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The anterior visceral endoderm of the mouse embryo is established from both preimplantation precursor cells and by de novo gene expression after implantation

Torres-Padilla, Maria-Elena and Richardson, Lucy and Kolasinska, Paulina and Meilhac, Sigolène M. and Luetke-Eversloh, Merlin Verena and Zernicka-Goetz, Magdalena (2007) The anterior visceral endoderm of the mouse embryo is established from both preimplantation precursor cells and by de novo gene expression after implantation. Developmental Biology, 309 (1). pp. 97-112. ISSN 0012-1606. PMCID PMC3353121. doi:10.1016/j.ydbio.2007.06.020. https://resolver.caltech.edu/CaltechAUTHORS:20190418-150055920

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[img] Image (JPEG) (Supplementary Fig. 1. Embryonic growth and staging of embryos cultured under time-lapse imaging) - Supplemental Material
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[img] Image (JPEG) (Supplementary Fig. 2. Examples of E5.25 embryos in which the distribution of Cer1/GFP-positive cells are located in one (top) or in opposite (bottom) sides of the embryo) - Supplemental Material
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[img] PDF (Supplementary Fig. 3. Examples of embryos in which Cer-1/GFP-positive cells lose expression (A, white arrow) or divide (B, white arrow) during culture from E4.75) - Supplemental Material
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[img] Image (JPEG) (Supplementary Fig. 4. Immunostaining of CER1 and LEFTY after in vitro culture and time-lapse imaging. Embryos were cultured from E5.0 for 15 h as in Fig. 6) - Supplemental Material
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[img] PDF (Supplementary Fig. 5. Examples of embryos in which Cer-1/GFP-positive cells increase (A, white arrow) or maintain (B, white arrow) or lose expression (C, white arrow) during culture from E5.0) - Supplemental Material
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[img] PDF (Supplementary Fig. 6. Examples of embryos in which Cer-1/GFP-positive cells gain (A, white arrow) or increase expression (B, white arrow) during culture from E5.25) - Supplemental Material
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Abstract

Initiation of the development of the anterior–posterior axis in the mouse embryo has been thought to take place only when the anterior visceral endoderm (AVE) emerges and starts its asymmetric migration. However, expression of Lefty1, a marker of the AVE, was recently found to initiate before embryo implantation. This finding has raised two important questions: are the cells that show such early, preimplantation expression of this AVE marker the real precursors of the AVE and, if so, how does this contribute to the establishment of the AVE? Here, we address both of these questions. First, we show that the expression of another AVE marker, Cer1, also commences before implantation and its expression becomes consolidated in the subset of ICM cells that comprise the primitive endoderm. Second, to determine whether the cells showing this early Cer1 expression are true precursors of the AVE, we set up conditions to trace these cells in time-lapse studies from early periimplantation stages until the AVE emerges and becomes asymmetrically displaced. We found that Cer1-expressing cells are asymmetrically located after implantation and, as the embryo grows, they become dispersed into two or three clusters. The expression of Cer1 in the proximal domain is progressively diminished, whilst it is reinforced in the distal–lateral domain. Our time-lapse studies demonstrate that this distal–lateral domain is incorporated into the AVE together with cells in which Cer1 expression begins only after implantation. Thus, the AVE is formed from both part of an ancestral population of Cerl-expressing cells and cells that acquire Cer1 expression later. Finally, we demonstrate that when the AVE shifts asymmetrically to establish the anterior pole, this occurs towards the region where the earlier postimplantation expression of Cer1 was strongest. Together, these results suggest that the orientation of the anterior–posterior axis is already anticipated before AVE migration.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1016/j.ydbio.2007.06.020DOIArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3353121/PubMed CentralArticle
ORCID:
AuthorORCID
Zernicka-Goetz, Magdalena0000-0002-7004-2471
Additional Information:© 2007 Elsevier. Under an Elsevier user license. Received 20 December 2006, Revised 26 June 2007, Accepted 28 June 2007, Available online 3 July 2007. We are grateful to Dr. J. Belo for the Cer1/GFP trasngenic line, Prof. H. Hamada for the Lefty1 probe, Dr. M. Pontoglio for the vHNF1 antibody and Dr. S. Frankenberg for the Cer1 probe. We are grateful to BBSRC and Wellcome Trust grants to MZG which funded this work. MZG is Wellcome Senior Research Fellow. M.E.T-P is a recipient of an EMBO long-term fellowship (present address: Institut de Genetique et de Biologie Moleculaire et Cellulaire, 1 rue Laurent Fries, Strasbourg, France). L.R. held a BBSRC studentship and S.M.M was support by a Marie Curie Intra-European Fellowship within the Sixth European Framework Programme (present address: Department of Developmental Biology, Pasteur Institute, 25 rue du Dr. Roux, Paris, France).
Funders:
Funding AgencyGrant Number
Biotechnology and Biological Sciences Research Council (BBSRC)UNSPECIFIED
Wellcome TrustUNSPECIFIED
European Molecular Biology Organization (EMBO)UNSPECIFIED
Marie Curie FellowshipUNSPECIFIED
Subject Keywords:Cerl; AVE; Anterior-posterior axis; Mouse embryo; Asymmetry; Implantation
Issue or Number:1
PubMed Central ID:PMC3353121
DOI:10.1016/j.ydbio.2007.06.020
Record Number:CaltechAUTHORS:20190418-150055920
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20190418-150055920
Official Citation:Maria-Elena Torres-Padilla, Lucy Richardson, Paulina Kolasinska, Sigolène M. Meilhac, Merlin Verena Luetke-Eversloh, Magdalena Zernicka-Goetz, The anterior visceral endoderm of the mouse embryo is established from both preimplantation precursor cells and by de novo gene expression after implantation, Developmental Biology, Volume 309, Issue 1, 2007, Pages 97-112, ISSN 0012-1606, https://doi.org/10.1016/j.ydbio.2007.06.020. (http://www.sciencedirect.com/science/article/pii/S0012160607011566)
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:94800
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:18 Apr 2019 23:15
Last Modified:16 Nov 2021 17:07

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