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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.
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“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]
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“INTRODUCTION In the last two decades the molecular analysis of axis induction and embryonic patterning has provided a blueprint for body axis formation and organizer function in several species, including amphibians, chicken, zebrafish and mouse (Arnold and Robertson, 2009; De Robertis et al., 2000; Niehrs, 2004; Nowo…”
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“Notably, Wnt3 was shown to activate Nodal expression directly through its proximal epiblast enhancer at the gastrulation stage (58, 59).”
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“This results in the posterior localization of the primitive streak, the morphological site where epiblast cells lose pluripotency and undergo an EMT as they acquire mesoderm and endoderm identities, heralding the start of gastrulation (Arnold and Robertson, 2009; Beddington and Robertson, 1999; Lewis and Tam, 2006; Ri…”
BackgroundInsulin fine-tunes self-renewal pathways governing naive pluripotency and extra-embryonic endoderm
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“3) that represents an important mediator of a feed-forward loop between the EXE and epiblast feeding on Nodal expression and mesoderm induction (Arnold and Robertson, 2009).”
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NODAL Secures Pluripotency upon Embryonic Stem Cell Progression from the Ground State
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“Since cross-talk between Nodal, BMP, and Wnt signaling pathways is essential for maintaining normal expression of these genes (Arnold and Robertson, 2009), the expanded expression of the major growth factors in Pofut2 mutants suggested that failure to O-fucosylate TSR-containing proteins disrupted…”
InfluentialGastruloids generated without exogenous Wnt activation develop anterior neural tissues
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“This is in marked contrast to the mouse embryo, where the WNT signaling pathway is initially activated in a highly localizedmanner at the primitive streak on the posterior domain and is strictly regulated by the secretion of WNT antagonists from the anterior visceral endoderm (Arnold and Robertson, 2009).”
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“…LIF; extraembryonic endoderm; XEN cell; visceral endoderm; hematopoiesis; live imaging INTRODUCTION The patterning of the early mouse embryo relies on reciprocal signalling interactions between embryonic and extraembryonic tissues (reviewed in (Arnold and Robertson, 2009; Rossant and Tam, 2009)).”
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“The specification of the primitive streak on the posterior side of the mouse embryo, and the positioning of the anterior visceral endoderm (AVE) on the prospective anterior side, are the two major events that establish the anterior-posterior axis of the embryo (Arnold and Robertson, 2009; Beddington and Robertson, 199…”
The T-box transcription factor Eomesodermin is essential for AVE induction in the mouse embryoPreprint
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“Subsequently, 40 these progenitors generate all major organ systems in a process known as organogenesis (Arnold and Robertson, 2009; Bardot and Hadjantonakis, 2020; Tam and Loebel, 2007).”
BackgroundGeneration and analysis of a mouse line harboring GFP in the Eomes/Tbr2 locus
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BackgroundSelf-citationTgif1 and Tgif2 regulate Nodal signaling and are required for gastrulation
Powers, S. E., Taniguchi, K., Yen, W., Melhuish, T. A., Shen, J., Walsh, C. A., Sutherland, A. E., & Wotton, D. (2009) · Development · doi:10.1242/dev.040782 · Cited by 69
“In the primitive streak, the epiblast cells undergo an epithelial-tomesenchymal transition (EMT) to form mesoderm and definitive endoderm, thereby establishing the three primary germ layers (Arnold and Robertson, 2009; Tam and Loebel, 2007).”
BackgroundZhu, D., Hölz, S., Metzger, E., Pavlovic, M., Jandausch, A., Jilg, C. A., Galgóczy, P., Herz, C., Moser, M., METZGER, D., et al. (2014) · Nature Communications · doi:10.1038/ncomms4174 · Cited by 67
Self-citationvan Leeuwen, J., Berg, D. K., & Pfeffer, P. (2015) · PLoS ONE · doi:10.1371/journal.pone.0129787 · Cited by 66
Activin A and Wnt-dependent specification of human definitive endoderm cells.
