Cellular dynamics in the early mouse embryo: from axis formation to gastrulation
Open accessAbstract
Coordinated cell movements and reciprocal tissue interactions direct the formation of the definitive germ layers and the elaboration of the major axes of the mouse embryo. Genetic and embryological studies have defined the major molecular pathways that mediate these morphogenetic processes and provided 'snapshots' of the morphogenetic program. However, it is increasingly clear that this foundation needs to be validated, and can be significantly refined and extended using live imaging approaches. In situ visualization of these processes in living specimens is a major goal, as it provides unprecedented detail of the individual cellular behaviors, which translate into the large-scale tissue rearrangements that shape the embryo.
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Definitive (embryonic) endoderm (DE) is specified from pluripotent epiblast (EPI) at gastrulation around E7.0.
“Later, around E7.0, definitive (embryonic) endoderm (DE) is specified from pluripotent epiblast (EPI) at gastrulation4.”
From The emergent landscape of the mouse gut endoderm at single-cell resolution (2019) · cites this paper as [4]
The ‘Emergence of the primitive streak’ section says that during gastrulation the epiblast generates definitive endoderm, and ‘Intercalation and endoderm morphogenesis’ says DE cells may be specified within the streak. The paper places streak formation at E6.5 and its elongation through E7.5, but does not specifically place DE specification around E7.0. (LLM, conf=0.82)
Experimental — accuracy not yet measuredThe early post-implantation (E5.5) mouse embryo is radially symmetrical, and the VE appears morphologically uniform around its proximal-distal axis.
“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 [4]
The section “PD polarity at early postimplantation results in DVE cell specification” describes the E5.5 egg cylinder as radially symmetric. It does not establish that the VE appears morphologically uniform around the proximal-distal axis; instead, it describes distinct proximal and distal VE morphologies and morphologically distinct DVE cells around E5.5. The source therefore supports the embryo-symmetry part but not the unqualified VE-uniformity part. (LLM, conf=0.84)
Experimental — accuracy not yet measured
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“KEY WORDS: Mouse, Gastrulation, Self-organisation, Symmetry breaking, Polarisation, Axial elongation, Endoderm, Mesoderm, Neural ectoderm, Pattern formation, Live cell imaging”
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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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“This process is tightly coordinated in time and space and begins with the formation of a transient structure, the primitive streak, at the posterior end of the embryo [6, 7].”
BackgroundMalaguti, M., Migueles, R. P., Annoh, J., Sadurska, D., Blin, G., & Lowell, S. (2022) · Development · doi:10.1242/dev.200226 · Cited by 32 · see citing works
Light-sheet imaging of mammalian development
de Medeiros, G., Balázs, B., & Hufnagel, L. (2016) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2015.11.001 · Cited by 33 · see citing works
Gutsy moves in mice: cellular and molecular dynamics of endoderm morphogenesis
Viotti, M., Foley, A. C., & Hadjantonakis, A. (2014) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2013.0547 · Cited by 30 · see citing works
“5), the VE epithelium comprises several subpopulations, generally encompassing: the extraembryonic VE (exVE), a cuboidal epithelium overlying the ExE, and the embryonic VE (emVE), a squamous epithelium overlying the epiblast [4–9].”
BackgroundSelf-citationTakaoka, K., Nishimura, H., & Hamada, H. (2017) · Nature Communications · doi:10.1038/s41467-017-01625-x · Cited by 30 · see citing works
Matrix metalloproteinase function in non-mammalian model organisms
Jessen, J. R. (2011) · Frontiers in Bioscience-Scholar · doi:10.2741/431 · Cited by 24 · see citing works
<i>Afp::mCherry</i>, a red fluorescent transgenic reporter of the mouse visceral endoderm
Viotti, M., Nowotschin, S., & Hadjantonakis, A. (2011) · genesis · doi:10.1002/dvg.20695 · Cited by 29 · see citing works
Self-citationGiving the right tug for migration: Cadherins in tissue movements
Becker, S. F. S., Langhe, R., Huang, C., Wedlich, D., & Kashef, J. (2012) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2012.02.013 · Cited by 23 · see citing works
The Smurf ubiquitin ligases regulate tissue separation via antagonistic interactions with ephrinB1Preprint
Hwang, Y., Lee, H., Kamata, T., Mood, K., Cho, H. J., Winterbottom, E. F., Ji, Y. J., Singh, A., & Daar, I. O. (2013) · Genes & Development · doi:10.1101/gad.208355.112 · Cited by 23 · see citing works
“The creation of the embryonic body and its organization into separate tissues requires the coordinated behavior of cells through adhesive and repulsive mechanisms, which promote and maintain the segregation of different cell populations at tissue boundaries (Nowotschin and Hadjantonakis 2010).”
