The DOI matches its Crossref record; 147 of the 147 references it cites were found in a registry or an index.
Making a commitment: cell lineage allocation and axis patterning in the early mouse embryo
Abstract
Genetic studies have identified the key signalling pathways and developmentally regulated transcription factors that govern cell lineage allocation and axis patterning in the early mammalian embryo. Recent advances have uncovered details of the molecular circuits that tightly control cell growth and differentiation in the mammalian embryo from the blastocyst stage, through the establishment of initial anterior-posterior polarity, to gastrulation, when the germ cells are set aside and the three primary germ layers are specified. Relevant studies in lower vertebrates indicate the conservation and divergence of regulatory mechanisms for cell lineage allocation and axis patterning.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
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?
In the citing paper
“Expression of markers of embryonic (em)VE, and anterior visceral endoderm (AVE), a specialized cellular cohort of emVE exhibiting an intra-epithelial, distal-to-anterior migratory behavior between E5.5 and E6.0, including Lefty1, Cer1 and Hhex30–32, suggested these EPI descendants resembled emVE and AVE (Fig. 2c, Extended Data Fig. 6e)33.”
From The emergent landscape of the mouse gut endoderm at single-cell resolution (2019) · cites this paper as [33]
In the citing paper
“The early post-implantation (E5.5, Fig. 1) mouse embryo is radially symmetrical, and the VE appears morphologically uniform around its proximal-distal axis4,33.”
From The emergent landscape of the mouse gut endoderm at single-cell resolution (2019) · cites this paper as [33]
Citations
Cites
Wnt/β-Catenin Signaling in Development and Disease
Clevers, H. (2006) · Cell · doi:10.1016/j.cell.2006.10.018 · Cited by 5,568
Massagué, J. (2008) · Cell · doi:10.1016/j.cell.2008.07.001 · Cited by 3,907
Cano, A., Pérez‐Moreno, M., Rodrigo, I., Locascio, A., Blanco, M. J., Barrio, M. G. D., Portillo, F., & Nieto, M. A. (2000) · Nature Cell Biology · doi:10.1038/35000025 · Cited by 3,672
Functional Expression Cloning of Nanog, a Pluripotency Sustaining Factor in Embryonic Stem Cells
Chambers, I., Colby, D., Robertson, M., Nichols, J., Lee, S., Tweedie, S., & Smith, A. G. (2003) · Cell · doi:10.1016/s0092-8674(03)00392-1 · Cited by 3,255
The Homeoprotein Nanog Is Required for Maintenance of Pluripotency in Mouse Epiblast and ES Cells
Mitsui, K., Tokuzawa, Y., Itoh, H., Segawa, K., Murakami, M., Takahashi, K., Maruyama, M., Maeda, M., & Yamanaka, S. (2003) · Cell · doi:10.1016/s0092-8674(03)00393-3 · Cited by 3,192
Epithelial-Mesenchymal Transition: At the Crossroads of Development and Tumor Metastasis
Yang, J., & Weinberg, R. A. (2008) · Developmental Cell · doi:10.1016/j.devcel.2008.05.009 · Cited by 3,079
Batlle, E., Sancho, E., Francí, C., Dominguez-Sola, D., Monfar, M., Baulida, J., & de Herreros, A. G. (2000) · Nature Cell Biology · doi:10.1038/35000034 · Cited by 2,730
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
Echelard, Y., Epstein, D. J., St-Jacques, B., Shen, L., Mohler, J., McMahon, J. A., & McMahon, A. P. (1993) · Cell · doi:10.1016/0092-8674(93)90627-3 · Cited by 2,154
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
Cited by
Sorted by citations
Items 201–300 of 816
Single-cell transcriptional profiling: a window into embryonic cell-type specification
Pijuan-Sala, B., Guibentif, C., & Göttgens, B. (2018) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-018-0002-5 · Cited by 57
Dzobo, K., Turnley, T., Wishart, A. L., Rowe, A., Kallmeyer, K., van Vollenstee, F. A., Thomford, N. E., Dandara, C., Chopera, D., Pepper, M. S., et al. (2016) · International Journal of Molecular Sciences · doi:10.3390/ijms17081259 · Cited by 55
Causes and evolutionary consequences of primordial germ-cell specification mode in metazoans
Whittle, C. A., & Extavour, C. G. M. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1610600114 · Cited by 58
Turner, D. A., Trott, J., Hayward, P. C., Rué, P., & Arias, A. M. (2014) · Biology Open · doi:10.1242/bio.20148409 · Cited by 55
“In the embryo, the blastocyst differentiates into the epiblast where, after implantation, within a single cell layered epithelium and under the influence of spatially organized signalling centres, cells are assigned to one of two fates: 1) an anteriorly located neural primordium or neuroectoderm (NECT), that will give…”
BackgroundRho GTPases in embryonic development
Duquette, P. M., & Lamarche‐Vane, N. (2014) · Small GTPases · doi:10.4161/sgtp.29716 · Cited by 57
“0 mouse embryos.(14) In Rac1-null embryos, the anterior-posterior body axis was impaired due to defects in migration of AVE cells.”
