10.1038/nrg1748 · Cited by 1,851 · see citing works
DNMT3L connects unmethylated lysine 4 of histone H3 to de novo methylation of DNA
Ooi, S. K. T., Qiu, C., Bernstein, E., Li, K., Jia, D., Yang, Z., Erdjument‐Bromage, H., Tempst, P., Lin, S., Allis, C. D., et al. (2007) · Nature · doi:10.1038/nature05987 · Cited by 1,558 · see citing works
Hoadley, K. A., Yau, C. S. F., Wolf, D. M., Cherniack, A. D., Tamborero, D., Ng, S., Leiserson, M. D. M., Niu, B., McLellan, M. D., Uzunangelov, V., et al. (2014) · Cell · doi:10.1016/j.cell.2014.06.049 · Cited by 1,500 · see citing works
Charting a dynamic DNA methylation landscape of the human genome
Ziller, M. J., Gu, H., Müller, F., Donaghey, J., Tsai, L. T.-Y., Kohlbacher, O., De Jager, P. L., Rosen, E. D., Bennett, D. A., Bernstein, B. E., et al. (2013) · Nature · doi:10.1038/nature12433 · Cited by 1,357 · see citing works
Self-citationEpigenetic plasticity and the hallmarks of cancer
Flavahan, W. A., Gaskell, E., & Bernstein, B. E. (2017) · Science · doi:10.1126/science.aal2380 · Cited by 1,340 · see citing works
DNMT1 and DNMT3b cooperate to silence genes in human cancer cells
Rhee, I. P., Bachman, K. E., Park, B. H., Jair, K.-W., Yen, R.-W. C., Schuebel, K. E., Cui, H., Feinberg, A. P., Christoph Lengauer, C., Kinzler, K. W., et al. (2002) · Nature · doi:10.1038/416552a · Cited by 1,243 · see citing works
Schlesinger, Y., Straussman, R., Keshet, I., Farkash, S., Hecht, M., Zimmerman, J., Eden, E., Yakhini, Z., Ben-Shushan, E., Reubinoff, B. E., et al. (2007) · Nature Genetics · doi:10.1038/ng1950 · Cited by 1,226 · see citing works
Epigenetic stem cell signature in cancer
Widschwendter, M., Fiegl, H., Egle, D., Mueller-Holzner, E., Spizzo, G., Marth, C., Weisenberger, D. J., Campan, M., Young, J., Jacobs, I., et al. (2007) · Nature Genetics · doi:10.1038/ng1941 · Cited by 1,143 · see citing works
Ohm, J. E., McGarvey, K. M., Yu, X., Cheng, L., Schuebel, K. E., Cope, L., Mohammad, H. P., Chen, W., Daniel, V. C., Yu, W., et al. (2007) · Nature Genetics · doi:10.1038/ng1972 · Cited by 1,130 · see citing works
A unique regulatory phase of DNA methylation in the early mammalian embryo
Smith, Z. D., Chan, M. M., Mikkelsen, T. S., Gu, H., Gnirke, A., Regev, A., & Meissner, A. (2012) · Nature · doi:10.1038/nature10960 · Cited by 964 · see citing works
Self-citationCHOPCHOP v2: a web tool for the next generation of CRISPR genome engineering
Labun, K., Montague, T. G., Gagnon, J. A., Thyme, S. B., & Valen, E. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw398 · Cited by 910 · see citing works
Making a commitment: cell lineage allocation and axis patterning in the early mouse embryo
Arnold, S. J., & Robertson, E. J. (2009) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2618 · Cited by 816 · see citing works
Chromatin state dynamics during blood formation
Lara-Astiaso, D., Weiner, A., Lorenzo-Vivas, E., Zaretsky, I., Jaitin, D. A., David, E., Keren-Shaul, H., Mildner, A., Winter, D., Jung, S., et al. (2014) · Science · doi:10.1126/science.1256271 · Cited by 776 · see citing works
Gu, H., Smith, Z. D., Bock, C., Boyle, P., Gnirke, A., & Meissner, A. (2011) · Nature Protocols · doi:10.1038/nprot.2010.190 · Cited by 750 · see citing works
Self-citationG&T-seq: parallel sequencing of single-cell genomes and transcriptomes
Macaulay, I. C., Haerty, W., Kumar, P., Li, Y. I., Hu, T. X., Teng, M. J., Goolam, M., Saurat, N., Coupland, P., Shirley, L. M., et al. (2015) · Nature Methods · doi:10.1038/nmeth.3370 · Cited by 750 · see citing works
Blackledge, N. P., Farcas, A. M., Kondo, T., King, H. W., McGouran, J. F., Hanssen, L. L. P., Ito, S., Cooper, S., Kondo, K., Koseki, Y., et al. (2014) · Cell · doi:10.1016/j.cell.2014.05.004 · Cited by 734 · see citing works
Dynamic CpG island methylation landscape in oocytes and preimplantation embryos
Smallwood, S. A., Tomizawa, S.-I., Krueger, F., Ruf, N., Carli, N., Segonds-Pichon, A., Sato, S., Hata, K., Andrews, S., & Kelsey, G. (2011) · Nature Genetics · doi:10.1038/ng.864 · Cited by 701 · see citing works
Arman, E., Haffner‐Krausz, R., Chen, Y., Heath, J. K., & Lonai, P. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.9.5082 · Cited by 614 · see citing works
Suppression of Erk signalling promotes ground state pluripotency in the mouse embryo
