Cited by 181Pluripotent Stem Cells ResearchDevelopmental Biology and Gene RegulationEpigenetics and DNA Methylation

The DOI matches its Crossref record; 47 of the 47 references it cites were found in a registry or an index.

ELF5-enforced transcriptional networks define an epigenetically regulated trophoblast stem cell compartment in the human placenta

Hemberger, Myriam, Udayashankar, Ramya, Tesar, Paul, Moore, Harry, Burton, Graham J.·2010·Human Molecular Genetics

Open this paper in CoChat — free account

Abstract

The first definitive cell fate decision in development occurs at the blastocyst stage with establishment of the trophoblast and embryonic cell lineages. In the mouse, lineage commitment is achieved by epigenetic regulation of a critical gatekeeper gene, the transcription factor Elf5, that reinforces placental cell fate and is necessary for trophoblast stem (TS) cell self-renewal. In humans, however, the epigenetic lineage boundary seems to be less stringent since human embryonic stem (ES) cells, unlike their murine counterparts, harbour some potential to differentiate into trophoblast derivatives. Here, we show that ELF5 is expressed in the human placenta in villous cytotrophoblast cells but not in post-mitotic syncytiotrophoblast and invasive extravillous cytotrophoblast cells. ELF5 establishes a circuit of mutually interacting transcription factors with CDX2 and EOMES, and the highly proliferative ELF5(+)/CDX2(+) double-positive subset of cytotrophoblast cells demarcates a putative TS cell compartment in the early human placenta. In contrast to placental trophoblast, however, ELF5 is hypermethylated and largely repressed in human ES cells and derived trophoblast cell lines, as well as in induced pluripotent stem cells and murine epiblast stem cells. Thus, these cells exhibit an embryonic lineage-specific epigenetic signature and do not undergo an epigenetic reprogramming to reflect the trophoblast lineage at key loci such as ELF5. Our identification of the trophoblast-specific transcriptional circuit established by ELF5 will be instrumental to derive human TS cell lines that truly reflect early placental trophoblast and that will be most beneficial to gain insights into the aetiology of common pregnancy complications, including intra-uterine growth restriction and pre-eclampsia.

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

Crossref · 10.1093/hmg/ddq128

Cites

47 of 47 references verified0 citation errors · 0 not checkable

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?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Embryonic Stem Cell Lines Derived from Human Blastocysts
Thomson, J. A., Itskovitz‐Eldor, J., Shapiro, S. S., Waknitz, M. A., Swiergiel, J. J., Marshall, V. S., & Jones, J. M. (1998) · Science · doi:10.1126/science.282.5391.1145 · Cited by 15,947
Human DNA methylomes at base resolution show widespread epigenomic differences
Lister, R., Pelizzola, M., Dowen, R. H., Hawkins, R. D., Hon, G., Tonti-Filippini, J., Nery, J. R., Lee, L., Ye, Z., Ngo, Q.-M., et al. (2009) · Nature · doi:10.1038/nature08514 · Cited by 4,673
Targeted mutation of the DNA methyltransferase gene results in embryonic lethality
Li, E., Bestor, T. H., & Jaenisch, R. (1992) · Cell · doi:10.1016/0092-8674(92)90611-f · Cited by 3,984
Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells
Niwa, H., Miyazaki, J., & Smith, A. G. (2000) · Nature Genetics · doi:10.1038/74199 · Cited by 3,904
New cell lines from mouse epiblast share defining features with human embryonic stem cells
Tesar, P. J., Chenoweth, J. G., Brook, F. A., Davies, T. J., Evans, E. P., Mack, D. L., Gardner, R. L., & McKay, R. D. G. (2007) · Nature · doi:10.1038/nature05972 · Cited by 2,187
Self-citation
Derivation of pluripotent epiblast stem cells from mammalian embryos
Brons, I. G. M., Smithers, L. E., Trotter, M. W. B., Rugg‐Gunn, P. J., Sun, B., Lopes, S. M. C. D. S., Howlett, S., Clarkson, A., Ährlund‐Richter, L., Pedersen, R. A., et al. (2007) · Nature · doi:10.1038/nature05950 · Cited by 2,007
Promotion of Trophoblast Stem Cell Proliferation by FGF4
Tanaka, S., Kunath, T., Hadjantonakis, A., Nagy, A., & Rossant, J. (1998) · Science · doi:10.1126/science.282.5396.2072 · Cited by 1,370
The SRA protein Np95 mediates epigenetic inheritance by recruiting Dnmt1 to methylated DNA
Sharif, J., Muto, M., Takebayashi, S., Suetake, I., Iwamatsu, A., Endo, T. A., Shinga, J., Mizutani-Koseki, Y., Toyoda, T., Okamura, K., et al. (2007) · Nature · doi:10.1038/nature06397 · Cited by 1,360
The Uterine Spiral Arteries In Human Pregnancy: Facts and Controversies
Pijnenborg, R., Vercruysse, L., & HANSSENS, M. C. A. J. A. (2006) · Placenta · doi:10.1016/j.placenta.2005.12.006 · Cited by 1,229
Interaction between Oct3/4 and Cdx2 Determines Trophectoderm Differentiation
Niwa, H., Toyooka, Y., Shimosato, D., Strumpf, D., Takahashi, K., Yagi, R., & Rossant, J. (2005) · Cell · doi:10.1016/j.cell.2005.08.040 · Cited by 1,192

