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The amniote primitive streak is defined by epithelial cell intercalation before gastrulation

Nature volume 449, pages 1049–1052 (2007)Cite this article

Abstract

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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Figure 1: Cell movements and behaviours during primitive streak formation.
Figure 2: Summary of expression patterns of Wnt-PCP genes.
Figure 3: The Wnt-PCP pathway controls primitive streak morphogenesis.
Figure 4: Early medio-lateral intercalation as an evolutionary step that shapes the primitive streak.

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Acknowledgements

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M. Tada, N. Itasaki and V. Papaioannou for reagents; C. Thrasivoulou for advice on imaging; A. Nieto for sharing unpublished information and S. Fraser, M. Tada and A. Streit for comments on the manuscript.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.

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Authors and Affiliations

  1. Department of Anatomy & Developmental Biology, University College London, Gower Street, London WC1E 6BT, UK,

    Octavian Voiculescu, Federica Bertocchini, Lewis Wolpert & Claudio D. Stern

  2. Department of Biology, Gilmer Hall, University of Virginia, Charlottesville, Virginia 22903, USA,

    Ray E. Keller

Authors
  1. Octavian Voiculescu
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  2. Federica Bertocchini
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  3. Lewis Wolpert
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  4. Ray E. Keller
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  5. Claudio D. Stern
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Correspondence to Octavian Voiculescu or Claudio D. Stern.

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Supplementary information

Supplementary Information

This file contains Supplementary Figures S5-S6 with Legends, Supplementary Methods and Legends to Supplementary Videos S1-S4. (PDF 1744 kb)

Supplementary Video S1

This file contains Supplementary Video S1 which shows chick embryo development and cell movements at stages XIII to 5. (MOV 8472 kb)

Supplementary Video S2

This file contains Supplementary Video S2 which shows cell divisions during primitive streak formation. (MOV 339 kb)

Supplementary Video S3

This file contains Supplementary Video S3 which shows cell movements during formation of the primitive streak. (MOV 1328 kb)

Supplementary Video S4

This file contains Supplementary Video S4 which shows relative movements of cells during formation of the primitive streak. (MOV 883 kb)

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Voiculescu, O., Bertocchini, F., Wolpert, L. et al. The amniote primitive streak is defined by epithelial cell intercalation before gastrulation. Nature 449, 1049–1052 (2007). https://doi.org/10.1038/nature06211

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