Nichols, J., Silva, J., Roode, M., & Smith, A. G. (2009) · Development · doi:10.1242/dev.038893 · Cited by 601 · see citing works
DNA methylation dynamics of the human preimplantation embryo
Smith, Z. D., Chan, M. M., Humm, K. C., Karnik, R., Mekhoubad, S., Regev, A., Eggan, K. C., & Meissner, A. (2014) · Nature · doi:10.1038/nature13581 · Cited by 580 · see citing works
Self-citationRecurrent DNMT3A mutations in patients with myelodysplastic syndromes
Walter, M. J., Ding, L., Shen, D., Shao, J., Grillot, M., McLellan, M., Fulton, R., Schmidt, H., Kalicki-Veizer, J., O'Laughlin, M., et al. (2011) · Leukemia · doi:10.1038/leu.2011.44 · Cited by 527 · see citing works
Naive pluripotency is associated with global DNA hypomethylation
Leitch, H. G., McEwen, K. R., Turp, A., Encheva, V., Carroll, T., Grabole, N., Mansfield, W., Nashun, B., Knezovich, J. G., Smith, A., et al. (2013) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2510 · Cited by 516 · see citing works
Epigenetic memory at embryonic enhancers identified in DNA methylation maps from adult mouse tissues
Hon, G. C., Rajagopal, N., Shen, Y., McCleary, D. F., Yue, F., Dang, M. D., & Ren, B. (2013) · Nature Genetics · doi:10.1038/ng.2746 · Cited by 457 · see citing works
Raychaudhuri, S., Plenge, R. M., Rossin, E. J., Ng, A., Purcell, S., Sklar, P. B., Scolnick, E. M., Xavier, R. J., Altshuler, D., & Daly, M. J. (2009) · PLoS Genetics · doi:10.1371/journal.pgen.1000534 · Cited by 422 · see citing works
Landau, D. A., Clement, K., Ziller, M. J., Boyle, P., Fan, J., Gu, H., Stevenson, K. E., Sougnez, C. L., Wang, L., Li, S., et al. (2014) · Cancer Cell · doi:10.1016/j.ccell.2014.10.012 · Cited by 385 · see citing works
Self-citationSchep, A. N., Buenrostro, J. D., Denny, S. K., Schwartz, K., Sherlock, G., & Greenleaf, W. J. (2015) · Genome Research · doi:10.1101/gr.192294.115 · Cited by 375 · see citing works
Fbxl10/Kdm2b Recruits Polycomb Repressive Complex 1 to CpG Islands and Regulates H2A Ubiquitylation
Wu, X., Johansen, J. V., & Helin, K. (2013) · Molecular Cell · doi:10.1016/j.molcel.2013.01.016 · Cited by 375 · see citing works
Wu, H., Xu, T., Feng, H., Chen, L., Li, B., Yao, B., Qin, Z. S., Jin, P., & Conneely, K. N. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv715 · Cited by 350 · see citing works
Ralston, A., & Rossant, J. (2007) · Developmental Biology · doi:10.1016/j.ydbio.2007.10.054 · Cited by 340 · see citing works
He, J., Shen, L., Wan, M., Taranova, O., Wu, H., & Zhang, Y. (2013) · Nature Cell Biology · doi:10.1038/ncb2702 · Cited by 316 · see citing works
Schroeder, D. I., Blair, J. D., Lott, P. C., Yu, H. O. K., Hong, D., Crary-Dooley, F. K., Ashwood, P., Walker, C. K., Korf, I. F., Robinson, W. P., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1215145110 · Cited by 310 · see citing works
Landan, G., Cohen, N. M., Mukamel, Z., Bar, A., Molchadsky, A., Brosh, R., Horn-Saban, S., Zalcenstein, D. A., Goldfinger, N., Zundelevich, A., et al. (2012) · Nature Genetics · doi:10.1038/ng.2442 · Cited by 305 · see citing works
Kang, M., Piliszek, A., Artus, J., & Hadjantonakis, A.-K. (2013) · Development · doi:10.1242/dev.084996 · Cited by 284 · see citing works
Dnmt3a loss predisposes murine hematopoietic stem cells to malignant transformation
Mayle, A., Yang, L., Rodriguez, B., Zhou, T., Chang, E., Curry, C. V., Challen, G. A., Li, W., Wheeler, D., Rebel, V. I., et al. (2015) · Blood · doi:10.1182/blood-2014-08-594648 · Cited by 235 · see citing works
Loss of the extraembryonic ectoderm in Elf5 mutants leads to defects in embryonic patterning
Donnison, M. J., Beaton, A., Davey, H. W., Broadhurst, R. B., L'Huillier, P. J., & Pfeffer, P. (2005) · Development · doi:10.1242/dev.01819 · Cited by 213 · see citing works
Auclair, G., Guibert, S., Bender, A., & Weber, M. (2014) · Genome biology · doi:10.1186/s13059-014-0545-5 · Cited by 189 · see citing works
Regulation of DNA Methylation by the Ras Signaling Pathway
MacLeod, A. R., Rouleau, J., & Moshe Szyf, A. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.19.11327 · Cited by 185 · see citing works
Piezo-actuated mouse intracytoplasmic sperm injection (ICSI)
Yoshida, N., & Perry, A. C. F. (2007) · Nature Protocols · doi:10.1038/nprot.2007.7 · Cited by 174 · see citing works
A KRAS-directed transcriptional silencing pathway that mediates the CpG island methylator phenotype
