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Labo

Shaping the embryo

Project description :

We use the advantages of ascidian early embryogenesis to study the control of  1) Cell number,  2) Cell size,  and 3) Cell position.  Since neither cell migration nor cell death occur before gastrulation, ascidian embryos rely upon these three cell biological mechanisms to generate the blastula-stage embryo that displays the typical fate map of chordates.

 

 

  • Cell Number

We found that cell number is precisely controlled such that all ascidian embryos display a 24-cell stage.  This asynchrony is maintained (at the 44-cell stage) and amplified giving rise to a 112-cell gastrula.  The onset of cell cycle asynchrony in ascidian embryos (at the 5th cell cycle, 16 cell stage) precedes the onset of gastrulation by 2 cell cycles, as is also the case in Zebrafish or Xenopus embryos.  We have shown that in the ascidian these phases of cell cycle remodeling depend upon a gene-regulatory network controlled by b-Catenin (McDougall et al, 2012; Dumollard et al., 2013).


Figure 1: Cell cycle timing (fig 1 Dumollard et al., 2013)

 

  • Cell size

In parallel we studied how unequal cell division (UCD) is controlled in the ascidian embryo.  We had previously shown that UCD in Phallusia embryos occurred due to the attraction of one spindle pole towards a cortical structure termed the CAB (for centrosome-attracting body) during prometaphase through anaphase (Prodon et al., 2010, McDougall et al., 2015).  We recently discovered that the microtubule depolymerase Kif2 is localized to the CAB and is involved in reducing the size of the proximal aster thereby facilitating the pulling of the spindle pole towards the CAB (Costache et al., 2017 in review).  In terms of shaping the whole embryo, CAB ablation completely radializes the embryo indicating that UCD affects the shape of all blastomeres in the early embryo.

 

 
Figure 2: Centrosome-attracting body

 

  • Cell position

Recently we discovered that an apical shape sensing mechanism operates to align all the spindles parallel to the outside (apical) surface of the embryo, orienting them within each cell's longest axis in the apical plane (with the exception of those oriented by the CAB) (Dumollard et al., 2017).  Intriguingly, this apical shape-dependent orientation of the mitotic spindles depended upon cell cycle asynchrony, since abolition of the 24-cell stage disrupted the invariant cleavage pattern (Dumollard et al., 2017).  We provided a computational model based on apical cell surface shape that predicts cell division orientation and hence cell position up to the blastula stage (Dumollard et al., 2017).  Finally, our model provides a partial cell-biological explanation of the invariant cleavage pattern of ascidian embryos that was elegantly described by Conklin more than a century ago (Conklin, 1905).

 


Figure 3: Cell position

 

 

Movie 1: 32 cell animal extract planes

 

 

Publications :

- Conklin E.G., (1905) The organization and cell-lineage of the Ascidian Egg. Journal of the Academy of Natural Sciences of Philadelphia 3 (1). (View or download pdf)

 

- Vlad Costache1, Celine Hebras, Gerard Pruliere, Lydia Besnardeau, Margaux Failla, Richard R. Copley, David Burgess, Janet Chenevert & Alex McDougall. Kif 2 localizes to a subdomain of cortical endoplasmic reticulum that drives asymmetric spindle position. Nature Communications 8, Article number: 917(2017) doi:10.1038/s41467-017-01048-8. (View or download pdf)

 

- Dumollard R, Hebras C, Besnardeau L, McDougall A. (2013) Beta-catenin patterns the cell cycle during maternal-to-zygotic transition in urochordate embryos. Dev Biol.;384(2):331-42. (View or download pdf)

 

- Dumollard R, Minc N, Salez G, BEN Aicha S, Bekkouche F, Hebras C, Besnardeau L, McDougall A. (2017) The invariant cleavage pattern displayed by ascidian embryos depends on spindle positioning along the cell's longest axis in the apical plane and relies on asynchronous cell divisions. Elife. Jan 25;6. pii: e19290. (View or download pdf)

 

- Prodon F, Chenevert J, Hébras C, Dumollard R, Faure E, Gonzalez-Garcia J, Nishida H, Sardet C, McDougall A. (2010) Dual mechanism controls asymmetric spindle position in ascidian germ cell precursors. Development. Jun;137(12):2011-21. (View or download pdf)

 

- McDougall, A., Chenevert, J. and Dumollard, R. (2012). Cell Cycle Control in Oocytes and during Embryonic Cleavage Cycles in Ascidians. Int Rev Cell Mol Biol. 297, 237-266. (View or download pdf)

 

- McDougall A, Chenevert J, Pruliere G, Costache V, Hebras C, Salez G, Dumollard R (2015) Centrosomes and spindles in ascidian embryos and eggs. Methods in Cell Biology, Volume 129, 317-39. (View or download pdf)

 

Protocols :

Omero, Imaging data base :

 

17/10/17

Traductions :

 

 Alex McDougall

  

Rémi Dumollard

 

Ievgeniia Gazo

 

Isa Gomes

 

 Bioclips

Fertilization

Meiosis

 

 

06/10/17