BackgroundInfluentialEMT and MET as paradigms for cell fate switching
Chen, J., Han, Q., & Pei, D. (2011) · Journal of Molecular Cell Biology · doi:10.1093/jmcb/mjr045 · Cited by 53
“0, which gives rise to ectoderm, mesoderm, and definitive endoderm (DE) (Arnold and Robertson, 2009) (Figure 1A).”
BackgroundNegrón‐Pérez, V. M., & Hansen, P. J. (2017) · Biology of Reproduction · doi:10.1093/biolre/iox172 · Cited by 55
“The first differentiation event in the mammalian embryo occurs when the totipotent morula goes through processes of compaction and cell polarization that lead to formation of the blastocyst containing a pluripotent inner cell mass (ICM), a differentiated trophectoderm (TE), and a blastocoel [1, 2].”
BackgroundAn in vitro stem cell model of human epiblast and yolk sac interaction
Mackinlay, K. M., Weatherbee, B. A. T., Rosa, V. S., Handford, C. E., Hudson, G., Coorens, T. H. H., Pereira, L. V., Behjati, S., Vallier, L., Shahbazi, M. N., et al. (2021) · eLife · doi:10.7554/elife.63930 · Cited by 52
Time-integrated BMP signaling determines fate in a stem cell model for early human development
Teague, S., Primavera, G., Chen, B., Liu, Z.-Y., Yao, L., Freeburne, E., Khan, H., Jo, K., Johnson, C. N., & Heemskerk, I. (2024) · Nature Communications · doi:10.1038/s41467-024-45719-9 · Cited by 58
“This problem is particularly acute in early mammalian development, where no maternal cues are present and signalinggradientsareformedinfeedback loopsbythesame cellsthat differentiate in response to them 4 .”
Bueno, D. F., Sunaga, D. Y., Kobayashi, G. S., Aguena, M., Raposo-Amaral, C. E., Masotti, C., Alvizi, L., Pearson, P. L., & Passos‐Bueno, M. R. (2010) · Stem Cell Reviews and Reports · doi:10.1007/s12015-010-9197-3 · Cited by 52
Costello, I., Biondi, C., Taylor, J. M., Bikoff, E. K., & Robertson, E. J. (2009) · BMC Developmental Biology · doi:10.1186/1471-213x-9-54 · Cited by 52
“In the early embryo, reciprocal signalling between the epiblast, extra-embryonic ectoderm (ExE) and the overlying visceral endoderm (VE) is responsible for axis patterning and specification of the germ layers (reviewed by [3,4]).”
BackgroundSelf-citationEpigenetic coordination of signaling pathways during the epithelial-mesenchymal transition
Cieslik, M. P., Hoang, S. A., Baranova, N. N., Chodaparambil, S. V., Kumar, M., Allison, D. F., Xu, X., Wamsley, J. J., Gray, L. G., Jones, D. R., et al. (2013) · Epigenetics & Chromatin · doi:10.1186/1756-8935-6-28 · Cited by 52
“Background Differentiation and lineage commitment occurs through a highly regulated sequence of cellular changes in response to the environment [1].”
BackgroundArtus, J., & Hadjantonakis, A. (2010) · Methods in molecular biology · doi:10.1007/978-1-60761-974-1_3 · Cited by 52
Argonaute 2 Is Required for Extra-embryonic Endoderm Differentiation of Mouse Embryonic Stem Cells
Ngondo, R. P., Cirera‐Salinas, D., Yu, J., Wischnewski, H., Bodak, M., Vandormael‐Pournin, S., Geiselmann, A., Wettstein, R., Luitz, J., Cohen‐Tannoudji, M., et al. (2018) · Stem Cell Reports · doi:10.1016/j.stemcr.2017.12.023 · Cited by 51
“…three lineages: the trophectoderm that will give rise to the Stem Cell Rep This is an open access article under the C placenta, the primitive endoderm (PrE) contributing to the yolk sac, and the epiblast (EPI), which will form the embryo proper (Arnold and Robertson, 2009; Rossant and Tam, 2009).”
BackgroundJang, S., Choubey, S., Furchtgott, L., Zou, L.-N., Doyle, A. M., Menon, V., Loew, E. B., Krostag, A.-R., Martinez, R. A., Madisen, L., et al. (2017) · eLife · doi:10.7554/elife.20487 · Cited by 52
“…Gata4 and Eomes, and endoderm cells by Sox17 and FoxA2, although in mouse these genes are shared between both lineages, with differences only in their timing and level of expression (Arnold and Robertson, 2009; Kanai-Azuma et al., 2002; Kim and Ong, 2012; Lumelsky et al., 2001; Rojas et al., 2005).”