Show all 47 references

Sorted by citations

Derivation of Human Trophoblast Stem Cells
Okae, H., Toh, H., Sato, T., Hiura, H., Takahashi, S., Shirane, K., Kabayama, Y., Suyama, M., Sasaki, H., & Arima, T. (2017) · Cell stem cell · doi:10.1016/j.stem.2017.11.004 · Cited by 915
Human placenta and trophoblast development: key molecular mechanisms and model systems
Knöfler, M., Haider, S., Saleh, L., Pollheimer, J., Gamage, T. K. J. B., & James, J. L. (2019) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-019-03104-6 · Cited by 818
Placental Origins of Chronic Disease
Burton, G. J., Fowden, A. L., & Thornburg, K. L. (2016) · Physiological Reviews · doi:10.1152/physrev.00029.2015 · Cited by 717
Self-citation
Development of the human placenta
Turco, M. Y., & Moffett, A. (2019) · Development · doi:10.1242/dev.163428 · Cited by 742
Trophoblast organoids as a model for maternal–fetal interactions during human placentation
Turco, M. Y., Gardner, L., Kay, R. G., Hamilton, R. S., Prater, M., Hollinshead, M. S., McWhinnie, A., Esposito, L., Fernando, R. C., Skelton, H. E., et al. (2018) · Nature · doi:10.1038/s41586-018-0753-3 · Cited by 717
Self-citation
Distinct Lineage Specification Roles for NANOG, OCT4, and SOX2 in Human Embryonic Stem Cells
Wang, Z., Oron, E., Nelson, B., Razis, S., & Ivanova, N. B. (2012) · Cell stem cell · doi:10.1016/j.stem.2012.02.016 · Cited by 565
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 515
Self-citation
Self-Renewing Trophoblast Organoids Recapitulate the Developmental Program of the Early Human Placenta
Haider, S., Meinhardt, G., Saleh, L., Kunihs, V., Gamperl, M., Kaindl, U., Ellinger, A., Burkard, T. R., Fiala, C., Pollheimer, J., et al. (2018) · Stem Cell Reports · doi:10.1016/j.stemcr.2018.07.004 · Cited by 424
Establishment of porcine and human expanded potential stem cells
Gao, X., Nowak‐Imialek, M., Chen, X. X., Chen, D., Herrmann, D., Ruan, D., Chen, A. C. H., Eckersley-Maslin, M. A., Ahmad, S., Lee, Y. L., et al. (2019) · Nature Cell Biology · doi:10.1038/s41556-019-0333-2 · Cited by 395
BRACHYURY and CDX2 Mediate BMP-Induced Differentiation of Human and Mouse Pluripotent Stem Cells into Embryonic and Extraembryonic Lineages
Bernardo, A. S., Faial, T., Gardner, L., Niakan, K. K., Ortmann, D., Senner, C. E., Callery, E. M., Trotter, M. W. B., Hemberger, M., Smith, J. C., et al. (2011) · Cell stem cell · doi:10.1016/j.stem.2011.06.015 · Cited by 385
Self-citation
Analysis of human embryos from zygote to blastocyst reveals distinct gene expression patterns relative to the mouse
Niakan, K. K., & Eggan, K. C. (2012) · Developmental Biology · doi:10.1016/j.ydbio.2012.12.008 · Cited by 361
Derivation of trophoblast stem cells from naïve human pluripotent stem cells
Dong, C., Beltcheva, M., Gontarz, P. M., Zhang, B., Popli, P., Fischer, L. A., Khan, S. A., Park, K., Yoon, E., Xing, X., et al. (2020) · eLife · doi:10.7554/elife.52504 · Cited by 306
What Is Trophoblast? A Combination of Criteria Define Human First-Trimester Trophoblast
Lee, C. Q. E., Gardner, L., Turco, M. Y., Zhao, N., Murray, M. J., Coleman, N., Rossant, J., Hemberger, M., & Moffett, A. (2016) · Stem Cell Reports · doi:10.1016/j.stemcr.2016.01.006 · Cited by 292
Self-citation
Complete and unidirectional conversion of human embryonic stem cells to trophoblast by BMP4
Amita, M., Adachi, K., Alexenko, A. P., Sinha, S., Schust, D. J., Schulz, L. C., Roberts, R. M., & Ezashi, T. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1303094110 · Cited by 272
Human trophoblast stem cell self-renewal and differentiation: Role of decorin
Nandi, P., Lim, H. J., Torres-Garcia, E. J., & Lala, P. K. (2018) · Scientific Reports · doi:10.1038/s41598-018-27119-4 · Cited by 265
Rat placentation: An experimental model for investigating the hemochorial maternal-fetal interface
Soares, M. J., Chakraborty, D., Rumi, M. A. K., Konno, T., & Renaud, S. J. (2012) · Placenta · doi:10.1016/j.placenta.2011.11.026 · Cited by 219
Dissecting the dynamics of signaling events in the BMP, WNT, and NODAL cascade during self-organized fate patterning in human gastruloids
