Segmental Groove Formation

A fascinating problem in developmental biology is the transformation of a simple egg into an animal with complex organs.

To get a better understanding of morphogenesis, we are studying a simple step towards the making of the Drosophila larva: The folding of a single layered epithelium that forms the segmental furrows. These furrows are present at mid embryogenesis and separate the segments just behind the stripe of engrailed cells that mark the posterior cells of the previous segment. A set of interesting molecule is enriched specifically in the groove cells: the actin binding molecule enabled, the apical factors crumbs and the atypical protein kinase C.

For many years the morphogen model prevailed to explain how the shape of organs is determined. A morphogen is a secreted molecule with an instructive capacity that determines cell fate depending on its concentration. The morphogen is secreted by an organizing center that induces na•ve fields of cells. This model has been proposed to explain segmental furrow formation, where an organizer, determined by the engrailed transcription factor uses the secreted factor Hedgehog to induce groove fate.

We have shown that this view is too simplistic as the groove cells are indeed determined much earlier in development. We traced back their origin with the marker Odd skipped. We find that the function of the organizer is to maintain this fate as long as the cells end up next to the organizer. Our experiments suggest that the secreted factor Hedgehog is mediating this paracrine signaling. In any case, the organizer is not able to induce the groove fate in random cells. These data provide a different view of the organizer. Whereas before it was seen as an entity sufficient to generate shape across an epithelium, we show that it is only one part of a wider unit. A second group of cells are defined at the same time and next to the organizer, and are responsible for the organ fate. We propose that the function of the organizer is to maintain the fate of these cells at the right location.

Above: In embryos were the signaling molecule hedgehog is over-expressed in the engrailed cells we can find more groove cells. The following figure shows such an embryo with four rows of Odd skipped cells in blue, and the accumulation of the apical marker Crumbs in green in these cells. Cadherin, in red are uniform. Crumbs and Odd skipped can be viewed with red/green glasses in the two last images.