BackgroundMechanisms of Pluripotency In Vivo and In Vitro
Pósfai, E., Tam, O. H., & Rossant, J. (2014) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/b978-0-12-416022-4.00001-9 · Cited by 54
Holoprosencephaly in the genomics era
Roessler, E., Hu, P., & Muenke, M. (2018) · American Journal of Medical Genetics Part C Seminars in Medical Genetics · doi:10.1002/ajmg.c.31615 · Cited by 52
“…axial mesendoderm (AME); specifically, it involves the most anterior extent of this notochord-like anterior extension the prechordal plate (PrCP) (Arnold & Robertson, 2009; Beddington & Robertson, 1999; Gritsman et al., 1999; Kiecker & Niehrs, 2001; Marlow et al., 1998; Robertson, 2014; K. Sulik…”
BackgroundGroote, P. D., Tran, H. T., Fransen, M., Tanghe, G., Urwyler-Rösselet, C., Craene, B. D., Leurs, K., Gilbert, B., Imschoot, G. V., Rycke, R. M. D., et al. (2014) · Cell Death and Differentiation · doi:10.1038/cdd.2014.191 · Cited by 49
Wang, P.-R., McKnight, K. D., Wong, D. J., Rodriguez, R. T., Sugiyama, T., Gu, X.-Y., Ghodasara, A., Qu, K., Chang, H. Y., & Kim, S. K. (2012) · Stem Cells and Development · doi:10.1089/scd.2011.0416 · Cited by 45
“…endoderm formation, patterning, and differentiation is the culmination of a dynamic, complex series of cell fate decisions and morphogenetic movements orchestrated by Wnt, Nodal/Activin, bone morphogenetic protein (BMP), fibroblast growth factor (FGF), and retinoic acid (RA) signaling [9–11].”
Lavagi, I., Krebs, S., Simmet, K., Beck, A. H., Zakhartchenko, V., Wolf, E., & Blum, H. (2018) · Scientific Reports · doi:10.1038/s41598-018-22248-2 · Cited by 52
SCL/TAL1 cooperates with Polycomb RYBP-PRC1 to suppress alternative lineages in blood-fated cells
Chagraoui, H., Kristiansen, M. S., Ruíz, J. P., Barros, A. S., Richter, J., Hall-Ponselé, E., Gray, N., Waithe, D., Clark, K., Hublitz, P., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-07787-6 · Cited by 46
Mesnard, D., Donnison, M. J., Fuerer, C., et al. (2011) · Genes & Development · doi:10.1101/gad.16738711 · Cited by 47
Notch signaling in the division of germ layers in bilaterian embryos
Favarolo, M. B., & López, S. L. (2018) · Mechanisms of Development · doi:10.1016/j.mod.2018.06.005 · Cited by 44
Extra-embryonic Wnt3 regulates the establishment of the primitive streak in mice
Yoon, Y., Huang, T., Tortelote, G. G., et al. (2015) · Developmental Biology · doi:10.1016/j.ydbio.2015.04.008 · Cited by 46
“Several lines of evidence suggest that Bmp4 emanating from the extra-embryonic ectoderm signals to the adjacent epiblast to activate primitive streak markers (Arnold and Robertson, 2009; Beddington and Robertson, 1999; Ben-Haim et al., 2006).”
BackgroundEpiblast stem cells contribute new insight into pluripotency and gastrulation
Chenoweth, J. G., McKay, R. D. G., & Tesar, P. J. (2010) · Development Growth & Differentiation · doi:10.1111/j.1440-169x.2010.01171.x · Cited by 46
“…that communicates with the overlying extra-embryonic tissues by means of factors including those from the transforming growth factor- b (TGF-b), ª 2010 The Authors Journal compilation ª 2010 Japanese Society of Developmental Biolog Wnt, and FGF families (reviewed in Arnold & Robertson 2009).”
BackgroundLineage Tracing: Computational Reconstruction Goes Beyond the Limit of Imaging.
Wu, S.-H. S., Lee, J., & Koo, B. (2019) · Europe PMC (PubMed Central) · doi:10.14348/molcells.2019.0006 · Cited by 46
“Subsequently, pluripotent cells differentiate and give rise to patterned tissues and organs with distinct functions (Arnold and Robertson, 2009).”
BackgroundMarangoni-like tissue flows enhance symmetry breaking of embryonic organoids
Gsell, S., Tlili, S., Merkel, M., & Lenne, P. (2025) · Nature Physics · doi:10.1038/s41567-025-02802-2 · Cited by 50
Rnf165/Ark2C Enhances BMP-Smad Signaling to Mediate Motor Axon Extension
Kelly, C. E., Thymiakou, E., Dixon, J. E., Tanaka, S., Godwin, J., & Episkopou, V. (2013) · PLoS Biology · doi:10.1371/journal.pbio.1001538 · Cited by 44
“Arkadia is required for head/anterior development in the mammalian embryo [34,35], which also depends on the establishment of high Nodal-Smad2/3 signaling [30].”