Chhabra, S., Liu, L., Goh, R., Kong, X., & Warmflash, A. (2019) · PLoS Biology · doi:10.1371/journal.pbio.3000498 · Cited by 198
Hemochorial placentation: development, function, and adaptations†
Soares, M. J., Varberg, K. M., & Iqbal, K. (2018) · Biology of Reproduction · doi:10.1093/biolre/ioy049 · Cited by 207
Comparative analysis of mouse and human placentae across gestation reveals species-specific regulators of placental development
Soncin, F., Khater, M., To, C. C., Pizzo, D. P., Farah, O., Wakeland, A. K., Rajan, K. A. N., Nelson, K. K., Chang, C., Moretto-Zita, M., et al. (2018) · Development · doi:10.1242/dev.156273 · Cited by 205
Signaling pathways in mouse and human trophoblast differentiation: a comparative review
Soncin, F., Natale, D. R. C., & Parast, M. M. (2014) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-014-1794-x · Cited by 162
Trophoblast Stem Cells1
Roberts, R. M., & Fisher, S. J. (2010) · Biology of Reproduction · doi:10.1095/biolreprod.110.088724 · Cited by 159
Human pluripotent stem cells as a model of trophoblast differentiation in both normal development and disease
Horii, M., Li, Y., Wakeland, A. K., Pizzo, D. P., Nelson, K. K., Sabatini, K., Laurent, L. C., Liu, Y., & Parast, M. M. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1604747113 · Cited by 153
TEAD4 ensures postimplantation development by promoting trophoblast self-renewal: An implication in early human pregnancy loss
Saha, B., Ganguly, A., Home, P., Bhattacharya, B., Ray, S. S., Ghosh, A., Rumi, M. A. K., Marsh, C. A., French, V. A., Gunewardena, S., et al. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2002449117 · Cited by 154
Notch1 controls development of the extravillous trophoblast lineage in the human placenta
Haider, S., Meinhardt, G., Saleh, L., Fiala, C., Pollheimer, J., & Knöfler, M. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1612335113 · Cited by 138
DNA Methylation and Development
Neidhart, M. (2015) · Elsevier eBooks · doi:10.1016/b978-0-12-420194-1.00013-0 · Cited by 139
Genome-wide expression profile of first trimester villous and extravillous human trophoblast cells
Apps, R., Sharkey, A., Gardner, L., Male, V. H., Trotter, M. W. B., Miller, N. G. A., North, R. A., Founds, S. A., & Moffett, A. (2010) · Placenta · doi:10.1016/j.placenta.2010.10.010 · Cited by 136
The cytotrophoblastic shell and complications of pregnancy
Burton, G. J., & Jauniaux, E. R. M. (2017) · Placenta · doi:10.1016/j.placenta.2017.06.007 · Cited by 138
Self-citation
BMP4-directed trophoblast differentiation of human embryonic stem cells is mediated through a ΔNp63+ cytotrophoblast stem cell state
Li, Y., Moretto-Zita, M., Soncin, F., Wakeland, A. K., Wolfe, L., Leon-Garcia, S., Pandian, R., Pizzo, D. P., Cui, L., Nazor, K. L., et al. (2013) · Development · doi:10.1242/dev.092155 · Cited by 131
Genetic Control of Early Cell Lineages in the Mammalian Embryo
Rossant, J. (2018) · Annual Review of Genetics · doi:10.1146/annurev-genet-120116-024544 · Cited by 131
The ever growing complexity of placental epigenetics – Role in adverse pregnancy outcomes and fetal programming
Novakovic, B., & Saffery, R. (2012) · Placenta · doi:10.1016/j.placenta.2012.10.003 · Cited by 127
From the stem of the placental tree: trophoblast stem cells and their progeny
Latos, P. A., & Hemberger, M. (2016) · Development · doi:10.1242/dev.133462 · Cited by 122
Self-citation
Establishment of Human Trophoblast Progenitor Cell Lines from the Chorion
Genbačev, O., Donne, M. L., Kapidzic, M., Gormley, M. J., Lamb, J. D., Gilmore, J., Larocque, N., Goldfien, G. A., Zdravkovic, T., McMaster, M., et al. (2011) · Stem Cells · doi:10.1002/stem.686 · Cited by 115
How trophoblasts fuse: an in-depth look into placental syncytiotrophoblast formation
Renaud, S. J., & Jeyarajah, M. J. (2022) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-022-04475-z · Cited by 115
Retroviruses facilitate the rapid evolution of the mammalian placenta
Chuong, E. B. (2013) · BioEssays · doi:10.1002/bies.201300059 · Cited by 115