Toivonen, S., Lundin, K., Balboa, D., Ustinov, J., Tamminen, K., Palgi, J., Trokovic, R., Tuuri, T., & Otonkoski, T. (2013) · Experimental Cell Research · doi:10.1016/j.yexcr.2013.07.007 · Cited by 67
Blin, G., Wisniewski, D., Picart, C., Théry, M., Pucéat, M., & Lowell, S. (2018) · Development · doi:10.1242/dev.166025 · Cited by 66
Asai-Coakwell, M., March, L. D., Dai, X. H., DuVal, M. G., López, I., French, C. R., Famulski, J. K., Baere, E. B. W. D., Francis, P. J., Sundaresan, P., et al. (2013) · Human Molecular Genetics · doi:10.1093/hmg/dds560 · Cited by 68
Malaguti, M., Nistor, P., Blin, G., Pegg, A., Zhou, X., & Lowell, S. (2013) · eLife · doi:10.7554/elife.01197 · Cited by 64
Massey, J., Liu, Y., Alvarenga, O. E., Saez, T., Schmerer, M. W., & Warmflash, A. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1815363116 · Cited by 67
“During gastrulation, dramatic morphogenetic rearrangements occur simultaneously with patterning of the primitive streak (PS) by BMP, WNT, and NODAL signals (12).”
BackgroundMethodMapping cell migrations and fates in a gastruloid model to the human primitive streak
Martyn, I., Siggia, E. D., & Brivanlou, A. H. (2019) · Development · doi:10.1242/dev.179564 · Cited by 64
A Sprouty4 reporter to monitor FGF/ERK signaling activity in ESCs and mice
Morgani, S. M., Saiz, N., Garg, V., Raina, D., Simon, C. S., Kang, M., Arias, A. M., Nichols, J., Schröter, C., & Hadjantonakis, A.-K. (2018) · Developmental Biology · doi:10.1016/j.ydbio.2018.06.017 · Cited by 55
“subsequently migrate bilaterally around the embryo between the Epi and VE cell layers [68].”
BackgroundSpatiotemporal sequence of mesoderm and endoderm lineage segregation during mouse gastrulation
Probst, S., Sagar, Tošić, J., Schwan, C., Grün, D., & Arnold, S. J. (2020) · Development · doi:10.1242/dev.193789 · Cited by 65
Self-citationNeuromesodermal Progenitors: A Basis for Robust Axial Patterning in Development and Evolution
Sambasivan, R., & Steventon, B. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.607516 · Cited by 63
“In mice, Wnt3A signaling cascade directly activates T (Yamaguchi et al., 1999; Arnold and Robertson, 2009; Ramkumar and Anderson, 2011) and this regulatory relationship appears conserved between amniotes and anamniotes (Vonica and Gumbiner, 2002; Martin and Kimelman, 2008, 2009).”
BackgroundComparison of Tendon Development Versus Tendon Healing and Regeneration
He, P., Ruan, D., Huang, Z., Wang, C., Xu, Y., Cai, H., Liu, H., Fei, Y., Heng, B. C., Chen, W., et al. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.821667 · Cited by 66
Paracrine effects of embryo-derived FGF4 and BMP4 during pig trophoblast elongation
Magaña, G. V., Rodríguez, A., Zhang, H., WEBB, R., & Alberio, R. (2014) · Developmental Biology · doi:10.1016/j.ydbio.2014.01.008 · Cited by 63
Scoliosis and segmentation defects of the vertebrae
Eckalbar, W. L., Fisher, R. E., Rawls, A., & Kusumi, K. (2012) · Wiley Interdisciplinary Reviews Developmental Biology · doi:10.1002/wdev.34 · Cited by 60
Coda, D. M., Gaarenstroom, T., East, P., Patel, H., Miller, D. S. J., Lobley, A., Matthews, N., Stewart, A., & Hill, C. S. (2017) · eLife · doi:10.7554/elife.22474 · Cited by 63
“*For correspondence: caroline. hill@crick.ac.uk †These authors contributed equally to this work”
Regulation of extra-embryonic endoderm stem cell differentiation by Nodal and Cripto signaling
Julio, M. K.-D., Alvarez, M. J., Galli, A., Chu, J., Price, S. M., Califano, A., & Shen, M. M. (2011) · Development · doi:10.1242/dev.065656 · Cited by 62
“In particular, a central role in anterior-posterior (A-P) axis specification is played by the anterior visceral endoderm (AVE), a specialized population of cells within the visceral endoderm that overlies and patterns the adjacent epiblast at pregastrulation and early gastrulation stages (Arnold and Robertson, 2009; R…”
BackgroundExtracellular interactions and ligand degradation shape the nodal morphogen gradient
Wang, Y., Wang, X., Wohland, T., & Sampath, K. (2016) · eLife · doi:10.7554/elife.13879 · Cited by 61
“Nodal proteins, which belong to the TGF-b family of signaling proteins, play critical roles in vertebrate development (Arnold and Robertson, 2009; Wakefield and Hill, 2013).”
