During gastrulation, a single epithelial cell layer, the ectoderm, generates two others: the mesoderm and the endoderm. In amniotes (birds and mammals), mesendoderm formation occurs through an axial midline structure, the primitive streak1, the formation of which is preceded by massive ‘polonaise’ movements2,3 of ectoderm cells. The mechanisms controlling these processes are unknown. Here, using multi-photon time-lapse microscopy of chick (Gallus gallus) embryos, we reveal a medio-lateral cell intercalation confined to the ectodermal subdomain where the streak will later form. This intercalation event differs from the convergent extension movements of the mesoderm described in fish and amphibians (anamniotes)4,5,6,7,8: it occurs before gastrulation and within a tight columnar epithelium. Fibroblast growth factor from the extraembryonic endoderm (hypoblast, a cell layer unique to amniotes) directs the expression of Wnt planar-cell-polarity pathway components to the intercalation domain. Disruption of this Wnt pathway causes the mesendoderm to form peripherally, as in anamniotes1,9. We propose that the amniote primitive streak evolved from the ancestral blastopore by acquisition of an additional medio-lateral intercalation event, preceding gastrulation and acting independently of mesendoderm formation to position the primitive streak at the midline.
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We thank C. Formstone, C. Marcelle, M. Tada, N. Itasaki and V. Papaioannou for reagents; C. Thrasivoulou for advice on imaging; A. Nieto for sharing unpublished information and S. Fraser, M. Tada and A. Streit for comments on the manuscript. This study was funded by grants from the BBSRC, the Medical Research Council and the European Union FP6 Network of Excellence ‘Cells into Organs’. O.V. was supported by an HFSP fellowship.
This file contains Supplementary Video S1 which shows chick embryo development and cell movements at stages XIII to 5.
This file contains Supplementary Video S2 which shows cell divisions during primitive streak formation.
This file contains Supplementary Video S3 which shows cell movements during formation of the primitive streak.
This file contains Supplementary Video S4 which shows relative movements of cells during formation of the primitive streak.
About this article
Myosin-II-mediated cell shape changes and cell intercalation contribute to primitive streak formation
Nature Cell Biology (2015)