Basic Structure of the Villous Trees
Benirschke, K., Burton, G. J., & Baergen, R. N. (2012) · Springer eBooks · doi:10.1007/978-3-642-23941-0_6 · Cited by 101
Self-citation
Direct Induction of Trophoblast Stem Cells from Murine Fibroblasts
Kubaczka, C., Senner, C. E., Cierlitza, M., Araúzo-Bravo, M. J., Kuckenberg, P., Peitz, M., Hemberger, M., & Schorle, H. (2015) · Cell stem cell · doi:10.1016/j.stem.2015.08.005 · Cited by 97
Self-citation
Stem cell insights into human trophoblast lineage differentiation
Gamage, T. K. J. B., Chamley, L., & James, J. L. (2016) · Human Reproduction Update · doi:10.1093/humupd/dmw026 · Cited by 98
Macrophage-Derived IL-33 Is a Critical Factor for Placental Growth
Fock, V., Mairhofer, M., Otti, G. R., Hiden, U., Spittler, A., Zeisler, H., Fiala, C., Knöfler, M., & Pollheimer, J. (2013) · The Journal of Immunology · doi:10.4049/jimmunol.1300490 · Cited by 96
Adaptive mechanisms controlling uterine spiral artery remodeling during the establishment of pregnancy
Soares, M. J., Chakraborty, D., Kubota, K., Renaud, S. J., & Rumi, M. A. K. (2014) · The International Journal of Developmental Biology · doi:10.1387/ijdb.140083ms · Cited by 91
Developmental differences in the expression of FGF receptors between human and mouse embryos
Kunath, T., Yamanaka, Y., Detmar, J., MacPhee, D. J., Caniggia, I., Rossant, J., & Jurisicova, A. (2014) · Placenta · doi:10.1016/j.placenta.2014.09.008 · Cited by 91
Two distinct trophectoderm lineage stem cells from human pluripotent stem cells
Mischler, A., Karakis, V., Mahinthakumar, J., Carberry, C. K., San‐Miguel, A., Rager, J. E., Fry, R. C., & Rao, B. M. (2021) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2021.100386 · Cited by 83
Innate Immune Mechanisms to Protect Against Infection at the Human Decidual-Placental Interface
Hoo, R., Nakimuli, A., & Vento‐Tormo, R. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.02070 · Cited by 84
Single-cell assessment of primary and stem cell-derived human trophoblast organoids as placenta-modeling platforms
Shannon, M. J., McNeill, G. L., Koksal, B., Baltayeva, J., Wächter, J., Castellana, B., Peñaherrera, M. S., Robinson, W. P., Leung, P. C. K., & Beristain, A. G. (2024) · Developmental Cell · doi:10.1016/j.devcel.2024.01.023 · Cited by 88
Isolation and Characterization of Human Trophoblast Side-Population (SP) Cells in Primary Villous Cytotrophoblasts and HTR-8/SVneo Cell Line
Takao, T., Asanoma, K., Kato, K., Fukushima, K., Tsunematsu, R., Hirakawa, T., Matsumura, S., Seki, H., Takeda, S., & Wake, N. (2011) · PLoS ONE · doi:10.1371/journal.pone.0021990 · Cited by 81
Genetic redundancy of GATA factors in extraembryonic trophoblast lineage ensures progression of both pre and postimplantation mammalian development
Home, P., Kumar, R. P., Ganguly, A., Saha, B., Milano-Foster, J., Bhattacharya, B., Ray, S. S., Gunewardena, S., Paul, A., Camper, S. A., et al. (2017) · Development · doi:10.1242/dev.145318 · Cited by 80
Epigenetic memory of the first cell fate decision prevents complete ES cell reprogramming into trophoblast
Cambuli, F., Murray, A., Dean, W., Dudzińska, D., Krueger, F., Andrews, S., Senner, C. E., Cook, S. J., & Hemberger, M. (2014) · Nature Communications · doi:10.1038/ncomms6538 · Cited by 80
Self-citation
ELF5 Suppresses Estrogen Sensitivity and Underpins the Acquisition of Antiestrogen Resistance in Luminal Breast Cancer
Kalyuga, M., Gallego‐Ortega, D., Lee, H. J., Roden, D. L., Cowley, M. J., Caldon, C. E., Stone, A. M., Allerdice, S. L., Valdés‐Mora, F., Launchbury, R., et al. (2012) · PLoS Biology · doi:10.1371/journal.pbio.1001461 · Cited by 84
Oxygen and placental development; parallels and differences with tumour biology
Burton, G. J., Jauniaux, E. R. M., & Murray, A. J. (2017) · Placenta · doi:10.1016/j.placenta.2017.01.130 · Cited by 81
Self-citation
Transcription factor networks in trophoblast development
Papúchová, H., & Latos, P. A. (2022) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-022-04363-6 · Cited by 80
Understanding and management of gestational trophoblastic disease
