Epithelial Cell Wedging and Neural Trough Formation Are Induced Planarly inXenopus,without Persistent Vertical Interactions with Mesoderm

Abstract

In this study we investigate the induction of the cell behaviors underlying neurulation in the frog, Xenopus laevis. Although planar signals from the organizer can induce convergent extension movements of the posterior neural tissue in explants, the remaining morphogenic processes of neurulation do not appear to occur in absence of vertical interactions with the organizer (R. Keller et al. , 1992, Dev. Dyn. 193, 218-234). These processes include: (1) cell elongation perpendicular to the plane of the epithelium, forming the neural plate; (2) cell wedging, which rolls the neural plate into a trough; (3) intercalation of two layers of neural plate cells to form one layer; and (4) fusion of the neural folds. To allow planar signaling between all the inducing tissues of the involuting marginal zone and the responding prospective ectoderm, we have designed a "giant sandwich" explant. In these explants, cell elongation and wedging are induced in the superficial neural layer by planar signals without persistent vertical interactions with underlying, involuted mesoderm. A neural trough forms, and neural folds form and approach one another. However, the neural folds do not fuse with one another, and the deep cells of these explants do not undergo their normal behaviors of elongation, wedging, and intercalation between the superficial neural cells, even when planar signals are supplemented with vertical signaling until the late midgastrula (stage 11.5). Vertical interactions with mesoderm during and beyond the late gastrula stage were required for expression of these deep cell behaviors and for neural fold fusion. These explants offer a way to regulate deep and superficial cell behaviors and thus make possible the analysis of the relative roles of these behaviors in closing the neural tube.

Ror2 signaling is required for local upregulation of GDF6 and activation of BMP signaling at the neural plate border

“…Specifically, Ror2 depletion caused disruption of coordinated cell orientation and polarity at the lateral neural plate and flattening of the NPB area. Neural PCP activity and vertical signals from the underlying mesoderm interact to coordinate cell polarity and convergent extension movements in the neural plate (Elul and Keller, 2000;Poznanski et al, 1997;Wallingford and Harland, 2002). Disturbed morphogenesis during gastrulation and early neurulation would result in aberrant positioning of these tissues and thereby expose NPB precursors to different concentrations of morphogens from the dorsoventral gradients and the underlying mesoderm.…”

Neural tube closure requires Dishevelled-dependent convergent extension of the midline

“…3F). Although thinning of the neural plate has been suggested to contribute to tube closure (Poznanski et al, 1997), because it was not consistently observed (Fig. 3E), this midline bulge of the neuroepithelium cannot be the primary cause of the open NT phenotype in Xdd1-injected embryos.…”

“…It has been shown that proper signaling from underlying mesoderm is required for the fusion of neural folds in Xenopus (Poznanski et al, 1997), so it is possible that the NT defect arises from disruption of involution due to defective convergent extension in the mesoderm. However, this possibility is unlikely, as Xdd1 open-NT embryos successfully complete gastrulation (not shown).…”

“…Intrinsic processes include elongation and shaping of the neural plate by cell rearrangement, cell shapechange, and cell division; elevation and apposition of the neural folds; and fusion of the folds at the dorsal midline (Davidson and Keller, 1999;Jacobson and Gordon, 1976;Schoenwolf and Alvarez, 1989;Schroeder, 1970;van Straaten et al, 1993). Extrinsic processes include medial pushing on the neural folds by the adjacent epidermis, as well as inductive and mechanical contributions from the underlying mesoderm (Alvarez and Schoenwolf, 1992;Brun and Garson, 1983;Jacobson and Jacobson, 1973;Moury and Schoenwolf, 1995;Poznanski et al, 1997;Schroeder, 1970;van Straaten et al, 1996).…”

Force production and mechanical accommodation during convergent extension

“…In both cases the fragments of the dorsal isolate that contain the most paraxial mesoderm produce the greater stress. However, the dorsal isolate consists of both neural and mesodermal tissues, and both tissues are known to elongate in isolation (Elul et al, 1997;Poznanski et al, 1997;Keller et al, 2000). As the neural plate in Xenopus is only two cells thick, we utilized a neural plate 'sandwich' (NS) explant created from two neural plates isolated from embryos at mid-to late-gastrula stages (st. 11.5-12; Fig.…”