BackgroundFuerer, C., Nostro, M. C., & Constam, D. B. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m114.550301 · Cited by 46
Cui, W., Dai, X., Marcho, C., et al. (2016) · Scientific Reports · doi:10.1038/srep37396 · Cited by 44
Cellular diversity and lineage trajectory: insights from mouse single cell transcriptomes
Tam, P., & Ho, J. W. K. (2020) · Development · doi:10.1242/dev.179788 · Cited by 44
Transcription Factors: The Fulcrum Between Cell Development and Carcinogenesis
Islam, Z., Ali, A. M., Naik, A., Eldaw, M., Decock, J. V., & Kolatkar, P. R. (2021) · Frontiers in Oncology · doi:10.3389/fonc.2021.681377 · Cited by 46
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 43
Peng, G., Cui, G., Ke, J., & Jing, N. (2020) · Annual Review of Genomics and Human Genetics · doi:10.1146/annurev-genom-120219-083220 · Cited by 42
An ex vivo system to study cellular dynamics underlying mouse peri-implantation development
Ichikawa, T., Zhang, H. T., Panavaite, L., Erzberger, A., Fabrèges, D., Snajder, R., Wolny, A., Korotkevich, E., Tsuchida-Straeten, N., Hufnagel, L., et al. (2022) · Developmental Cell · doi:10.1016/j.devcel.2021.12.023 · Cited by 44
“In the embryo proper, implantation coincides with major changes in tissue architecture as it undergoes gastrulation and body axes specification (Arnold and Robertson, 2009; Rossant and Tam, 2009; Takaoka and Hamada, 2012).”
Epithelial-Mesenchymal Transition-Inducing Factors Involved in the Progression of Lung Cancers
Nam, M.-W., Kim, C., & Choi, K. (2022) · Biomolecules & Therapeutics · doi:10.4062/biomolther.2021.178 · Cited by 43
“gastrulation after apical constriction (Arnold and Robertson, 2009).”
BackgroundRepina, N. A., Johnson, H. J., Bao, X., Zimmermann, J. A., Joy, D. A., Bi, S. Z., Kane, R. S., & Schaffer, D. V. (2023) · Development · doi:10.1242/dev.201386 · Cited by 43
Glycolytic activity instructs germ layer proportions through regulation of Nodal and Wnt signaling
Stapornwongkul, K. S., Hahn, E., Poliński, P., Palau, L. S., Arató, K., Yao, L., Williamson, K., Gritti, N., Anlaş, K., Lopez, M. O., et al. (2025) · Cell stem cell · doi:10.1016/j.stem.2025.03.011 · Cited by 44
Establishment of epigenetic patterns in development
Leeb, M., & Wutz, A. (2012) · Chromosoma · doi:10.1007/s00412-012-0365-x · Cited by 46
“A number of studies have contributed to the understanding of patterning and lineage commitment in the mouse embryo (Arnold and Robertson 2009).”
BackgroundSignaling Roadmap Modulating Naive and Primed Pluripotency
Hassani, S., Totonchi, M., Gourabi, H., Schöler, H. R., & Baharvand, H. (2013) · Stem Cells and Development · doi:10.1089/scd.2013.0368 · Cited by 44
“The transcription factor Oct4 is considered to be the cardinal marker for ICM cells, whereas Cdx2 is a marker for epithelial TE cells [14].”
Murray, A., Sienerth, A. R., & Hemberger, M. (2016) · Scientific Reports · doi:10.1038/srep25112 · Cited by 41
Opening the black box: Stem cell–based modeling of human post-implantation development
Taniguchi, K., Heemskerk, I., & Gumucio, D. L. (2018) · The Journal of Cell Biology · doi:10.1083/jcb.201810084 · Cited by 43
“The AVE secretes antagonists of BMP, TGFβ/NOD AL, and WNT signaling such as CER1, LEF TY1, and DKK1, to specify anterior identity and inhibit formation of the primitive streak on the anterior side of the embryo (Arnold and Robertson, 2009).”
BackgroundZfp281 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
Hsa-miR-335 regulates cardiac mesoderm and progenitor cell differentiation
Kay, M., Soltani, B. M., Aghdaei, F. H., Ansari, H., & Baharvand, H. (2019) · Stem Cell Research & Therapy · doi:10.1186/s13287-019-1249-2 · Cited by 45
Robust integration of multiple single-cell RNA sequencing datasets using a single reference space
Liu, Y., Wang, T., Zhou, B., & Zheng, D. (2021) · Nature Biotechnology · doi:10.1038/s41587-021-00859-x · Cited by 41
A new era of stem cell and developmental biology: from blastoids to synthetic embryos and beyond
Kim, Y., Kim, I. S., & Shin, K. (2023) · Experimental & Molecular Medicine · doi:10.1038/s12276-023-01097-8 · Cited by 44
“These transcription factors govern lineage speci fi cation and cell differentiation, with GATA6 promoting the formation of the PrE lineage and CDX2 playing a crucial role in inducing the proper differentiation of the TE lineage 43,50,51 .”