Ning, F., Hou, H., Morse, A. N., & Lash, G. E. (2019) · F1000Research · doi:10.12688/f1000research.14953.1 · Cited by 77
A placenta for life
John, R. M., & Hemberger, M. (2012) · Reproductive BioMedicine Online · doi:10.1016/j.rbmo.2012.03.018 · Cited by 77
Self-citation
Differentiation of trophoblast cells from human embryonic stem cells: to be or not to be?
Roberts, R. M., Loh, K. M., Amita, M., Bernardo, A. S., Adachi, K., Alexenko, A. P., Schust, D. J., Schulz, L. C., Telugu, B. P. V. L., Ezashi, T., et al. (2014) · Reproduction · doi:10.1530/rep-14-0080 · Cited by 76
Derivation of functional trophoblast stem cells from primed human pluripotent stem cells
Soncin, F., Morey, R. E., Bui, T., Requena, D. F., Cheung, V. C., Kallol, S., Kittle, R., Jackson, M. G., Farah, O., Chousal, J. N., et al. (2022) · Stem Cell Reports · doi:10.1016/j.stemcr.2022.04.013 · Cited by 74
A niche of trophoblast progenitor cells identified by integrin α2 is present in first trimester human placentas
Lee, C. Q. E., Turco, M. Y., Gardner, L., Simons, B. D., Hemberger, M., & Moffett, A. (2018) · Development · doi:10.1242/dev.162305 · Cited by 78
Self-citation
The role of transcription factor Tcfap2c/TFAP2C in trophectoderm development
Kuckenberg, P., Kubaczka, C., & Schorle, H. (2012) · Reproductive BioMedicine Online · doi:10.1016/j.rbmo.2012.02.015 · Cited by 73
Trophoblast development
Pfeffer, P., & Pearton, D. J. (2012) · Reproduction · doi:10.1530/rep-11-0374 · Cited by 72
Human Pre-gastrulation Development
Wamaitha, S. E., & Niakan, K. K. (2018) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2017.11.004 · Cited by 80
Epigenetic Mechanisms Influencing Epithelial to Mesenchymal Transition in Bladder Cancer
Monteiro‐Reis, S., Lobo, J., Henrique, R., & Jerónimo, C. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20020297 · Cited by 67
Modeling human trophoblast, the placental epithelium at the maternal fetal interface
Horii, M., Touma, O., Bui, T., & Parast, M. M. (2020) · Reproduction · doi:10.1530/rep-19-0428 · Cited by 72
Review: Histotrophic nutrition and the placental-endometrial dialogue during human early pregnancy
Burton, G. J., Cindrová‐Davies, T., & Turco, M. Y. (2020) · Placenta · doi:10.1016/j.placenta.2020.02.008 · Cited by 68
Self-citation
Cell dynamics in human villous trophoblast
Aplin, J., & Jones, C. J. P. (2021) · Human Reproduction Update · doi:10.1093/humupd/dmab015 · Cited by 70
HTR8/SVneo Cells Display Trophoblast Progenitor Cell-Like Characteristics Indicative of Self-Renewal, Repopulation Activity, and Expression of “Stemness-” Associated Transcription Factors
Weber, M., Knöfler, I., Schleußner, E., Markert, U. R., & Fitzgerald, J. S. (2013) · BioMed Research International · doi:10.1155/2013/243649 · Cited by 68
Transcription Factors That Regulate Trophoblast Development and Function
Baines, K. J., & Renaud, S. J. (2017) · Progress in molecular biology and translational science · doi:10.1016/bs.pmbts.2016.12.003 · Cited by 71
FGF4-dependent stem cells derived from rat blastocysts differentiate along the trophoblast lineage
Asanoma, K., Rumi, M. A. K., Kent, L. N., Chakraborty, D., Renaud, S. J., Wake, N., Lee, D.-S., Kubota, K., & Soares, M. J. (2011) · Developmental Biology · doi:10.1016/j.ydbio.2010.12.038 · Cited by 66
Regulation of early trophoblast differentiation – Lessons from the mouse
Senner, C. E., & Hemberger, M. (2010) · Placenta · doi:10.1016/j.placenta.2010.07.013 · Cited by 65
Self-citation
HCMV Infection of Human Trophoblast Progenitor Cells of the Placenta Is Neutralized by a Human Monoclonal Antibody to Glycoprotein B and Not by Antibodies to the Pentamer Complex
Zydek, M., Petitt, M., Fang-Hoover, J., Adler, B., Kauvar, L. M., Pereira, L., & Tabata, T. (2014) · Viruses · doi:10.3390/v6031346 · Cited by 64
Model systems for studying trophoblast differentiation from human pluripotent stem cells
Ezashi, T., Telugu, B. P. V. L., & Roberts, R. M. (2012) · Cell and Tissue Research · doi:10.1007/s00441-012-1371-2 · Cited by 58