Serra, R. W., Fang, M., Park, S. M., Hutchinson, L., & Green, M. R. (2014) · eLife · doi:10.7554/elife.02313 · Cited by 166 · see citing works
Ras-MAPK signaling promotes trophectoderm formation from embryonic stem cells and mouse embryos
Lu, C.-W., Yabuuchi, A., Chen, L., Viswanathan, S. R., Kim, K., & Daley, G. Q. (2008) · Nature Genetics · doi:10.1038/ng.173 · Cited by 164 · see citing works
Expression of the T-box gene Eomesodermin during early mouse development
Ciruna, B. G., & Rossant, J. (1999) · Mechanisms of Development · doi:10.1016/s0925-4773(98)00243-3 · Cited by 154 · see citing works
FBXL10 protects Polycomb-bound genes from hypermethylation
Boulard, M., Edwards, J. R., & Bestor, T. H. (2015) · Nature Genetics · doi:10.1038/ng.3272 · Cited by 153 · see citing works
Maternal DNA Methylation Regulates Early Trophoblast Development
Branco, M. R., King, M. R., Pérez-García, V., Bogutz, A., Caley, M. P., Fineberg, E., Lefebvre, L., Cook, S. J., Dean, W., Hemberger, M., et al. (2016) · Developmental Cell · doi:10.1016/j.devcel.2015.12.027 · Cited by 146 · see citing works
Goldin, S. N., & Papaioannou, V. E. (2003) · genesis · doi:10.1002/gene.10192 · Cited by 135 · see citing works
DNMT3A loss drives enhancer hypomethylation in FLT3-ITD-associated leukemias
Yang, L.-B., Rodriguez, B., Mayle, A., Park, H., Lin, X.-Q., Luo, M., Jeong, M., Curry, C., Kim, S., Ruau, D., et al. (2016) · Cancer Cell · doi:10.1016/j.ccell.2016.05.003 · Cited by 135 · see citing works
Suppression of Intestinal Neoplasia by Deletion of Dnmt3b
Lin, H., Yamada, Y., Nguyen, S. P., Linhart, H., Jackson‐Grusby, L., Meissner, A., Meletis, K., Lo, G., & Jaenisch, R. (2006) · Molecular and Cellular Biology · doi:10.1128/mcb.26.8.2976-2983.2006 · Cited by 104 · see citing works
Self-citationCdx2 regulation of posterior development through non-Hox targets
Savory, J. G. A., Bouchard, N., Pierre, V. J., Rijli, F. M., Repentigny, Y. D., Kothary, R., & Lohnes, D. (2009) · Development · doi:10.1242/dev.041582 · Cited by 102 · see citing works
Genes methylated by DNA methyltransferase 3b are similar in mouse intestine and human colon cancer
Steine, E. J., Ehrich, M., Bell, G. W., Raj, A., Reddy, S., van Oudenaarden, A., Jaenisch, R., & Linhart, H. (2011) · Journal of Clinical Investigation · doi:10.1172/jci43169 · Cited by 65 · see citing works
Novakovic, B., & Saffery, R. (2013) · Frontiers in Genetics · doi:10.3389/fgene.2013.00285 · Cited by 49 · see citing works
Increased DNA methylation of Dnmt3b targets impairs leukemogenesis
Schulze, I., Rohde, C., Scheller, M., Bäumer, N., Krause, A., Herbst, F., Riemke, P., Hebestreit, K., Tschanter, P., Lin, Q., et al. (2016) · Blood · doi:10.1182/blood-2015-07-655928 · Cited by 41 · see citing works
Isolation and Maintenance of Mouse Epiblast Stem Cells
Chenoweth, J. G., & Tesar, P. J. (2010) · Methods in molecular biology · doi:10.1007/978-1-60761-691-7_2 · Cited by 33 · see citing works
Haney, S. L., Upchurch, G. M., Opavska, J., Klinkebiel, D. L., Hlady, R. A., Suresh, A., Pirruccello, S. J., Shukla, V., Lu, R., Costinean, S., et al. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.04.004 · Cited by 33 · see citing works
Abnormal X chromosome inactivation and sex-specific gene dysregulation after ablation of FBXL10
Boulard, M., Edwards, J. R., & Bestor, T. H. (2016) · Epigenetics & Chromatin · doi:10.1186/s13072-016-0069-1 · Cited by 20 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
The diverse roles of DNA methylation in mammalian development and disease
Greenberg, M., & Bourc’his, D. (2019) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-019-0159-6 · Cited by 2,160 · see citing works
Advances in epigenetics link genetics to the environment and disease
Cavalli, G., & Heard, E. (2019) · Nature · doi:10.1038/s41586-019-1411-0 · Cited by 1,509 · see citing works
DNA methylation: a historical perspective
Mattei, A. L., Bailly, N., & Meissner, A. (2022) · Trends in Genetics · doi:10.1016/j.tig.2022.03.010 · Cited by 876 · see citing works
Self-citationDynamic DNA methylation: In the right place at the right time
Luo, C., Hajkova, P., & Ecker, J. R. (2018) · Science · doi:10.1126/science.aat6806 · Cited by 668 · see citing works
How the Warburg effect supports aggressiveness and drug resistance of cancer cells?