BackgroundThe march of pluripotent stem cells in cardiovascular regenerative medicine
Abou-Saleh, H., Zouein, F. A., EL‐Yazbi, A. F., Sanoudou, D., Raynaud, C. M., Rao, C., Pintus, G., Dehaini, H., & Eid, A. H. (2018) · Stem Cell Research & Therapy · doi:10.1186/s13287-018-0947-5 · Cited by 44
Heart organoids and tissue models for modeling development and disease
Miyamoto, M., Nam, L. L., Kannan, S., & Kwon, C. (2021) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2021.03.011 · Cited by 45
“After mesoderm is formed during gastrulation [35] (Fig.”
Quantitative developmental biology in vitro using micropatterning
Blin, G. (2021) · Development · doi:10.1242/dev.186387 · Cited by 42
Biomaterials for intestinal organoid technology and personalized disease modeling
Hirota, A., AlMusawi, S., Nateri, A. S., Ordóñez‐Morán, P., & Imajo, M. (2021) · Acta Biomaterialia · doi:10.1016/j.actbio.2021.05.010 · Cited by 41
Stem cell-derived kidney cells and organoids: Recent breakthroughs and emerging applications
Chuah, J. K. C., & Zink, D. (2016) · Biotechnology Advances · doi:10.1016/j.biotechadv.2016.12.001 · Cited by 41
Mulas, C., Chia, G., Jones, K., Hodgson, A. C., Stirparo, G. G., & Nichols, J. (2018) · Development · doi:10.1242/dev.159103 · Cited by 41
Studying evolution of the primary body axis in vivo and in vitro
Anlaş, K., & Trivedi, V. (2021) · eLife · doi:10.7554/elife.69066 · Cited by 41
Cadherins in early neural development
Punovuori, K., Malaguti, M., & Lowell, S. (2021) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-021-03815-9 · Cited by 39
“This might explain why downregulation of E-cadherin does not result in neural differentiation in the posterior of the embryo, where several BMP family members (together with other anti-neural signals) are expressed at high levels [54].”
BackgroundYang, 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 41
Camacho-Aguilar, E., Yoon, S., Ortiz-Salazar, M. A., Du, S., Guerra, M. C., & Warmflash, A. (2024) · Cell Systems · doi:10.1016/j.cels.2024.04.001 · Cited by 53
Pou5f1/oct4 in pluripotency control: Insights from zebrafish
Onichtchouk, D. (2011) · genesis · doi:10.1002/dvg.20800 · Cited by 40
“…patterning and axis specification at pregastrulation stages show significant level of conservation of key regulatory processes between mammals and lower vertebrates (Arnold and Robertson, 2009; Beddington and Robertson, 1998, 1999) and can be directly compared between zebrafish, Xenopus, and mice.”
BackgroundMicrofluidic-based patterning of embryonic stem cells for in vitro development studies
Suri, S., Singh, A. K., Anh, N. T. V., Bratt‐Leal, A. M., McDevitt, T. C., & Lu, H. (2013) · Lab on a Chip · doi:10.1039/c3lc50663k · Cited by 40
Li, J., Zhu, L., Qu, X., Li, J., Lin, R., Liao, L., Wang, J., Wang, S., Xu, Q., & Zhao, R. C. (2012) · Stem Cells and Development · doi:10.1089/scd.2012.0148 · Cited by 39
“The sequential gene expression dynamics recapitulated those in gastrulation, mesendoderm [5,9], and DE development [28,29].”
Burtscher, I., Barkey, W., Schwarzfischer, M., et al. (2011) · genesis · doi:10.1002/dvg.20829 · Cited by 40
“The anterior VE (AVE) has long been known to play essential roles in anterior–posterior (AP) patterning of the developing mouse embryo (Arnold and Robertson, 2009; Srinivas, 2006).”
Muñoz‐Descalzo, S., Hadjantonakis, A., & Arias, A. M. (2015) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2015.08.011 · Cited by 42
“The mammalian embryo is patterned without maternal inputs [10,13,14] and, after the segregation of extraembryonic lineages and implantation, the remaining cells form the epiblast, a columnar epithelium of about 200 cells, will expand and become patterned into the different organs and tissues [10,15].”
Haillot, E., Molina, M. D., Lapraz, F., & Lepage, T. (2015) · PLoS Biology · doi:10.1371/journal.pbio.1002247 · Cited by 39
“While maternal information is clearly important for specification of the D/V axis in a number of species, in contrast, there is very little evidence for the presence of maternal determinants of axis formation in the oocyte of mammals, consistent with the idea that the embryonic axes are specified entirely by cell inte…”
BackgroundMouse ICM Organoids Reveal Three-Dimensional Cell Fate Clustering
Mathew, B., Descalzo, S. M., Corujo-Simón, E., et al. (2018) · Biophysical Journal · doi:10.1016/j.bpj.2018.11.011 · Cited by 40
“Although no definitive definition of this type of pattern exists, it is usually thought to indicate a random intermingling of Epi and PrE cells in the ICM (12,31).”
