Abstract
Zebrafish signal transducer and activator of transcription 3 (STAT3) controls the cell movements during gastrulation. Here, we show that noncell-autonomous activity of STAT3 signaling in gastrula organizer cells controls the polarity of neighboring cells through Dishevelled-RhoA signaling in the Wnt-planar cell polarity (Wnt-PCP) pathway. In STAT3-depleted embryos, although all the known molecules in the Wnt-PCP pathway were expressed normally, the RhoA activity in lateral mesendodermal cells was down-regulated, resulting in severe cell polarization defects in convergence and extension movements identical to Strabismus-depleted embryos. Cell-autonomous activation of Wnt-PCP signaling by ΔN-dishevelled rescued the defect in cell elongation, but not the orientation of lateral mesendodermal cells in STAT3-depleted embryos. The defect in the orientation could be rescued by transplantation of shield cells having noncell-autonomous activity of STAT3 signaling. These results suggest that the cells undergoing convergence and extension movement may sense the gradient of signaling molecules, which are expressed in gastrula organizer by STAT3 and noncell-autonomously activate PCP signaling in neighboring cells during zebrafish gastrulation.
Highlights
Vertebrate gastrulation involves the fate specification and coordinated movement of three germ layers
We previously reported that the activity of STAT3 in the zebrafish gastrula organizer is noncell-autonomously essential for the convergence and extension movement of neighboring cells, and cell-autonomously for the anterior migration of organizer cells
Consistent with this, transplantation of shield cells having cell-autonomous but not noncell-autonomous activity of STAT3 signaling could not rescue the defect in convergence and extension (Fig. 1 D and Fig. 2 D), indicating that noncell-autonomous activity of STAT3 signaling in organizer cells was essential for dorsal convergence movement of lateral mesendodermal cells
Summary
We show that noncell-autonomous activity of STAT3 signaling in gastrula organizer cells controls the polarity of neighboring cells through Dishevelled-RhoA signaling in the Wnt-planar cell polarity (WntPCP) pathway. In STAT3-depleted embryos, all the known molecules in the Wnt-PCP pathway were expressed normally, the RhoA activity in lateral mesendodermal cells was down-regulated, resulting in severe cell polarization defects in convergence and extension movements identical to Strabismus-depleted embryos. The defect in the orientation could be rescued by transplantation of shield cells having noncellautonomous activity of STAT3 signaling These results suggest that the cells undergoing convergence and extension movement may sense the gradient of signaling molecules, which are expressed in gastrula organizer by STAT3 and noncell-autonomously activate PCP signaling in neighboring cells during zebrafish gastrulation
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