Backgroundβ-Pix directs collective migration of anterior visceral endoderm cells in the early mouse embryoPreprint
Omelchenko, T., Rabadán, M. A., Hernández-Martínez, R., Grego‐Bessa, J., Anderson, K. V., & Hall, A. (2014) · Genes & Development · doi:10.1101/gad.251371.114 · Cited by 62
Madabhushi, M. E., & Lacy, E. (2011) · Developmental Cell · doi:10.1016/j.devcel.2011.08.027 · Cited by 60
“5 conceptus (Arnold and Robertson, 2009; Rivera-Perez et al., 2003), executes the key organizer activities of the VE prior to gastrulation.”
BackgroundA close look at the mammalian blastocyst: epiblast and primitive endoderm formation
Artus, J., & Chazaud, C. (2014) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-014-1630-3 · Cited by 60
Teo, A., Valdez, I., Dirice, E., & Kulkarni, R. (2014) · Stem Cell Reports · doi:10.1016/j.stemcr.2014.05.007 · Cited by 58
“…the complexNodal,Wnt (Wnt3,Wnt3a andWnt5a) and Bmp (Bmp4) signaling, which operate during gastrulation, primitive streak, andearlyDE formation in themouse embryo (Arnold and Robertson, 2009; Lawson et al., 1999; Liu et al., 1999; Ohinata et al., 2009; Teo et al., 2011; Yamaguchi et al., 1999).”
BackgroundInfluentialNano-scale control of cellular environment to drive embryonic stem cells selfrenewal and fate
Blin, G., Lablack, N., Louis-Tisserand, M., et al. (2009) · Biomaterials · doi:10.1016/j.biomaterials.2009.11.055 · Cited by 60
“Adhesion of ESCs on cross-linked nanofilms could trigger secretion of factors such as Wnts and/or FGFs which can direct the fate of ESCs toward the primitive streak and early mesendoderm [28–30].”
Sequential formation and resolution of multiple rosettes drive embryo remodelling after implantation
Christodoulou, N., Kyprianou, C., Weberling, A., Wang, R., Cui, G., Peng, G., Jing, N., & Zernicka‐Goetz, M. (2018) · Nature Cell Biology · doi:10.1038/s41556-018-0211-3 · Cited by 60
van den Ameele, J., Tiberi, L., Bondue, A., Paulissen, C., Herpoel, A., Iacovino, M., Kyba, M., Blanpain, C., & Vanderhaeghen, P. (2012) · EMBO Reports · doi:10.1038/embor.2012.23 · Cited by 61
“Interplay between extrinsic and intrinsic cues regulates the different cell fates and patterning of the early embryo [1,2].”
Symmetry Breaking in the Mammalian Embryo
Zhang, H. T., & Hiiragi, T. (2018) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-100617-062616 · Cited by 61
A Comparative Analysis of Extra-Embryonic Endoderm Cell Lines
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“This hypothesis has come largely from the observation of an anterior migration of the AVE just prior to the onset of gastrulation [54] and studies in avian embryos showing”
BackgroundTrichas, G., Joyce, B. W., Crompton, L., Wilkins, V., Clements, M., Tada, M., Rodríguez, T. A., & Srinivas, S. (2011) · PLoS Biology · doi:10.1371/journal.pbio.1001019 · Cited by 58
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“…the mesoderm and endoderm cells are emerging from the primitive streak of the posterior epiblast and gradually form distinct cell types that consist of the progenitors for the respective derivatives (Fossat et al., 2007; Tam and Loebel, 2007; Arnold and Robertson, 2009; Peng and Jing, 2017).”
BackgroundThe Roles of Embryonic Transcription Factor BRACHYURY in Tumorigenesis and Progression
Chen, M., Wu, Y., Zhang, H., et al. (2020) · Frontiers in Oncology · doi:10.3389/fonc.2020.00961 · Cited by 57
Axial differentiation and early gastrulation stages of the pig embryo
Hassoun, R., Schwartz, P. J., Feistel, K., et al. (2009) · Differentiation · doi:10.1016/j.diff.2009.07.006 · Cited by 57
Rac1 mediates morphogenetic responses to intercellular signals in the gastrulating mouse embryo
Migeotte, I., Grego‐Bessa, J., & Anderson, K. V. (2011) · Development · doi:10.1242/dev.059766 · Cited by 59
“Gastrulation signaling pathways are activated normally in Rac1 Depi embryos Gastrulation of the mouse embryo, which is the process that generates the mesoderm and endoderm germ layers from the epiblast epithelium, depends on the integrated activity of the Wnt, TGFb and Fgf signaling pathways (Arnold and Robertson, 200…”
BackgroundInfluentialSteventon, B., Busby, L. C., & Arias, A. M. (2021) · Developmental Cell · doi:10.1016/j.devcel.2021.08.012 · Cited by 56
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
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