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Active cell movements coupled to positional induction are involved in lineage segregation in the mouse blastocyst

Meilhac, Sigolène M. and Adams, Richard J. and Morris, Samantha A. and Danckaert, Anne and Le Garrec, Jean-François and Zernicka-Goetz, Magdalena (2009) Active cell movements coupled to positional induction are involved in lineage segregation in the mouse blastocyst. Developmental Biology, 331 (2). pp. 210-221. ISSN 0012-1606. PMCID PMC3353123. doi:10.1016/j.ydbio.2009.04.036. https://resolver.caltech.edu/CaltechAUTHORS:20190417-163115154

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[img] Image (JPEG) (Fig. S1. Live-imaging of mouse blastocysts is compatible with normal development) - Supplemental Material
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[img] Image (JPEG) (Fig. S2. Mitosis and apoptosis in the blastocyst inner cell mass. (A) Cell nuclei within the ICM of H2B-EGFP transgenic blastocysts were tracked manually and identified by numbers) - Supplemental Material
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[img] Image (JPEG) (Fig. S3. Parameters and outputs of the computer model) - Supplemental Material
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[img] Video (QuickTime) (Fig1 video1. Trajectories of the movement of cells in the blastocyst ICM) - Supplemental Material
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[img] Video (QuickTime) (Fig1 video2. Dynamic cell shape of ICM cells with protrusions. Accompanying movie of Fig. 1) - Supplemental Material
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[img] Video (QuickTime) (Fig2 video1. Nocodazole treatment does not inhibit ICM cell movement. Accompanying movie of Fig. 2) - Supplemental Material
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[img] Video (QuickTime) (Fig2 video2. Nocodazole treatment does not inhibit ICM cell protrusions) - Supplemental Material
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[img] Video (QuickTime) (Fig2 video3. Cytochalasin D treatment inhibits ICM cell movement) - Supplemental Material
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[img] Video (QuickTime) (Fig2 video4. Cytochalasin D treatment inhibits ICM cell protrusions) - Supplemental Material
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[img] Video (QuickTime) (Fig3 video1. Example of a stable surface ICM cell. Accompanying movie of Fig. 3A) - Supplemental Material
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[img] Video (QuickTime) (Fig3 video2. Example of a surface ICM cell moving to the deeper layers. Accompanying movie of Fig. 3B) - Supplemental Material
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[img] Video (QuickTime) (Fig3 video3. Example of a stable deeper ICM cell. Accompanying movie of Fig. 3C) - Supplemental Material
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[img] Video (QuickTime) (Fig3 video4. Example of a deeper ICM cell moving to the surface. Accompanying movie of Fig. 3D) - Supplemental Material
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Abstract

In the mouse blastocyst, some cells of the inner cell mass (ICM) develop into primitive endoderm (PE) at the surface, while deeper cells form the epiblast. It remained unclear whether the position of cells determines their fate, such that gene expression is adjusted to cell position, or if cells are pre-specified at random positions and then sort. We have tracked and characterised dynamics of all ICM cells from the early to late blastocyst stage. Time-lapse microscopy in H2B-EGFP embryos shows that a large proportion of ICM cells change position between the surface and deeper compartments. Most of this cell movement depends on actin and is associated with cell protrusions. We also find that while most cells are precursors for only one lineage, some give rise to both, indicating that lineage segregation is not complete in the early ICM. Finally, changing the expression levels of the PE marker Gata6 reveals that it is required in surface cells but not sufficient for the re-positioning of deeper cells. We provide evidence that Wnt9A, known to be expressed in the surface ICM, facilitates re-positioning of Gata6-expressing cells. Combining these experimental results with computer modelling suggests that PE formation involves both cell sorting movements and position-dependent induction.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1016/j.ydbio.2009.04.036DOIArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3353123/PubMed CentralArticle
ORCID:
AuthorORCID
Zernicka-Goetz, Magdalena0000-0002-7004-2471
Additional Information:© 2009 Elsevier Under an Elsevier user license. Received 23 January 2009, Revised 29 April 2009, Accepted 29 April 2009, Available online 5 May 2009. SMM dedicates this article to the late Pr Charles Babinet, who remains an inspiration. We are grateful to E. Parfitt, and ME. Torres-Padilla in the lab for help, Prs Tsien, Gurdon, Molkentin, Morrisey and Salbert for the gift of plasmids, Drs. Hadjantonakis and Papaioannou for the transgenic line, A. Sossick and the PFID for help with imaging and Pr Buckingham for allowing completion of the work in her lab. SMM was supported by a Marie Curie IEF within the Sixth European Framework Programme and by an EMBO fellowship and is now a research fellow in the INSERM. MZG is a Wellcome Senior Research Fellow. We are grateful to the Wellcome Trust fellowship and BBSRC grant to MZG which provided funding for this work.
Funders:
Funding AgencyGrant Number
Marie Curie FellowshipUNSPECIFIED
European Molecular Biology Organization (EMBO)UNSPECIFIED
Wellcome TrustUNSPECIFIED
Biotechnology and Biological Sciences Research Council (BBSRC)UNSPECIFIED
Subject Keywords:Mouse blastocyst; Cell lineage; Cell movement; Gata6; Wnt; Inner cell mass; Primitive endoderm
Issue or Number:2
PubMed Central ID:PMC3353123
DOI:10.1016/j.ydbio.2009.04.036
Record Number:CaltechAUTHORS:20190417-163115154
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20190417-163115154
Official Citation:Sigolène M. Meilhac, Richard J. Adams, Samantha A. Morris, Anne Danckaert, Jean-François Le Garrec, Magdalena Zernicka-Goetz, Active cell movements coupled to positional induction are involved in lineage segregation in the mouse blastocyst, Developmental Biology, Volume 331, Issue 2, 2009, Pages 210-221, ISSN 0012-1606, https://doi.org/10.1016/j.ydbio.2009.04.036. (http://www.sciencedirect.com/science/article/pii/S001216060900298X)
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:94775
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:18 Apr 2019 14:35
Last Modified:16 Nov 2021 17:07

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