Icard, P., Shulman, S. D., Farhat, D., Steyaert, J., Alifano, M., & Lincet, H. (2018) · Drug Resistance Updates · doi:10.1016/j.drup.2018.03.001 · Cited by 648 · see citing works
Mechanisms of early placental development in mouse and humans
Hemberger, M., Hanna, C. W., & Dean, W. (2019) · Nature Reviews Genetics · doi:10.1038/s41576-019-0169-4 · Cited by 492 · see citing works
DNA hypermethylation in disease: mechanisms and clinical relevance
Ehrlich, M. (2019) · Epigenetics · doi:10.1080/15592294.2019.1638701 · Cited by 375 · see citing works
Role of Mammalian DNA Methyltransferases in Development
Chen, Z., & Zhang, Y. (2019) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-103019-102815 · Cited by 377 · see citing works
Transgenerational Epigenetic Inheritance
Bošković, A., & Rando, O. J. (2018) · Annual Review of Genetics · doi:10.1146/annurev-genet-120417-031404 · Cited by 348 · see citing works
Transposable elements shape the evolution of mammalian development
Senft, A. D., & Macfarlan, T. S. (2021) · Nature Reviews Genetics · doi:10.1038/s41576-021-00385-1 · Cited by 276 · see citing works
DNA methylation in mammalian development and disease
Smith, Z. D., Hetzel, S., & Meissner, A. (2024) · Nature Reviews Genetics · doi:10.1038/s41576-024-00760-8 · Cited by 280 · see citing works
Self-citationInsights into epigenetic patterns in mammalian early embryos
Xu, R., Li, C., Liu, X., & Gao, S. (2021) · Protein & Cell · doi:10.1007/s13238-020-00757-z · Cited by 216 · see citing works
Dynamic epigenomic landscapes during early lineage specification in mouse embryos
Zhang, Y., Xiang, Y.-L., Yin, Q.-Z., Du, Z., Peng, X., Wang, Q.-J., Fidalgo, M., Xia, W., Li, Y.-Y., Zhao, Z.-A., et al. (2017) · Nature Genetics · doi:10.1038/s41588-017-0003-x · Cited by 192 · see citing works
Cinkornpumin, J. K., Kwon, S. Y., Guo, Y., Hossain, I., Sirois, J., Russett, C. S., Tseng, H.-W., Okae, H., Arima, T., Duchaîne, T. F., et al. (2020) · Stem Cell Reports · doi:10.1016/j.stemcr.2020.06.003 · Cited by 189 · see citing works
Regulation, functions and transmission of bivalent chromatin during mammalian development
Macrae, T. A., Fothergill-Robinson, J., & Ramalho‐Santos, M. (2022) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-022-00518-2 · Cited by 186 · see citing works
The road ahead in genetics and genomics
McGuire, A. L., Gabriel, S., Tishkoff, S. A., Wonkam, A., Chakravarti, A., Furlong, E. E. M., Treutlein, B., Meissner, A., Chang, H. Y., López-Bigas, N., et al. (2020) · Nature Reviews Genetics · doi:10.1038/s41576-020-0272-6 · Cited by 188 · see citing works
Self-citationDnmt1 has de novo activity targeted to transposable elements
Haggerty, C., Kretzmer, H., Riemenschneider, C., Kumar, A. S., Mattei, A. L., Bailly, N., Gottfreund, J., Gießelmann, P., Weigert, R., Brändl, B., et al. (2021) · Nature Structural & Molecular Biology · doi:10.1038/s41594-021-00603-8 · Cited by 171 · see citing works
Self-citationExploring the links between cancer and placenta development
Costanzo, V., Bardelli, A., Siena, S., & Abrignani, S. (2018) · Open Biology · doi:10.1098/rsob.180081 · Cited by 167 · see citing works
Dahlet, T., Lleida, A. A., Adhami, H. A., Dumas, M., Bender, A., Ngondo, R. P., Tanguy, M., Vallet, J., Auclair, G., Bardet, A. F., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-16919-w · Cited by 159 · see citing works
Self-patterning of human stem cells into post-implantation lineages
Pedroza, M., Gassaloglu, S. I., Dias, N., Zhong, L., Hou, T.-C. J., Kretzmer, H., Smith, Z. D., & Sözen, B. (2023) · Nature · doi:10.1038/s41586-023-06354-4 · Cited by 149 · see citing works
Self-citationThe dualistic origin of human tumors
Liu, J. (2018) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2018.07.004 · Cited by 148 · see citing works
Interplay between chromatin marks in development and disease
Janssen, S. M., & Lorincz, M. C. (2021) · Nature Reviews Genetics · doi:10.1038/s41576-021-00416-x · Cited by 141 · see citing works
Epigenetic regulator function through mouse gastrulation
Grosswendt, S., Kretzmer, H., Smith, Z. D., Kumar, A. S., Hetzel, S., Wittler, L., Klages, S., Timmermann, B., Mukherji, S., & Meissner, A. (2020) · Nature · doi:10.1038/s41586-020-2552-x · Cited by 132 · see citing works
Self-citationTodd, C. D., Deniz, Ö., Taylor, D., & Branco, M. R. (2019) · eLife · doi:10.7554/elife.44344 · Cited by 141 · see citing works
Chen, Z., Yin, Q., Inoue, A., Zhang, C., & Zhang, Y. (2019) · Science Advances · doi:10.1126/sciadv.aay7246 · Cited by 118 · see citing works
Rebooting the Epigenomes during Mammalian Early Embryogenesis
Xia, W., & Xie, W. (2020) · Stem Cell Reports · doi:10.1016/j.stemcr.2020.09.005 · Cited by 111 · see citing works
A DNMT3A PWWP mutation leads to methylation of bivalent chromatin and growth retardation in mice
