Morphogenetic movements driving neural tube closure in Xenopus require myosin IIB

Abstract

Vertebrate neural tube formation involves two distinct morphogenetic events -convergent extension (CE) driven by medio-lateral cell intercalation, and bending of the neural plate driven largely by cellular apical constriction. However, the cellular and molecular biomechanics of these processes are not understood. Here, using tissue-targeting techniques, we show that the myosin IIB motor protein complex is essential for both these processes, as well as for conferring resistance to deformation to the neural plate tissue. We show that myosin IIB is required for actin-cytoskeletal organization in both superficial and deep layers of the Xenopus neural plate. In the superficial layer, myosin IIB is needed for apical actin accumulation, which underlies constriction of the neurepithelial cells, and that ultimately drive neural plate bending, whereas in the deep neural cells myosin IIB organizes a cortical actin cytoskeleton, which we describe for the first time, and that is necessary for both normal neural cell cortical tension and shape and for autonomous CE of the neural tissue. We also show that myosin IIB is required for resistance to deformation (‘stiffness’) in the neural plate, indicating that the cytoskeleton-organizing roles of this protein translate in regulation of the biomechanical properties of the neural plate at the tissue-level.

Shaping organs by a wingless-int/Notch/nonmuscle myosin module which orients feather bud elongation

“…It is critical for cell intercalation in Drosophila germ band convergent extension (20). NM IIB is the subtype most frequently reported to mediate directional cell migration in vertebrates (17,39). In several cases canonical Wnt signaling lies upstream of NM II (40)(41)(42).…”

“…Polarized tissue morphogenesis can be attributed either to polarized cell rearrangement (17), oriented cell division (18), or localized cell proliferation/apoptosis (5,19). Previously we tried to examine the orientation of mitosis through γ-tubulin staining.…”

“…To test whether polarized cell rearrangement contributes to feather bud elongation we examined the expression patterns of NM II isoforms. These proteins are highly conserved motor proteins for cell motility (17,20). Mammals have three NM II isoforms (A, B, and C), distinguished by the nonhelical tail region of the heavy chains (21).…”

The roles and regulation of multicellular rosette structures during morphogenesis

“…Neurulation depends on a series of morphogenetic cellular movements that lead to neural tube closure (Copp and Greene, 2010). The importance of apical constriction in this process has been recognized and highly studied, and is dependent on myosin-II (Rolo et al, 2009). The scaffolding molecule Shroom3 is also important for neurulation in both mice and Xenopus (Haigo et al, 2003;Hildebrand and Soriano, 1999), as it is required in the apical localization of myosin-II (Hildebrand, 2005).…”

Cell movements of the deep layer of non-neural ectoderm underlie complete neural tube closure in Xenopus

“…Neural ectoderm cells undergo convergent extension and apical constriction: the former occurs with the cell-shape change to a bipolar morphology and cell rearrangement; the latter involves a morphological change in the cells to form a wedge shape (Burnside, 1971;Keller et al, 1992). The molecular and cellular mechanisms that regulate convergent extension and apical constriction have been extensively studied (Wallingford and Harland, 2002;Lee et al, 2007;Nishimura and Takeichi, 2008;Roffers-Agarwal et al, 2008;Rolo et al, 2009;Lee and Harland, 2010;Morita et al, 2010;Suzuki et al, 2010).…”