Transcriptional regulators of the trophoblast lineage in mammals with hemochorial placentation
Knott, J. G., & Paul, S. (2014) · Reproduction · doi:10.1530/rep-14-0072 · Cited by 60
BAP1/ASXL complex modulation regulates epithelial-mesenchymal transition during trophoblast differentiation and invasion
Pérez-García, V., Lea, G., López‐Jiménez, P., Okkenhaug, H., Burton, G. J., Moffett, A., Turco, M. Y., & Hemberger, M. (2021) · eLife · doi:10.7554/elife.63254 · Cited by 56
Self-citation
Human primed and naïve PSCs are both able to differentiate into trophoblast stem cells
Viukov, S. V., Shani, T., Bayerl, J., Aguilera-Castrejon, A., Oldak, B., Sheban, D., Tarazi, S., Stelzer, Y., Hanna, J. H., & Novershtern, N. (2022) · Stem Cell Reports · doi:10.1016/j.stemcr.2022.09.008 · Cited by 63
The role of DNA methylation in human trophoblast differentiation
Gamage, T. K. J. B., Schierding, W. S., Hurley, D., Tsai, P., Ludgate, J. L., Bhoothpur, C., Chamley, L., Weeks, R. J., Macaulay, E. C., & James, J. L. (2018) · Epigenetics · doi:10.1080/15592294.2018.1549462 · Cited by 53
Establishment of the fetal-maternal interface: developmental events in human implantation and placentation
Huang, C.-C., Hsueh, Y., Chang, C., Hsu, H.-C., Yang, T., Lin, W.-C., & Chang, H. (2023) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2023.1200330 · Cited by 51
Architecture of Normal Villous Trees
Benirschke, K., Burton, G. J., & Baergen, R. N. (2012) · Springer eBooks · doi:10.1007/978-3-642-23941-0_7 · Cited by 52
Self-citation
The placenta: epigenetic insights into trophoblast developmental models of a generation-bridging organ with long-lasting impact on lifelong health
Hemberger, M., & Dean, W. (2023) · Physiological Reviews · doi:10.1152/physrev.00001.2023 · Cited by 48
Self-citation
MicroRNA analysis in placentas from patients with preeclampsia: comparison of new and published results
Betoni, J. S., Derr, K., Pahl, M. C., Rogers, L., Muller, C. L., Packard, R. E., Carey, D. J., Kuivaniemi, H., & Tromp, G. C. (2013) · Hypertension in Pregnancy · doi:10.3109/10641955.2013.807819 · Cited by 47
Decoding the molecular pathways governing trophoblast migration and placental development; a literature review
Liu, L., Tang, L., Chen, D., Zheng, L., & Ma, X. (2024) · Frontiers in Endocrinology · doi:10.3389/fendo.2024.1486608 · Cited by 52
Establishment of a novel human embryonic stem cell-derived trophoblastic spheroid implantation model
Lee, Y. L., Fong, S. W., Chen, A. C. H., Li, T., Yue, C., Lee, C., Ng, E. H. Y., Yeung, W. S. B., & Lee, C. (2015) · Human Reproduction · doi:10.1093/humrep/dev223 · Cited by 46
Isolation and characterisation of a novel trophoblast side-population from first trimester placentae
James, J. L., Hurley, D., Gamage, T. K. J. B., Zhang, T., Vather, R., Pantham, P., Murthi, P., & Chamley, L. (2015) · Reproduction · doi:10.1530/rep-14-0646 · Cited by 46
Calcium signaling in placenta
Baczyk, D., Kingdom, J. C., & Uhlén, P. (2011) · Cell Calcium · doi:10.1016/j.ceca.2010.12.003 · Cited by 46
5-Aza-dC treatment induces mesenchymal-to-epithelial transition in 1st trimester trophoblast cell line HTR8/SVneo
Chen, Y., Wang, K., & Leach, R. E. (2013) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2013.01.075 · Cited by 44
Hippo signaling cofactor, WWTR1, at the crossroads of human trophoblast progenitor self-renewal and differentiation
Ray, S. S., Saha, A., Ghosh, A., Roy, N., Kumar, R. P., Meinhardt, G., Mukerjee, A., Gunewardena, S., Kumar, R., Knöfler, M., et al. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2204069119 · Cited by 43
Human Placental Endothelial Cell and Trophoblast Heterogeneity and Differentiation Revealed by Single-Cell RNA Sequencing
Li, H., Peng, H., Hong, W., Wei, Y., Tian, H., Huang, X., Jia, L., Zheng, J. J., Duan, T., He, Q., et al. (2022) · Cells · doi:10.3390/cells12010087 · Cited by 45
Zfp281 Shapes the Transcriptome of Trophoblast Stem Cells and Is Essential for Placental Development
Ishiuchi, T., Ohishi, H., Sato, T., Kamimura, S., Yorino, M., Abe, S., Suzuki, A., Wakayama, T., Suyama, M., & Sasaki, H. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.04.028 · Cited by 43