Sendžikaitė, G., Hanna, C. W., Stewart-Morgan, K. R., Ivanova, E., & Kelsey, G. (2019) · Nature Communications · doi:10.1038/s41467-019-09713-w · Cited by 109 · see citing works
Epigenetic Reprogramming in Early Animal DevelopmentPreprint
Du, Z., Zhang, K., & Xie, W. (2021) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a039677 · Cited by 103 · see citing works
Spatiotemporal transcriptomic maps of whole mouse embryos at the onset of organogenesis
Kumar, A. S., Tian, L., Bolondi, A., Hernández, A. A., Stickels, R. R., Kretzmer, H., Murray, E. M., Wittler, L., Walther, M., Barakat, G., et al. (2023) · Nature Genetics · doi:10.1038/s41588-023-01435-6 · Cited by 105 · see citing works
Self-citationRegulation of human trophoblast gene expression by endogenous retroviruses
Frost, J. M., Amante, S. M., Okae, H., Jones, E. M., Ashley, B., Lewis, R. M., Cleal, J. K., Caley, M. P., Arima, T., Maffucci, T., et al. (2023) · Nature Structural & Molecular Biology · doi:10.1038/s41594-023-00960-6 · Cited by 94 · see citing works
Andrews, S., Krueger, C., Mellado-López, M., Hemberger, M., Dean, W., Pérez-García, V., & Hanna, C. W. (2023) · Nature Communications · doi:10.1038/s41467-023-36019-9 · Cited by 95 · see citing works
Global delay in nascent strand DNA methylation
Charlton, J., Downing, T. L., Smith, Z. D., Gu, H., Clement, K., Pop, R., Akopian, V., Klages, S., Santos, D. P., Tsankov, A. M., et al. (2018) · Nature Structural & Molecular Biology · doi:10.1038/s41594-018-0046-4 · Cited by 94 · see citing works
Self-citationYagi, M., Kabata, M., Tanaka, A., Ukai, T., Ohta, S., Nakabayashi, K., Shimizu, M., Hata, K., Meissner, A., Yamamoto, T., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-16989-w · Cited by 89 · see citing works
Self-citationInto the multiverse: advances in single-cell multiomic profiling
Ogbeide, S., Giannese, F., Mincarelli, L., & Macaulay, I. C. (2022) · Trends in Genetics · doi:10.1016/j.tig.2022.03.015 · Cited by 82 · see citing works
Hijacking of transcriptional condensates by endogenous retroviruses
Asimi, V., Kumar, A. S., Niskanen, H., Riemenschneider, C., Hetzel, S., Naderi, J., Fasching, N., Popitsch, N. P., Du, M., Kretzmer, H., et al. (2022) · Nature Genetics · doi:10.1038/s41588-022-01132-w · Cited by 77 · see citing works
Self-citationThe DNMT1 inhibitor GSK-3484862 mediates global demethylation in murine embryonic stem cells
Portilho, N. A., Saini, D., Hossain, I., Sirois, J., Moraes, C., & Pastor, W. A. (2021) · Epigenetics & Chromatin · doi:10.1186/s13072-021-00429-0 · Cited by 69 · see citing works
Dunican, D. S., Mjoseng, H. K., Duthie, L., Flyamer, I. M., Bickmore, W. A., & Meehan, R. R. (2020) · BMC Biology · doi:10.1186/s12915-020-0752-3 · Cited by 66 · see citing works
Zhang, B., Kim, M. Y., Elliot, G., Zhou, Y., Zhao, G., Li, D., Lowdon, R. F., Gormley, M. J., Kapidzic, M., Robinson, J. F., et al. (2021) · Developmental Cell · doi:10.1016/j.devcel.2021.04.001 · Cited by 66 · see citing works
ATR expands embryonic stem cell fate potential in response to replication stress
Atashpaz, S., Shams, S. S., Gonzalez, J. M., Sebestyén, E., Arghavanifard, N., Gnocchi, A., Albers, E., Minardi, S. P., Fagà, G., Soffientini, P., et al. (2020) · eLife · doi:10.7554/elife.54756 · Cited by 65 · see citing works
Mulholland, C. B., Nishiyama, A., Ryan, J., Nakamura, R., Yiğit, M., Glück, I. M., Trummer, C., Qin, W., Bartoschek, M. D., Traube, F. R., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-19603-1 · Cited by 71 · see citing works
ZFP57 regulation of transposable elements and gene expression within and beyond imprinted domains
Shi, H., Strogantsev, R., Takahashi, N., Kazachenka, A., Lorincz, M., Hemberger, M., & Ferguson-Smith, A. (2019) · Epigenetics & Chromatin · doi:10.1186/s13072-019-0295-4 · Cited by 60 · see citing works
Smart-RRBS for single-cell methylome and transcriptome analysis
Gu, H., Raman, A. T., Wang, X., Gaiti, F., Chaligné, R., Mohammad, A. W., Arczewska, A., Smith, Z. D., Landau, D. A., Aryee, M. J., et al. (2021) · Nature Protocols · doi:10.1038/s41596-021-00571-9 · Cited by 64 · see citing works
Self-citationSOX17 in cellular reprogramming and cancer
Tan, D. S., Holzner, M., Weng, M., Srivastava, Y., & Jauch, R. (2019) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2019.08.008 · Cited by 67 · see citing works
Andergassen, D., Smith, Z. D., Kretzmer, H., Rinn, J. L., & Meissner, A. (2021) · Developmental Cell · doi:10.1016/j.devcel.2021.10.010 · Cited by 60 · see citing works
Self-citationYue, Y., Ren, L., Zhang, C., Miao, K., Tan, K., Yang, Q., Hu, Y., Xi, G., Luo, G., Yang, M., et al. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2201168119 · Cited by 54 · see citing works
Acute lymphoblastic leukemia displays a distinct highly methylated genome
