Nodal signal is required for morphogenetic movements of epiblast layer in the pre‐streak chick blastoderm

Abstract

During axis formation in amniotes, posterior and lateral epiblast cells in the area pellucida undergo a counterrotating movement along the midline to form primitive streak (Polonaise movements). Using chick blastoderms, we investigated the signaling involved in this cellular movement in epithelial-epiblast. In cultured posterior blastoderm explants from stage X to XI embryos, either Lefty1 or Cerberus-S inhibited initial migration of the explants on chamber slides. In vivo analysis showed that inhibition of Nodal signaling by Lefty1 affected the movement of DiI-marked epiblast cells prior to the formation of primitive streak. In Lefty1-treated embryos without a primitive streak, Brachyury expression showed a patchy distribution. However, SU5402 did not affect the movement of DiI-marked epiblast cells. Multi-cellular rosette, which is thought to be involved in epithelial morphogenesis, was found predominantly in the posterior half of the epiblast, and Lefty1 inhibited the formation of rosettes. Three-dimensional reconstruction showed two types of rosette, one with a protruding cell, the other with a ventral hollow. Our results suggest that Nodal signaling may have a pivotal role in the morphogenetic movements of epithelial epiblast including Polonaise movements and formation of multi-cellular rosette.

Collective Epithelial and Mesenchymal Cell Migration During Gastrulation

“…It is thought that, in the chicken embryo, the mesoderm is induced by a combination of Wnt and TGF-beta signals coming from a Nieuwkoop centre located in the posterior marginal zone [20, 21]. These mesoderm cells are endowed with different cell behaviours, which are likely to be critical for the execution of these cell flows, since treatments that block mesoderm differentiation also appear to block these cell flow patterns [18, 22]. An interesting but open question is when these rotational movements start, before or during mesoderm differentiation.…”

“…Nodal signalling has been implicated in streak formation through its effects on mesoderm differentiation [45]. More recently it has been demonstrated that inhibition of Nodal signalling results in delayed vortex movements and is associated with a reduction in rosette formation, providing further support for a functional link between ingression and streak formation [22, 45]. …”

The roles and regulation of multicellular rosette structures during morphogenesis

“…Recently, rosettes have been described during this process. In the epiblast of the chick embryo, rosettes with actin-rich centers are visible within the developing primitive streak (Wagstaff et al, 2008), and rosette number increases as development progresses (Chuai and Weijer, 2008;Wagstaff et al, 2008;Yanagawa et al, 2011). These rosettes are dependent on Nodal signaling, as inhibition of Nodal pathway members results in reduced rosette numbers (Yanagawa et al, 2011).…”

Taking the Middle Road

“…A lack of primitive streak formation in chick embryos overexpressing Nodal antagonists extends the case to birds and the last of the four core vertebrate models, suggesting a pan-vertebral function (Yanagawa et al, 2011).…”