The role of BMP4 signaling in trophoblast emergence from pluripotency
Roberts, R. M., Ezashi, T., Temple, J., Owen, J. R., Soncin, F., & Parast, M. M. (2022) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-022-04478-w · Cited by 43
ARID3A is required for mammalian placenta development
Rhee, C., Edwards, M., Dang, C., Harris, J., Brown, M., Kim, J., & Tucker, H. O. (2017) · Developmental Biology · doi:10.1016/j.ydbio.2016.12.003 · Cited by 42
The human placenta and its role in reproductive outcomes revisited
Aye, I. L. M. H., Tong, S., Jones, D. S., & Smith, G. C. S. (2025) · Physiological Reviews · doi:10.1152/physrev.00039.2024 · Cited by 49
Placenta-Specific Genes, Their Regulation During Villous Trophoblast Differentiation and Dysregulation in Preterm Preeclampsia
Szilágyi, A., Gelencsér, Z., Romero, R. J., Xu, Y., Király, P., Demeter, A., Pálhalmi, J., Györffy, B. A., Juhász, K., Hupuczi, P., et al. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21020628 · Cited by 42
Single-cell transcriptional profiling reveals cellular and molecular divergence in human maternal–fetal interface
Wang, Q., Li, J., Wang, S., Deng, Q., An, Y., Xing, Y., Dai, X., Li, Z., Ma, Q., Wang, K., et al. (2022) · Scientific Reports · doi:10.1038/s41598-022-14516-z · Cited by 40
Elf5, hormones and cell fate
Lee, H. J., & Ormandy, C. J. (2012) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2012.02.006 · Cited by 38
Epigenetic features of the mouse trophoblast
Rugg‐Gunn, P. J. (2012) · Reproductive BioMedicine Online · doi:10.1016/j.rbmo.2012.01.012 · Cited by 38
Elf5 inhibits TGF‐β‐driven epithelial‐mesenchymal transition in prostate cancer by repressing SMAD3 activation
Yao, B., Zhao, J., Li, Y., Li, H., Hu, Z., Pan, P., Zhang, Y., Du, E., Liu, R., & Xu, Y. (2015) · The Prostate · doi:10.1002/pros.22970 · Cited by 38
Modelling human placental villous development: designing cultures that reflect anatomy
James, J. L., Lissaman, A. C., Nursalim, Y. N. S., & Chamley, L. (2022) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-022-04407-x · Cited by 40
BMP4 regulation of human trophoblast development
Li, Y., & Parast, M. M. (2014) · The International Journal of Developmental Biology · doi:10.1387/ijdb.130341mp · Cited by 37
Regulatory Pathways Controlling the Endovascular Invasive Trophoblast Cell Lineage
Soares, M. J., Chakraborty, D., Renaud, S. J., Kubota, K., Bu, P., Konno, T., & Rumi, M. A. K. (2012) · Journal of Reproduction and Development · doi:10.1262/jrd.2011-039 · Cited by 35
From stem cells to spiral arteries: A journey through early placental development
James, J. L., Boss, A. L., Sun, C., Allerkamp, H. H., & Clark, A. R. (2021) · Placenta · doi:10.1016/j.placenta.2021.11.004 · Cited by 38
Overexpression of miR-210-3p Impairs Extravillous Trophoblast Functions Associated with Uterine Spiral Artery Remodeling
Hayder, H., Fu, G., Nadeem, L., O’Brien, J. A., Lye, S. J., & Peng, C. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22083961 · Cited by 30
Human trophoblast stem cells: Real or not real?
Chang, C., & Parast, M. M. (2017) · Placenta · doi:10.1016/j.placenta.2017.01.003 · Cited by 30
Embryonic signals perpetuate polar-like trophoblast stem cells and pattern the blastocyst axisPreprint
Frias-Aldeguer, J., Kip, M., Vivié, J., Li, L., Alemany, A., Korving, J., Darmis, F., van Oudenaarden, A., Geijsen, N., & Rivron, N. C. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/510362 · Cited by 30
Homeobox genes and down-stream transcription factor PPARγ in normal and pathological human placental development
Murthi, P., Kalionis, B., Cocquebert, M., Rajaraman, G., Chui, A., Keogh, R. J., Evain‐Brion, D., & Fournier, T. (2013) · Placenta · doi:10.1016/j.placenta.2013.01.005 · Cited by 29
New era of trophoblast research: integrating morphological and molecular approaches
Io, S., Kondoh, E., Chigusa, Y., Kawasaki, K., Mandai, M., & Yamada, A. S. (2020) · Human Reproduction Update · doi:10.1093/humupd/dmaa020 · Cited by 29