BackgroundSingle-cell analysis of mouse uterus at the invasion phase of embryo implantation
He, J., Tian, Q., Zhu, Q., & Liu, J. (2022) · Cell & Bioscience · doi:10.1186/s13578-022-00749-y · Cited by 22 · see citing works
“TGC cells are in closest contact to the uterus during embryo implantation [50].”
BackgroundPolydorou, C., & Georgiades, P. (2013) · Nature Communications · doi:10.1038/ncomms2646 · Cited by 21 · see citing works
Differentiation of PTH-Expressing Cells From Human Pluripotent Stem Cells
Lawton, B. R., Martineau, C., Sosa, J. A., Roman, S. A., Gibson, C. E., Levine, M. A., & Krause, D. S. (2020) · Endocrinology · doi:10.1210/endocr/bqaa141 · Cited by 21 · see citing works
Early autonomous patterning of the anteroposterior axis in gastruloids
Anlaş, K., Gritti, N., Nakaki, F., Palau, L. S., Tlili, S., Oriola, D., Arató, K., Lim, J. L., Sharpe, J. A., & Trivedi, V. (2024) · Development · doi:10.1242/dev.202171 · Cited by 19 · see citing works
Insight into Nephrocan Function in Mouse Endoderm Patterning
Addeo, M., Buonaiuto, S., Guerriero, I., Amendola, E., Visconte, F., Marino, A., Angelis, M. T. D., Russo, F., Roberto, L., Marotta, P., et al. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms21010008 · Cited by 20 · see citing works
“As gastrulation initiates, the pluripotent epiblast cells are recruited to a structure known as the primitive streak (PS), where they undergo an epithelial-to-mesenchymal transition (EMT) giving rise to mesoderm and definitive endoderm [4,5].”
BackgroundCell Lineage Allocation Within the Inner Cell Mass of the Mouse Blastocyst
Xenopoulos, P., Kang, M., & Hadjantonakis, A. (2012) · Results and problems in cell differentiation · doi:10.1007/978-3-642-30406-4_10 · Cited by 19 · see citing works
“10.1) (reviewed by Arnold and Robertson 2009; Nowotschin and Hadjantonakis 2010; Rossant and Tam 2009; Zernicka-Goetz et al. 2009).”
InfluentialSelf-citationUnderstanding the Molecular Circuitry of Cell Lineage Specification in the Early Mouse Embryo
Bergsmedh, A., Donohoe, M. E., Hughes, R., & Hadjantonakis, A. (2011) · Genes · doi:10.3390/genes2030420 · Cited by 18 · see citing works
“three lineages of the late blastocyst: TE, PrE and EPI will produce both the embryo-proper (EPI) as well as its ancillary extraembryonic tissues (TE and PrE), which serve as a maternal-fetal interface as well as guiding the development of a functional and viable embryo [2,16,17].”
BackgroundSelf-citationDynamics of anteroposterior axis establishment in a mammalian embryo-like systemPreprint
Anlaş, K., Gritti, N., Oriola, D., Arató, K., Nakaki, F., Lim, J. L., Sharpe, J. A., & Trivedi, V. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.02.24.432766 · Cited by 18 · see citing works
“5 at the diametrically opposite end, thereby demarcating the posterior, characterized by activity of Wnts, Nodal and Bra/T [6, 7, 8].”