Hetzel, S., Mattei, A. L., Kretzmer, H., Qu, C., Chen, X. '., Fan, Y., Wu, G., Roberts, K. G., Luger, S. M., Litzow, M. R., et al. (2022) · Nature Cancer · doi:10.1038/s43018-022-00370-5 · Cited by 52 · see citing works
Self-citationVlahos, A., Mansell, T., Saffery, R., & Novakovic, B. (2019) · PLoS Genetics · doi:10.1371/journal.pgen.1008236 · Cited by 52 · see citing works
Yang, P., Meng, M., & Zhou, Q. (2021) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2021.188558 · Cited by 47 · see citing works
Hemberger, M., & Dean, W. (2023) · Physiological Reviews · doi:10.1152/physrev.00001.2023 · Cited by 47 · see citing works
Dmitrijeva, M., Ossowski, S., Serrano, L. G., & Schaefer, M. H. (2018) · Nucleic Acids Research · doi:10.1093/nar/gky498 · Cited by 45 · see citing works
The Coevolution of Placentation and Cancer
Wagner, G. P., Gupta, K., Dighe, A., & Levchenko, A. (2021) · Annual Review of Animal Biosciences · doi:10.1146/annurev-animal-020420-031544 · Cited by 45 · see citing works
Genetic Variants in Preeclampsia: Lessons From Studies in Latin-American Populations
Michita, R. T., Kaminski, V. D. L., & Chies, J. A. B. (2018) · Frontiers in Physiology · doi:10.3389/fphys.2018.01771 · Cited by 45 · see citing works
The Intrinsic and Extrinsic Effects of Tet Proteins During Gastrulation
Cheng, S., Mittnenzweig, M., Mayshar, Y., Lifshitz, A., Dunjić, M., Rais, Y., Ben-Yair, R., Gehrs, S., Chomsky, E., Mukamel, Z., et al. (2021) · Cell · doi:10.1016/j.cell.2022.06.049 · Cited by 44 · see citing works
Yang, X., Hu, B., Liao, J., Qiao, Y., Chen, Y., Qian, Y., Feng, S., Yu, F., Dong, J., Hou, Y., et al. (2019) · Cell Research · doi:10.1038/s41422-019-0234-8 · Cited by 40 · see citing works
Reawakening the Developmental Origins of Cancer Through Transposable Elements
Lynch‐Sutherland, C. F., Chatterjee, A., Stockwell, P. A., Eccles, M. R., & Macaulay, E. C. (2020) · Frontiers in Oncology · doi:10.3389/fonc.2020.00468 · Cited by 40 · see citing works
Vural, S., Palmisano, A., Reinhold, W. C., Pommier, Y. G., Teicher, B. A., & Krushkal, J. (2021) · Clinical Epigenetics · doi:10.1186/s13148-021-01026-4 · Cited by 41 · see citing works
Yang, X., Hu, B., Hou, Y., Qiao, Y., Wang, R., Chen, Y., Qian, Y., Feng, S., Chen, J., Liu, C., et al. (2018) · Cell Research · doi:10.1038/s41422-018-0010-1 · Cited by 39 · see citing works
Senft, A. D., Costello, I., King, H. W., Mould, A., Bikoff, E., & Robertson, E. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.07.077 · Cited by 36 · see citing works
Liu, J. (2021) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2021.06.007 · Cited by 38 · see citing works
Scarpato, R., Testi, S., Colosimo, V., García‐Crespo, C., Micheli, C., Azzarà, A., Tozzi, M. G., & Ghirri, P. (2019) · Mutation Research/Reviews in Mutation Research · doi:10.1016/j.mrrev.2019.108295 · Cited by 37 · see citing works
The need for more research into reproductive health and disease
Mercuri, N., & Cox, B. (2022) · eLife · doi:10.7554/elife.75061 · Cited by 24 · see citing works
De Novo DNA Methylation at Imprinted Loci during Reprogramming into Naive and Primed Pluripotency
Yagi, M., Kabata, M., Ukai, T., Ohta, S., Tanaka, A., Shimada, Y., Sugimoto, M., Araki, K., Okita, K., Woltjen, K., et al. (2019) · Stem Cell Reports · doi:10.1016/j.stemcr.2019.04.008 · Cited by 30 · see citing works
Targets and genomic constraints of ectopic Dnmt3b expression
Zhang, Y., Charlton, J., Karnik, R., Beerman, I., Smith, Z. D., Gu, H., Boyle, P., Mi, X., Clement, K., Pop, R., et al. (2018) · eLife · doi:10.7554/elife.40757 · Cited by 35 · see citing works
Self-citationEpigenetics and Pregnancy: Conditional Snapshot or Rolling Event
Andrawus, M., Sharvit, L. E., & Atzmon, G. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms232012698 · Cited by 34 · see citing works
Single-cell RNA-seq highlights a specific carcinoembryonic cluster in ovarian cancer
Zhao, H., Gao, Y., Miao, J., Chen, S., Li, J., Li, Z., Yin, C., & Yue, W. (2021) · Cell Death and Disease · doi:10.1038/s41419-021-04358-4 · Cited by 30 · see citing works
Evidence for Converging DNA Methylation Pathways in Placenta and Cancer
Lorincz, M. C., & Schübeler, D. (2017) · Developmental Cell · doi:10.1016/j.devcel.2017.10.009 · Cited by 28 · see citing works
Transition to naïve human pluripotency mirrors pan-cancer DNA hypermethylation
Patani, H., Rushton, M. D., Higham, J., Álvarez–Teijeiro, S., Oxley, D., Cutillas, P. R., Sproul, D., & Ficz, G. (2020) · Nature Communications · doi:10.1038/s41467-020-17269-3 · Cited by 29 · see citing works
Clark, S. J., Argelaguet, R., Lohoff, T., Krueger, F., Drage, D., Göttgens, B., Marioni, J. C., Nichols, J., & Reik, W. (2022) · Genome biology · doi:10.1186/s13059-022-02762-3 · Cited by 28 · see citing works