Authors: Hemberger, M., Udayashankar, R., Tesar, P., Moore, H., & Burton, G. J.
Affiliations: Babraham Institute (GB)
University of Sheffield (GB)
Case Western Reserve University (US)
University of Cambridge (GB)
Corresponding author: Hemberger, Myriam
ORCID: Hemberger, Myriam
Tesar, Paul
Moore, Harry
Burton, Graham J.
Venue: Human Molecular Genetics
Publisher: Oxford University Press (OUP)
Published: 2010-03-30
Volume: 19
Issue: 12
Pages: 2456-2467
ISSN: 0964-6906 (ISSN-L)
1460-2083
DOI: 10.1093/hmg/ddq128
OpenAlex: W2134873562
Cited by: 181
References: 47
Citations by year: 2026: 3 · 2025: 9 · 2024: 6 · 2023: 6 · 2022: 14 · 2021: 13 · 2020: 10 · 2019: 12 · 2018: 12 · 2017: 11 · 2016: 14 · 2015: 8 · 2014: 9 · 2013: 17 · 2012: 24
FWCI: 7.04
Type: journal article
Language: en
Open access: closed
Locations: Human Molecular Genetics (publishedVersion)
PubMed (publishedVersion)
Funders: Medical Research Council
Biotechnology and Biological Sciences Research Council (BBS/E/B/0000C230)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Pluripotent Stem Cells Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
Keywords: ELF5, trophoblast stem cells, human placenta, epigenetic regulation, transcriptional regulatory networks, CDX2, Eomes, cytotrophoblast, syncytiotrophoblast, extravillous cytotrophoblast, DNA methylation, human embryonic stem cells, induced pluripotent stem cells, epiblast stem cells, fetal growth restriction, preeclampsia
MeSH terms: CDX2 Transcription Factor, Animals, DNA-Binding Proteins, Female, Humans, Placenta, Pregnancy, Pregnancy Complications, Stem Cells, Transcription Factors, Trophoblasts, Homeodomain Proteins, Cell Lineage, DNA Methylation, Oligonucleotide Array Sequence Analysis, T-Box Domain Proteins, Pluripotent Stem Cells, Epigenesis, Genetic, Proto-Oncogene Proteins c-ets, Mice, Gene Regulatory Networks

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

ELF5-enforced transcriptional networks define an epigenetically regulated trophoblast stem cell compartment in the human placenta

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Self-check

Citations

Cites

Cited by

Related

Metadata

Record

About these checks