BackgroundSauvegarde, C., Paul, D., Bridoux, L., Jouneau, A., Degrelle, S. A., Hue, I., Rezsöhazy, R., & Donnay, I. (2016) · PLoS ONE · doi:10.1371/journal.pone.0165898 · Cited by 16 · see citing works
Sun, C., Chen, F., Sun, K., Zhou, S. Y., Wang, J., Wang, Q., Meng, Z., Peng, J., Song, W., & Zhou, Y. (2020) · Journal of Cardiovascular Pharmacology · doi:10.1097/fjc.0000000000000803 · Cited by 15 · see citing works
Determinant molecular markers for peri-gastrulating bovine embryo development
Hue, I. (2015) · Reproduction Fertility and Development · doi:10.1071/rd15355 · Cited by 15 · see citing works
Rosenfeld, D., Tzchori, I., Fine, A., Chen‐Konak, L., & Levenberg, S. (2014) · Tissue Engineering Part A · doi:10.1089/ten.tea.2014.0008 · Cited by 14 · see citing works
Live Imaging Fluorescent Proteins in Early Mouse Embryos
Xenopoulos, P., Nowotschin, S., & Hadjantonakis, A. (2012) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/b978-0-12-391856-7.00042-1 · Cited by 13 · see citing works
“…comprises of a dynamic three-dimensional orchestration of cellular interactions, including proliferation, apoptosis, movement, and differentiation, which occur in a temporally and spatially regulated manner (Arnold and Robertson, 2009; Nowotschin and Hadjantonakis, 2010; Rossant and Tam, 2009).”
BackgroundSelf-citationCell Jamming Regulates Epithelial Chiral MorphogenesisPreprint
Rahman, T., Peters, F., & Wan, L. Q. (2022) · SSRN Electronic Journal · doi:10.2139/ssrn.4052248 · Cited by 10 · see citing works
Lu, X., Zhao, Z., Wang, X., Zhang, X., Zhai, Y., Deng, W., Yi, Z., & Li, L. (2018) · Biology Open · doi:10.1242/bio.032508 · Cited by 8 · see citing works
“Cell lineage specification during gastrulation is a highly dynamic and complex process involving drastic cell proliferation, migration and differentiation (Nowotschin and Hadjantonakis, 2010; Takaoka and Hamada, 2012; Tam and Behringer, 1997), which requires precise gene regulation.”
Formation of Germ Layers and Early Derivatives
Carlson, B. M. (2014) · Elsevier eBooks · doi:10.1016/b978-1-4557-2794-0.00005-x · Cited by 8 · see citing works
Effect of a Matrigel Sandwich on Endodermal Differentiation of Human Embryonic Stem Cells
Lawton, B. R., Sosa, J. A., Roman, S. A., & Krause, D. S. (2013) · Stem Cell Reviews and Reports · doi:10.1007/s12015-013-9447-2 · Cited by 8 · see citing works
Follow your gut: Relaying information from the site of left–right symmetry breaking in the mouse
Saijoh, Y., Viotti, M., & Hadjantonakis, A. (2014) · genesis · doi:10.1002/dvg.22783 · Cited by 7 · see citing works
“In this way, the DE would displace the VE in the area adjacent to the epiblast as gastrulation proceeded, thereby segregating embryonic (DE) and extraembryonic (VE) endoderm populations (reviewed in (Nowotschin and Hadjantonakis, 2010)).”
BackgroundSelf-citationA regulatory network controls nephrocan expression and midgut patterning
Hou, J., Wei, W., Saund, R. S., Xiang, P., Cunningham, T. J., Yi, Y., Alder, O., Lu, D. Y. D., Savory, J. G. A., Krentz, N. A. J., et al. (2014) · Development · doi:10.1242/dev.108274 · Cited by 7 · see citing works
Charting the emergent organotypic landscape of the mammalian gut endoderm at single-cell resolutionPreprint
Nowotschin, S., Setty, M. N., Kuo, Y.-Y., Lui, V. C. H., Garg, V., Sharma, R., Simon, C. S., Saiz, N., Gardner, R., Boutet, S. C., et al. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/471078 · Cited by 7 · see citing works
Self-citationA conditional mutant allele for analysis of Mixl1 function in the mouse
Pulina, M. V., Sahr, K. E., Nowotschin, S., Baron, M. H., & Hadjantonakis, A. (2014) · genesis · doi:10.1002/dvg.22768 · Cited by 6 · see citing works
“…mRNA is first detected at embryonic day (E)5.5 in cells of the posterior visceral endoderm (PVE) residing at the embryonic–extraembryonic junction (Nowotschin and Hadjantonakis, 2010, Rivera-Perez and Hadjantonakis, in press), as well as in VE cells overlying the embryonic region (the emVE)…”
BackgroundInfluentialSelf-citationWu, T., Hadjantonakis, A., & Nowotschin, S. (2017) · Biology Open · doi:10.1242/bio.024638 · Cited by 6 · see citing works
“Embryo culture and time-lapse imaging Embryos were dissected in DMEM/F12 containing 5% newborn calf serum, and then cultured in medium comprising 50% DMEM/F12 Glutamax/50% Rat Serum as previously described (Nowotschin et al., 2010).”