Hjort, L., Novakovic, B., Cvitic, S., Saffery, R., Damm, P., & Desoyé, G. (2022) · Epigenetics · doi:10.1080/15592294.2022.2111755 · Cited by 27 · see citing works
Kretzmer, H., Biran, A., Purroy, N., Lemvigh, C. K., Clement, K., Gruber, M., Gu, H., Rassenti, L. Z., Mohammad, A. W., Lesnick, C. E., et al. (2020) · Blood Cancer Discovery · doi:10.1158/2643-3230.bcd-19-0058 · Cited by 27 · see citing works
Self-citationAlteration of the brain methylation landscape following postnatal inflammatory injury in rat pups
Pierre, W. C., Legault, L., Londoño, I., McGraw, S., & Lodygensky, G. A. (2019) · The FASEB Journal · doi:10.1096/fj.201901461r · Cited by 25 · see citing works
Unique features and emerging in vitro models of human placental development
Shibata, S., Kobayashi, E. H., Kobayashi, N., Oike, A., Okae, H., & Arima, T. (2020) · Reproductive Medicine and Biology · doi:10.1002/rmb2.12347 · Cited by 26 · see citing works
Dissecting TET2 Regulatory Networks in Blood Differentiation and Cancer
Lazarenkov, A., & Sardina, J. L. (2022) · Cancers · doi:10.3390/cancers14030830 · Cited by 25 · see citing works
Dynamic antagonism between key repressive pathways maintains the placental epigenome
Weigert, R., Hetzel, S., Bailly, N., Haggerty, C., Ilik, İ., Yung, P. Y. K., Navarro, C., Bolondi, A., Kumar, A. S., Anania, C., et al. (2023) · Nature Cell Biology · doi:10.1038/s41556-023-01114-y · Cited by 26 · see citing works
Self-citationDvoriantchikova, G., Seemungal, R. J., & Ivanov, D. (2019) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2019.00182 · Cited by 25 · see citing works
ZMYM2 is essential for methylation of germline genes and active transposons in embryonic development
Graham-Paquin, A.-L., Saini, D., Sirois, J., Hossain, I., Katz, M. S., Zhuang, Q. K.-W., Kwon, S. Y., Yamanaka, Y., Bourque, G., Bouchard, M., et al. (2023) · Nucleic Acids Research · doi:10.1093/nar/gkad540 · Cited by 24 · see citing works
Xu, Z., Shi, J., Chen, Q., Yang, S., Wang, Z., Xiao, B., Lai, Z., Jing, Y., Li, Y., & Li, X. (2024) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2024.107990 · Cited by 25 · see citing works
Self-citationSu, K., Li, M., Lee, N.-W., Ho, B., Cheng, C.-L., Chuang, Y.-C., Yu, S., & Guo, Y. L. (2019) · Environmental Research · doi:10.1016/j.envres.2019.01.001 · Cited by 22 · see citing works
Araki, H., Miura, F., Watanabe, A., Morinaga, C., Kitaoka, F., Kitano, Y., Sakai, N., Shibata, Y., Terada, M., Goto, S., et al. (2019) · Stem Cell Reports · doi:10.1016/j.stemcr.2019.08.014 · Cited by 21 · see citing works
Get Out and Stay Out: New Insights Into DNA Methylation Reprogramming in Mammals
Greenberg, M. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.629068 · Cited by 21 · see citing works
Derrien, J., Guérin-Charbonnel, C., Gaborit, V., Campion, L., Devic, M., Douillard, E., Roi, N., Avet-Loiseau, H., Decaux, O., Facon, T., et al. (2020) · Genome Medicine · doi:10.1186/s13073-021-00938-3 · Cited by 23 · see citing works
Pang, H., Lei, D., Guo, Y., Yu, Y., Liu, T., Liu, Y., Chen, T., & Fan, C. (2022) · Frontiers in Oncology · doi:10.3389/fonc.2022.977618 · Cited by 22 · see citing works
Extraembryonic gut endoderm cells undergo programmed cell death during development
Batki, J., Hetzel, S., Schifferl, D., Bolondi, A., Walther, M., Wittler, L., Grosswendt, S., Herrmann, B. G., & Meissner, A. (2024) · Nature Cell Biology · doi:10.1038/s41556-024-01431-w · Cited by 21 · see citing works
Self-citationAyele, F. T., Biedrzycki, R. J., Habtewold, T. D., Wijesiriwardhana, P., Burt, A., Marsit, C. J., Ouidir, M., & Wapner, R. J. (2025) · Nature Communications · doi:10.1038/s41467-025-58128-3 · Cited by 21 · see citing works
Nye, T. M., Fernandez, N. L., & Simmons, L. A. (2020) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.1080/10409238.2020.1828257 · Cited by 21 · see citing works
Disabling de novo DNA methylation in embryonic stem cells allows an illegitimate fate trajectory
Kinoshita, M., Li, M. A., Barber, M., Mansfield, W. M., Dietmann, S., & Smith, A. G. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2109475118 · Cited by 20 · see citing works
Transcription of Endogenous Retroviruses: Broad and Precise Mechanisms of Control
Jarosz, A. S., & Halo, J. V. (2024) · Viruses · doi:10.3390/v16081312 · Cited by 19 · see citing works
Lea, G., Doria-Borrell, P., Ferrero-Micó, A., Varma, A., Simon, C. S., Anderson, H., Biggins, L., Clercq, K. D., Andrews, S., Niakan, K. K., et al. (2025) · Cell stem cell · doi:10.1016/j.stem.2024.12.007 · Cited by 19 · see citing works
Developmental genome-wide DNA methylation asymmetry between mouse placenta and embryo
Legault, L., Doiron, K., Lemieux, A., Caron, M., Chan, D., Lopes, F. L., Bourque, G., Sinnett, D., & McGraw, S. (2020) · Epigenetics · doi:10.1080/15592294.2020.1722922 · Cited by 18 · see citing works
