The Endoderm of the Mouse Embryo Arises by Dynamic Widespread Intercalation of Embryonic and Extraembryonic Lineages
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The cell movements underlying the morphogenesis of the embryonic endoderm, the tissue that will give rise to the respiratory and digestive tracts, are complex and not well understood. Using live imaging combined with genetic labeling, we investigated the cell behaviors and fate of the visceral endoderm during gut endoderm formation in the mouse gastrula. Contrary to the prevailing view, our data reveal no mass displacement of visceral endoderm to extraembryonic regions concomitant with the emergence of epiblast-derived definitive endoderm. Instead, we observed dispersal of the visceral endoderm epithelium and extensive mixing between cells of visceral endoderm and epiblast origin. Visceral endoderm cells remained associated with the epiblast and were incorporated into the early gut tube. Our findings suggest that the segregation of extraembryonic and embryonic tissues within the mammalian embryo is not as strict as believed and that a lineage previously defined as exclusively extraembryonic contributes cells to the embryo.
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13ss (E8.75) is the latest stage at which the visceral endoderm versus definitive endoderm origin of gut tube cells can be unambiguously assigned using Afp-GFP or Ttr-Cre mouse lines.
“13ss (E8.75), approximately corresponding to midgestation, the latest stage analyzed in this study, is the latest stage for unambiguous assignment of visceral endoderm (VE)-vs.-definitive endoderm (DE) origin of gut tube cells using Afp-GFP7,12 or Ttr-Cre7,35 mouse lines.”
From The emergent landscape of the mouse gut endoderm at single-cell resolution (2019) · cites this paper as [7]
The Results section, “Visceral endoderm-derived cells are incorporated into the gut tube” (page unavailable), supports using Afp::GFP and Ttr::Cre to identify visceral endoderm-derived gut cells and says reporter reactivation precluded analysis at 20+ somites. It reports analysis at 12–18 somites, however, so it does not support 13 somites as the latest stage for unambiguous assignment. (LLM, conf=0.88)
Experimental — accuracy not yet measuredThe gut endoderm is comprised of cells of both PrE and DE.
“Our previous studies revealed the gut endoderm to be comprised of cells of both PrE and DE (Extended Data Fig. 1a)5–7.”
From The emergent landscape of the mouse gut endoderm at single-cell resolution (2019) · cites this paper as [7]
At gastrulation (E7.0-E7.5), EPI-derived DE cells intercalate into the emVE epithelium to form the gut endoderm.
“At gastrulation (E7.0-E7.5), EPI-derived (embryonic) DE cells intercalate into the emVE epithelium to form the gut endoderm5,7.”
From The emergent landscape of the mouse gut endoderm at single-cell resolution (2019) · cites this paper as [7]
Proximal-distal spatial patterning across the VE has been described preceding and coincident to onset of gastrulation at E6.5, with clear distinction between morphology and function of proximally located exVE and distal emVE.
“Proximal-distal spatial patterning across the VE has been described preceding, and coincident to the onset of gastrulation at E6.5, with a clear distinction between the morphology and function of the proximally located exVE (cuboidal epithelium, overlying the ExE, giving rise to yolk sac endoderm, YsE) and distal emVE (squamous epithelium, overlying the epiblast, contributing to the gut tube7).”
From The emergent landscape of the mouse gut endoderm at single-cell resolution (2019) · cites this paper as [7]
Gut endoderm comprises EPI-derived DE and VE descendants.
“Gut endoderm comprises EPI-derived DE and VE descendants6,7.”
From The emergent landscape of the mouse gut endoderm at single-cell resolution (2019) · cites this paper as [7]
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- Authors
- Kwon, G. S., Viotti, M., & Hadjantonakis, A.-K.
- Affiliations
- Cornell University (US)
- Corresponding author
- Hadjantonakis, Anna-Katerina
- Venue
- Developmental Cell
- Publisher
- Elsevier BV
- Published
- 2008-10
- Volume
- 15
- Issue
- 4
- Pages
- 509-520
- ISSN
- 1534-5807 (ISSN-L)
- PMC
- PMC2677989
- OpenAlex
- W2109293927
- Cited by
- 402
- References
- 69
- Citations by year
- 2026: 13 · 2025: 18 · 2024: 24 · 2023: 19 · 2022: 26 · 2021: 16 · 2020: 26 · 2019: 25 · 2018: 12 · 2017: 18 · 2016: 18 · 2015: 19 · 2014: 32 · 2013: 29 · 2012: 28
- FWCI
- 10.85
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 1750 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Developmental Cell (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health (RO1-HD052115)
- 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 › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- embryonic endoderm, visceral endoderm, cell intercalation, cell mixing, epiblast, extraembryonic lineages, gastrula, mouse embryo, cell fate, morphogenesis, lineage segregation
- MeSH terms
- Animals, Embryo, Mammalian, Endoderm, Extraembryonic Membranes, Gastrula, Image Processing, Computer-Assisted, Immunohistochemistry, Mice, Transgenic, Models, Biological, Morphogenesis, Respiratory System, RNA, Messenger, In Situ Hybridization, Gene Expression Regulation, Developmental, Cell Lineage, Transgenes, Gastrointestinal Tract, Green Fluorescent Proteins, Mice
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