BackgroundPrediction and control of symmetry breaking in embryoid bodies by environment and signal integration
Sagy, N., Slovin, S., Allalouf, M., Pour, M., Savyon, G., Boxman, J., & Nachman, I. (2019) · Development · doi:10.1242/dev.181917 · Cited by 40
“The primitive streak is formed through interaction between BMP, Nodal, FGF and Wnt pathways at the posterior side of the blastocyst and is limited to that side by inhibitory signals originating from the AVE at the anterior side (Arnold and Robertson, 2009; Robertson, 2005).”
BackgroundSnapShot: Mouse Primitive Streak
Ramkumar, N., & Anderson, K. V. (2011) · Cell · doi:10.1016/j.cell.2011.07.028 · Cited by 40
Eomes restricts Brachyury functions at the onset of mouse gastrulation
Schüle, K. M., Weckerle, J., Probst, S., et al. (2023) · Developmental Cell · doi:10.1016/j.devcel.2023.07.023 · Cited by 39
Self-citationDavidson, A. J., Lewis, P. M., Przepiorski, A. J., et al. (2018) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2018.08.016 · Cited by 39
Self-organization of human dorsal-ventral forebrain structures by light induced SHH
Santis, R. D., Etoc, F., Rosado-Olivieri, E. A., & Brivanlou, A. H. (2021) · Nature Communications · doi:10.1038/s41467-021-26881-w · Cited by 38
“Downstream of these primary neural inducing signals, highly localized and dynamic organizing centers provide multiple morphogen sources that pattern the central nervous system (Arnold and Robertson, 2009; Borello and Pierani, 2010; Kiecker and Lumsden, 2012).”
BackgroundLi, F.-M., He, Z., Li, Y.-F., Liu, P.-Y., Chen, F., Wang, M.-J., Zhu, H.-Y., Ding, X.-Y., Wangensteen, K., Hu, Y.-P., et al. (2011) · Journal of Cellular Biochemistry · doi:10.1002/jcb.22962 · Cited by 37
Alev, C., Wu, Y., Nakaya, Y., & Sheng, G. (2013) · Development · doi:10.1242/dev.094318 · Cited by 39
“Furthermore, mammals and birds have been hypothesized to employ different cellular mechanisms to generate a streak (Arnold and Robertson, 2009; Chuai and Weijer, 2008; Stern, 2004; Voiculescu et al., 2007; Williams et al., 2012).”
BackgroundHuang, X., Balmer, S., Yang, F., Fidalgo, M., Li, D., Guallar, D., Hadjantonakis, A., & Wang, J. (2017) · eLife · doi:10.7554/elife.33333 · Cited by 38
The principles of teratology: Are they still true?
Friedman, J. M. (2010) · Birth Defects Research Part A Clinical and Molecular Teratology · doi:10.1002/bdra.20697 · Cited by 38
Vianello, S., & Lütolf, M. P. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.06.07.138883 · Cited by 38
“…epiblast cells respond by engaging so-called Epithelial to Mesenchymal Transition (EMT) programmes: they start losing attachment with the rest of the epithelium, they become motile and mesenchymal, they leave the epiblast (Arnold & Robertson, 2009; Tam & Behringer, 1997; Tam & Loebel, 2007).”
BackgroundNucleotide exchange factor RIC‐8 is indispensable in mammalian early development
Tõnissoo, T., Lulla, S., Meier, R., et al. (2010) · Developmental Dynamics · doi:10.1002/dvdy.22480 · Cited by 37
“Upon EMT, cells lose their characteristic apical-basal cell polarity, and undergo rapid and profound cytoskeletal rearrangements that enable them to delaminate and migrate (Arnold and Robertson, 2009).”
BackgroundSuzuki, K., Adachi, Y., Numata, T., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0043453 · Cited by 37
“Bone Morphogenetic Protein (BMP) signaling regulates a range of cellular processes and plays essential roles regulating the morphogenesis of many organs [15–19].”