Kita-Kyushu Lung Cancer Antigen-1 (KK-LC-1): A Promising Cancer Testis Antigen
Bai, R., & Yuan, C. (2022) · Aging and Disease · doi:10.14336/ad.2021.1207 · Cited by 17 · see citing works
GBE1 Promotes Glioma Progression by Enhancing Aerobic Glycolysis through Inhibition of FBP1
Chen, Z., Bao, H., Long, J., Zhao, P., Hu, X., Wang, H., Zhang, Y., Yang, J., Zhuge, Q., & Xia, L. (2023) · Cancers · doi:10.3390/cancers15051594 · Cited by 17 · see citing works
Blake, G. E. T., Zhao, X., Yung, H. W., Burton, G. J., Ferguson‐Smith, A. C., Hamilton, R. S., & Watson, E. D. (2021) · Nature Communications · doi:10.1038/s41467-021-24036-5 · Cited by 15 · see citing works
Blastocyst-Inspired Hydrogels to Maintain Undifferentiation of Mouse Embryonic Stem Cells
Hang, Y., Ma, X., Liu, C., Li, S., Zhang, S., Feng, R., Shang, Q., Liu, Q., Ding, Z., Zhang, X., et al. (2021) · ACS Nano · doi:10.1021/acsnano.0c10468 · Cited by 15 · see citing works
Distinctive aspects of the placental epigenome and theories as to how they arise
Pastor, W. A., & Kwon, S. Y. (2022) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-022-04568-9 · Cited by 15 · see citing works
Origin, fate and function of extraembryonic tissues during mammalian development
Thowfeequ, S., Hanna, C. W., & Srinivas, S. (2024) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-024-00809-w · Cited by 13 · see citing works
Transcriptional and epigenetic control of early life cell fate decisions
Al-Mousawi, J., & Bošković, A. (2022) · Current Opinion in Oncology · doi:10.1097/cco.0000000000000814 · Cited by 13 · see citing works
The DNA methylation haplotype (mHap) format and mHapTools
Zhang, Z., Dan, Y., Xu, Y., Zhang, J., Zheng, X., & Shi, J. (2021) · Bioinformatics · doi:10.1093/bioinformatics/btab458 · Cited by 13 · see citing works
Self-citationDivergent DNA methylation dynamics in marsupial and eutherian embryos
Leeke, B. J., Varsally, W., Ogushi, S., Zohren, J., Menchero, S., Courtois, A., Snell, D. M., Teissandier, A., Ojarikre, O. A., Mahadevaiah, S. K., et al. (2025) · Nature · doi:10.1038/s41586-025-08992-2 · Cited by 12 · see citing works
Disruption of maternal vascular remodeling by a fetal endoretrovirus-derived gene in preeclampsia
Gong, X., He, W., Jin, W., Ma, H., Wang, G., Li, J., Xiao, Y., Zhao, Y., Chen, Q., Guo, H., et al. (2024) · Genome biology · doi:10.1186/s13059-024-03265-z · Cited by 12 · see citing works
Fritsche, K., Boccellato, F., Schlaermann, P., Koeppel, M., Denecke, C., Link, A., Malfertheiner, P., Gut, I., Meyer, T. F., & Berger, H. (2022) · Clinical Epigenetics · doi:10.1186/s13148-022-01406-4 · Cited by 12 · see citing works
- Authors
- Smith, Z. D., Shi, J., Gu, H., Donaghey, J., Clement, K., Cacchiarelli, D., Gnirke, A., Michor, F., & Meissner, A.
- Affiliations
- Broad Institute (US)
- Harvard University (US)
- Corresponding author
- Meissner, Alexander
- ORCID
- Venue
- Nature
- Published
- 2017-09-20
- Volume
- 549
- Issue
- 7673
- Pages
- 543-547
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC5789792
- OpenAlex
- W2754109996
- Cited by
- 201
- References
- 67
- Citations by year
- 2026: 13 · 2025: 17 · 2024: 20 · 2023: 20 · 2022: 29 · 2021: 37 · 2020: 26 · 2019: 25 · 2018: 11 · 2017: 3
- FWCI
- 7.26
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Digital Access to Scholarship at Harvard (DASH) (Harvard University) (submittedVersion, cc-by)
- RePEc: Research Papers in Economics (submittedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion, other-oa)
- Funders
- New York Stem Cell Foundation (P01GM099117, R01DA036898)
- Starr Foundation (R01DA036898)
- Israel Science Foundation
- Max-Planck-Gesellschaft
- National Institutes of Health (5rm1hg006193-10, NIH U54CA193461)
- National Institute on Drug Abuse (R01DA036898)
- National Human Genome Research Institute (RM1‐HG006193, P50HG006193)
- National Cancer Institute (U54CA193461)
- National Institute of General Medical Sciences (P01GM099117)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (R01HD078679)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Syndromes and Imprinting
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Keywords
- DNA methylation, extraembryonic ectoderm, epiblast, preimplantation embryo, de novo methylation, CpG island promoters, developmental regulators, cancer epigenetics, Polycomb group proteins, mouse embryo development, carcinogenesis
- MeSH terms
- Animals, Blastocyst, Ectoderm, Female, Germ Layers, Humans, Male, Neoplasms, Placenta, Pregnancy, Promoter Regions, Genetic, Gene Expression Regulation, Neoplastic, Gene Expression Regulation, Developmental, CpG Islands, Cell Lineage, DNA Methylation, Epigenesis, Genetic, Mice
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
