Neural tube formation in the mouse: a morphometric and computerized three-dimensional reconstruction study of the relationship between apical constriction of neuroepithelial cells and the shape of the neuroepithelium

Abstract

Morphometry and computerized three-dimensional reconstruction were used to study the relationship between apical constriction of neuroepithelial cells and the pattern of bending of the neuroepithelium in the developing neural tube of the 12-somite mouse embryo. The neuroepithelium of the mouse exhibits prominent regional variations in size and shape along the embryo axis. The complex shape of most of the cephalic neural tube (e.g., forebrain and midbrain) is due to the coexistence of concave and convex bending sites whereas more caudal regions (e.g., hindbrain and spinal cord) generally lack sites of convex bending and have a relatively simple shape. The apical morphology of neuroepithelial cells was found to be correlated more closely with the local status of bending of the neuroepithelium than with the specific region of the neural tube in which they are located. In areas of enhanced apical constriction, microfilament bundles were particularly prominent. Morphometry revealed that patterns of bending of the neuroepithelium were correlated almost exactly with those of apical constriction throughout the forming neural tube. These findings support the idea that apical constriction of neuroepithelial cells, resulting from tension generated by microfilament bundles, plays a major role in bending of the neuroepithelium during neural tube formation in the mouse.

A Dynamic Microtubule Cytoskeleton Directs Medial Actomyosin Function during Tube Formation

“…A topologically related process in Xenopus , the apical constriction of bottle cells during gastrulation, depends on both intact actomyosin and microtubule networks, revealed when constriction upon treatment with specific chemical inhibitors was analyzed (Lee and Harland, 2007). Furthermore, tube formation in mammals, where live analysis is technically very challenging, also depends on apical constriction (Bush et al., 1990). Thus, data obtained on tubulogenesis in more accessible models will be a valuable guide to further studies in mammals.…”

Apical constriction: A cell shape change that can drive morphogenesis

“…This occurs in a variety of vertebrate systems, including amphibians (Baker and Schroeder, 1967; Burnside, 1971; Schroeder, 1970), birds (Karfunkel, 1972; Schoenwolf and Franks, 1984) and mammals (Moore et al, 1987; Morriss-Kay, 1981; Shum and Copp, 1996). Patterns of bending in the neural tube have been shown to correlate with regions of apical constriction in the neuroepithelium (Bush et al, 1990; Nagele and Lee, 1987). Dense distributions of microfilaments have been observed under apical surfaces of neuroepithelial cells, leading to the long-standing hypothesis that a contractile network is responsible for hingepoint cell apical constriction (Baker and Schroeder, 1967; Schroeder, 1970; Freeman, 1972; Burnside, 1973; Schroeder, 1973; Nagel and Lee, 1980).…”

Evidence for multi‐site closure of the neural tube in humans

“…The process resulting in fold elevation is complicated and influenced by the cytoskeleton and cell shape of the neuroepithelium [Bush et al, 1990;Svoboda and O'Shea, 1987;Lee and Nagele, 1985;Sadler et al,, 19861, mesenchymal cells and extracellular matrix [MorrisWiman and Brinkley, 19901, and elongation of the lateral edge of the neural plate [Jacobson and Tam, 19821. Fusion of closure 4 is unique in that the neural folds remain separate and closure occurs by growth of a membrane which eventually covers the rhombencephalon [Golden and Chernoff, 1993;Geelan and Langman, 19771.…”