MethodSelf-citationGastrulation and Germ Layer Formation
Carlson, B. M. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-801238-3.05432-5 · Cited by 6 · see citing works
Wnt Signaling in Early Vertebrate Development
Żyłkiewicz, E., Sokol, S. Y., & Hoppler, S. (2014) · Wiley eBooks · doi:10.1002/9781118444122.ch19 · Cited by 5 · see citing works
Formation of Germ Layers and Early Derivatives
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Photo-dependent cytosolic delivery of shRNA into a single blastomere in a mouse embryo
Ikawa, Y., Wakai, T., Funahashi, H., Soe, T. H., Watanabe, K., & Ohtsuki, T. (2023) · Scientific Reports · doi:10.1038/s41598-023-40361-9 · Cited by 2 · see citing works
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Competence to epithelialise coincides with competence to differentiate in pluripotent cellsPreprint
Lin, C., Tatar, T., Blin, G., Malaguti, M., Migueles, R. P., Shao, H., Chen, N., Chambers, I., & Lowell, S. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/809467 · Cited by 2 · see citing works
“For example, in all amniotes pluripotent cells organise themselves into an epithelium prior to gastrulation (Nowotschin & Hadjantonakis, 2010; Bedzhov & Zernicka-Goetz, 2014; Sheng, 2015), and it has been suggested that this morphological change may be a prerequisite for subsequent lineage…”
BackgroundQuantitative analyses for elucidating mechanisms of cell fate commitment in the mouse blastocyst
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Hypoxia signaling-driven metabolic reprogramming regulates mouse formative epiblast cell developmentPreprint
Li, L., Wang, Q., He, B., Wang, X., Wu, Y., Hou, Y., Gu, C., Lu, X., Xu, C., Su, J., et al. (2025) · Research Square · doi:10.21203/rs.3.rs-7963938/v1 · Cited by 1 · see citing works
Analysis of Band 4.1B in Integrin-Mediated Cell Adhesion and Signaling
Jung, Y. (2011) · Digital Commons-TMC (Texas Medical Center)
Kispert, A., & Gossler, A. (2012) · Elsevier eBooks · doi:10.1016/b978-0-12-382008-2.00006-4
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Development of the Avian Respiratory System
Maina, J. N. (2023) · Zoological monographs · doi:10.1007/978-3-031-35180-8_2
- Authors
- Nowotschin, S., & Hadjantonakis, A.-K.
- Affiliations
- Memorial Sloan Kettering Cancer Center (US)
- Corresponding author
- Hadjantonakis, Anna-Katerina
- Venue
- Current Opinion in Genetics & Development
- Publisher
- Elsevier BV
- Published
- 2010-08
- Volume
- 20
- Issue
- 4
- Pages
- 420-427
- ISSN
- 0959-437X (ISSN-L)
- PMC
- PMC2908213
- OpenAlex
- W2093803051
- Cited by
- 79
- References
- 54
- Citations by year
- 2025: 1 · 2024: 1 · 2023: 2 · 2022: 4 · 2021: 2 · 2020: 4 · 2019: 5 · 2018: 4 · 2017: 2 · 2016: 5 · 2015: 5 · 2014: 14 · 2013: 11 · 2012: 9
- FWCI
- 0.81
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Current Opinion in Genetics & Development (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Cancer Institute (P30CA008748)
- National Institute of Diabetes and Digestive and Kidney Diseases (R01DK084391)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (R01HD052115)
- 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
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular Mechanics and Interactions
- Keywords
- mouse embryo, axis formation, gastrulation, germ layer formation, cell motility, tissue interactions, live imaging, cell dynamics, early embryonic development
- MeSH terms
- Animals, Cell Communication, Cell Movement, Embryo, Mammalian, Signal Transduction, Cell Polarity, Cell Lineage, Body Patterning, Embryonic Development, Mice, Gastrulation
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