BackgroundConvergence of cMyc and β‐catenin on Tcf7l1 enables endoderm specification
Morrison, G. M., Scognamiglio, R., Trumpp, A., & Smith, A. G. (2015) · The EMBO Journal · doi:10.15252/embj.201592116 · Cited by 36
Harrison, S., Sözen, B., & Zernicka‐Goetz, M. (2018) · Nature Protocols · doi:10.1038/s41596-018-0005-x · Cited by 37
Guts and gastrulation: Emergence and convergence of endoderm in the mouse embryo
Nowotschin, S., & Hadjantonakis, A. (2019) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2019.11.012 · Cited by 37
Hedgehog–FGF signaling axis patterns anterior mesoderm during gastrulation
Guzzetta, A., Koska, M., Rowton, M., Sullivan, K. R., Jacobs-Li, J., Kweon, J., Hidalgo, H. A., Eckart, H., Hoffmann, A. D., Back, R., et al. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1914167117 · Cited by 37
Plasticity underlies tumor progression: role of Nodal signaling
Bodenstine, T. M., Chandler, G. S., Seftor, R. E. B., et al. (2016) · Cancer and Metastasis Reviews · doi:10.1007/s10555-016-9605-5 · Cited by 37
“Nodal also induces Smad2 signaling in the underlying visceral endoderm (VE) to pattern a specialized region known as the distal visceral endoderm (DVE) [15, 57].”
InfluentialTime-aligned hourglass gastrulation models in rabbit and mouse
Mayshar, Y., Raz, O., Cheng, S., Ben-Yair, R., Hadas, R., Reines, N., Mittnenzweig, M., Ben-Kiki, O., Lifshitz, A., Tanay, A., et al. (2023) · Cell · doi:10.1016/j.cell.2023.04.037 · Cited by 34
Establishing Three Blastocyst Lineages--Then What?
Gasperowicz, M., & Natale, D. R. C. (2010) · Biology of Reproduction · doi:10.1095/biolreprod.110.085209 · Cited by 39
“As stated previously, VE is important for mediating signals controlling differentiation and patterning of the EPI [5, 81], and interestingly, VE has also recently been shown to contribute a small number of cells to the developing gut, a finding that suggests that segregation of extraembryonic and embryonic lineages wi…”
BackgroundYamamizu, K., Fujihara, M., Tachibana, M., Katayama, S., Takahashi, A., Hara, E., Imai, H., Shinkai, Y., & Yamashita, J. K. (2012) · Cell stem cell · doi:10.1016/j.stem.2012.02.022 · Cited by 36
“Mouse ESCs are able to maintain pluripotency in the presence of LIF by the transcriptional regulatory circuit with genes such as Oct3/4, Nanog, and Sox2 (Nishiyama et al., 2009; Takahashi and Yamanaka, 2006; Walker et al., 2009; Arnold and Robertson, 2009; Ng and Surani, 2011).”
BackgroundRetractedEx Uno Plures: Molecular Designs for Embryonic Pluripotency
Loh, K. M., Lim, B., & Ang, L. T. (2014) · Physiological Reviews · doi:10.1152/physrev.00001.2014 · Cited by 35
“This is the developmental process through which the three fetal germ layers (definitive endoderm, mesoderm, and definitive ectoderm) are born (14, 334) (FIGURE 1A).”
BackgroundThe Evx1/Evx1as gene locus regulates anterior-posterior patterning during gastrulation
Bell, C. C., Amaral, P., Kalsbeek, A. M. F., Magor, G. W., Gillinder, K. R., Tangermann, P., Lisio, L. D., Cheetham, S. W., Gruhl, F., Frith, J. E., et al. (2016) · Scientific Reports · doi:10.1038/srep26657 · Cited by 36
A high-content small molecule screen identifies novel inducers of definitive endoderm
Korostylev, A., Mahaddalkar, P. U., Keminer, O., Hadian, K., Schorpp, K., Gribbon, P. M., & Lickert, H. (2017) · Molecular Metabolism · doi:10.1016/j.molmet.2017.04.009 · Cited by 36
“Furthermore, Wnt3a and Nodal/TGF-b signaling are known to pattern the endoderm in a dosedependent fashion [10].”
BackgroundColombier, P., Halgand, B., Chédeville, C., et al. (2020) · Cells · doi:10.3390/cells9020509 · Cited by 36
“In contrast, when hiPSCs were treated with 6 µM HIR, cells cquired a Posterior PS-like (PPS-like) identity revealed by elevated level of T and MIXL1 tr nscripts and conversely lower levels of NODAL, EOMES, FOXA2 and CER1 [41].”
MethodInfluentialRNA polymerase II pausing in development: orchestrating transcription
Abuhashem, A., Garg, V., & Hadjantonakis, A. (2022) · Open Biology · doi:10.1098/rsob.210220 · Cited by 38
Stem-cell-based human and mouse embryo models
Bao, M., Cornwall-Scoones, J., & Zernicka‐Goetz, M. (2022) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2022.101970 · Cited by 36
PI3K/Akt1 signalling specifies foregut precursors by generating regionalized extra-cellular matrix
Villegas, S. N., Rothová, M., Barrios-Llerena, M. E., Pulina, M. V., Hadjantonakis, A., Bihan, T. L., Astrof, S., & Brickman, J. M. (2013) · eLife · doi:10.7554/elife.00806 · Cited by 36
Single-cell analysis reveals lineage segregation in early post-implantation mouse embryos
Wen, J., Zeng, Y., Fang, Z., Gu, J., Ge, L., Tang, F., Qu, Z., Hu, J., Cui, Y., Zhang, K., et al. (2017) · Journal of Biological Chemistry · doi:10.1074/jbc.m117.780585 · Cited by 37
“Pre-MEN cells had higher levels of Nodal, Wnt3, and Fgf8 ligands, which are all signaling molecules required for the generation of the MEN (6).”
