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An asymmetry in the frequency and position of mitosis in the epiblast precedes gastrulation and suggests a role for mitotic rounding in cell delamination during primitive streak epithelial-mesenchymal transition

View ORCID ProfileEvangéline Despin-Guitard, View ORCID ProfileNavrita Mathiah, View ORCID ProfileMatthew Stower, View ORCID ProfileWallis Nahaboo, View ORCID ProfileElif Sema Eski, View ORCID ProfileSumeet Pal Singh, View ORCID ProfileShankar Srinivas, View ORCID ProfileIsabelle Migeotte
doi: https://doi.org/10.1101/2020.02.21.959080
Evangéline Despin-Guitard
1Université Libre de Bruxelles, IRIBHM, Brussels B-1070, Belgium
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  • ORCID record for Evangéline Despin-Guitard
Navrita Mathiah
1Université Libre de Bruxelles, IRIBHM, Brussels B-1070, Belgium
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Matthew Stower
2Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford OX1 3QX, United Kingdom
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Wallis Nahaboo
1Université Libre de Bruxelles, IRIBHM, Brussels B-1070, Belgium
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Elif Sema Eski
1Université Libre de Bruxelles, IRIBHM, Brussels B-1070, Belgium
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Sumeet Pal Singh
1Université Libre de Bruxelles, IRIBHM, Brussels B-1070, Belgium
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Shankar Srinivas
2Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford OX1 3QX, United Kingdom
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Isabelle Migeotte
1Université Libre de Bruxelles, IRIBHM, Brussels B-1070, Belgium
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  • ORCID record for Isabelle Migeotte
  • For correspondence: imigeott@ulb.ac.be
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ABSTRACT

The epiblast, a pseudostratified epithelium, is the precursor for the three main germ layers required for body shape and organogenesis: ectoderm, mesoderm, and endoderm. At gastrulation, a subpopulation of epiblast cells constitutes a transient posteriorly located structure called the primitive streak, where cells that undergo epithelial-mesenchymal transition make up the mesoderm and endoderm lineages.

In order to observe the behavior of individual cells, epiblast cells were labeled ubiquitously or in a mosaic fashion using fluorescent membrane reporters. The cell shapes of individual cells and the packing and behaviour of neighbouring cells during primitive streak formation were recorded through live time-lapse imaging. Posterior epiblast displayed a higher frequency of rosettes, a signature of cell rearrangements, prior to primitive streak initiation. A third of rosettes were associated with a central cell undergoing mitosis. Interestingly, cells at the primitive streak, in particular delaminating cells, underwent mitosis twice more frequently than other epiblast cells, suggesting a role for cell division in epithelial-mesenchymal transition. Pseudostratified epithelia are characterized by interkinetic nuclear migration, where mitosis occurs at the apical side of the epithelium. However, we found that exclusively on the posterior side of the epiblast, mitosis was not restricted to the apical side. Non-apical mitosis was apparent as early as E5.75, just after the establishment of the anterior-posterior axis, and prior to initiation of epithelial-mesenchymal transition. Non-apical mitosis was associated with primitive streak morphogenesis, as it occurred specifically in the streak even when ectopically located. Most non-apical mitosis resulted in one or two daughter cells leaving the epiblast layer to become mesoderm. Furthermore, in contrast to what has been described in other pseudostratified epithelia such as neuroepithelium, the majority of cells dividing apically detached completely from the basal pole in the epiblast.

Cell rearrangement associated with mitotic cell rounding in the posterior epiblast during gastrulation, in particular when it occurs on the basal side, might thus facilitate cell ingression through the PS and transition to a mesenchymal phenotype.

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An asymmetry in the frequency and position of mitosis in the epiblast precedes gastrulation and suggests a role for mitotic rounding in cell delamination during primitive streak epithelial-mesenchymal transition
Evangéline Despin-Guitard, Navrita Mathiah, Matthew Stower, Wallis Nahaboo, Elif Sema Eski, Sumeet Pal Singh, Shankar Srinivas, Isabelle Migeotte
bioRxiv 2020.02.21.959080; doi: https://doi.org/10.1101/2020.02.21.959080
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An asymmetry in the frequency and position of mitosis in the epiblast precedes gastrulation and suggests a role for mitotic rounding in cell delamination during primitive streak epithelial-mesenchymal transition
Evangéline Despin-Guitard, Navrita Mathiah, Matthew Stower, Wallis Nahaboo, Elif Sema Eski, Sumeet Pal Singh, Shankar Srinivas, Isabelle Migeotte
bioRxiv 2020.02.21.959080; doi: https://doi.org/10.1101/2020.02.21.959080

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