Dynamic Maintenance of Cell Polarity with Respect to the Antero-posterior Axis in the Xenopus Neurula

This work reports that neurula-stage Xenopus notochordal and presumptive somitic cells dynamically maintain their orientation with respect to the A-P axis in the face of experimental perturbation. Time-lapse videomicroscopy studies show that explanted dorsal mesoderm cells reorient their long axes in response to experimental apposition of tissues from disparate A-P axial levels so as to remain orthogonal to the largest local difference in A-P tissue identity. The direction taken by reorienting cells is determined by their location in the context of global A-P tissue identity, demonstrating the action of both a local and a tissue-level or global component of the A-P signaling system. Cells of both the notochord and the somitic mesoderm reorient in response in A-P positional information disparity when apposed to the same tissue (notochord-to-notochord, somitic mesoderm to somitic mesoderm) and to the other tissue (notochord-to-somitic mesoderm), indicating that the maintenance of cell orientation with respect to the A-P axis is a phenomenon general to the mesoderm of the dorsal axis. Live confocal imaging studies show that reorienting cells retain their bipolar protrusive activity and are able to intercalate along their novel axis of orientation, producing tissue extension perpendicular to the original A-P axis. Although reorientation in notochord cells was elicited by apposition of normal notochords to animal cap tissue induced to mesodermal fates by expression of Xnr-1 mRNA, small-molecule based interdictions of the nodal, 3 FGF, and retinoic acid pathways failed to prevent reorientation. Examination of fixed samples stained for the matrix components XFibrillin and fibronectin demonstrate that the matrix-rich interface between apposed antiparallel notochords disintegrates over the time-course of reorientation, and is absent from the outset in somitic mesoderm-only appositions (that nonetheless reorient), indicating that the matrix does not play an instructive role in reorientation. The reorientation response we characterize reveals an important mechanism by which mesodermal cells of the dorsal axis maintain a polarized, parallel array perpendicular to the A-P axis, that may be critical to aligning the axes of A-P fate and tissue extension, and possibly maintenance of left-right registration of the somitic mesoderm across the notochord.

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