BackgroundInfluentialSelf-Organization of Spatial Patterning in Human Embryonic Stem Cells
Deglincerti, A., Etoc, F., Ozair, M. Z., & Brivanlou, A. H. (2016) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2015.11.010 · Cited by 37
“Integration of signaling activities and cell movement ultimately leads to gastrulation [6].”
BackgroundYAP1 regulates the self-organized fate patterning of hESC-derived gastruloids
Stronati, E., Giráldez, S., Huang, L., et al. (2022) · Stem Cell Reports · doi:10.1016/j.stemcr.2021.12.012 · Cited by 35
Sirtuin 1 Promotes Deacetylation of Oct4 and Maintenance of Naive Pluripotency
Williams, E. O., Taylor, A. K., Bell, E. L., Lim, R., Kim, D. M., & Guarente, L. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.09.046 · Cited by 35
“During embryo implantation, cells of the epiblast layer transition from the naive state to the primed pluripotency state (Arnold and Robertson, 2009; Brons et al., 2007; Kojima et al., 2014; Tesar et al., 2007).”
Malaguti, M., Migueles, R. P., Annoh, J., Sadurska, D., Blin, G., & Lowell, S. (2022) · Development · doi:10.1242/dev.200226 · Cited by 33
A small set of extra-embryonic genes defines a new landmark for bovine embryo staging
Degrelle, S. A., Cao, K. L., Heyman, Y., et al. (2010) · Reproduction · doi:10.1530/rep-10-0174 · Cited by 34
“…top list of discriminative genes (nZ50 per list) was loaded with the mouse patterning genes (nZ55 (Pfister et al. 2007, Tam & Loebel 2007, Arnold & Robertson 2009)) into the IPA software (version 6.5) and converted into gene networks, based on the human, mouse and rat database created by…”
BackgroundMethodInfluentialLessons for inductive germline determination
Seervai, R. N. H., & Wessel, G. M. (2013) · Molecular Reproduction and Development · doi:10.1002/mrd.22151 · Cited by 34
Heemskerk, I., & Warmflash, A. (2016) · Developmental Dynamics · doi:10.1002/dvdy.24432 · Cited by 33
“This process is mainly orchestrated by the BMP and Activin/Nodal branches of the TGFb pathway, through interplay with Wnt and FGF (Arnold and Robertson, 2009).”
BackgroundInfluentialLi, Y., Wang, R., Qiao, N., Peng, G., Zhang, K., Tang, K., Han, J. J., & Jing, N. (2017) · Journal of Biological Chemistry · doi:10.1074/jbc.m117.796383 · Cited by 37
Harland, L. T. G., Simon, C. S., Senft, A. D., Costello, I., Greder, L. V., Imaz-Rosshandler, I., Göttgens, B., Marioni, J. C., Bikoff, E. K., Porcher, C., et al. (2021) · Nature Cell Biology · doi:10.1038/s41556-020-00611-8 · Cited by 30
Self-citation
Metadata
- Authors
- Arnold, S. J., & Robertson, E. J.
- Affiliations
- University of Oxford (GB)
- Corresponding author
- Robertson, Elizabeth J.
- Venue
- Nature Reviews Molecular Cell Biology
- Published
- 2009-01-08
- Volume
- 10
- Issue
- 2
- Pages
- 91-103
- ISSN
- 1471-0072 (ISSN-L)
- 1471-0080
- OpenAlex
- W2070700342
- Cited by
- 816
- References
- 147
- Citations by year
- 2026: 39 · 2025: 52 · 2024: 46 · 2023: 45 · 2022: 55 · 2021: 66 · 2020: 49 · 2019: 56 · 2018: 60 · 2017: 48 · 2016: 46 · 2015: 35 · 2014: 56 · 2013: 41 · 2012: 39
- FWCI
- 3.14
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Nature Reviews Molecular Cell Biology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Wellcome Trust (059312)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Pluripotent Stem Cells Research
- Health Sciences › Medicine › Reproductive Medicine › Reproductive Biology and Fertility
- Keywords
- early mouse embryo, anterior-posterior polarity, gastrulation, germ layer specification, germ cell specification, signaling pathways, transcription factors, blastocyst, in vivo imaging, developmental conservation, lower vertebrates
- MeSH terms
- Positive Regulatory Domain I-Binding Factor 1, Animals, DNA-Binding Proteins, Embryo, Mammalian, Morphogenesis, Transcription Factors, Signal Transduction, RNA-Binding Proteins, Cell Lineage, Bone Morphogenetic Proteins, Body Patterning, Mice, Smad Proteins, Gastrulation
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
