Sequential Contraction and Exchange of Apical Junctions Drives Zippering and Neural Tube Closure in a Simple Chordate

Cho

Proc. Natl. Acad. Sci. U.S.A.

et al. 2017

153

Significance Neurulation has been intensively studied in lower vertebrates, but marked species differences call into question the relevance of these models for human neural tube (NT) closure. Here, using mouse embryos, we demonstrate that mammalian neural fold apposition results from constriction of the open posterior NT, which is biomechanically coupled to the zippering point by an F-actin network. Using the Zic2 mutant model, we show that genetic predisposition to spina bifida, which likely underlies most human cases, directly affects the biomechanics of closure. We also identify a NT closure point at the caudal end of the embryo. Many spina bifida cases correspond to this anatomic portion of the NT, suggesting that this closure point may be important in humans as well.

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

Biomechanical coupling facilitates spinal neural tube closure in mouse embryos

Cho

Proc. Natl. Acad. Sci. U.S.A.

et al. 2017

153

“…Eventually, the lateral plate borders, aided by force from the surrounding epidermis (Ogura et al, 2011), meet at the dorsal midline together with the adjacent epidermis. Sequential contractions and rearrangements of neural-epidermal junctions cause a progressive posterior-to-anterior fusion of the epidermis overlying the neural tube following involution (Hashimoto et al, 2015).…”

Section: Introductionmentioning

confidence: 99%

Nodal and FGF coordinate ascidian neural tube morphogenesis

Navarrete

Levine

2016

Development

Formation of the vertebrate neural tube represents one of the premier examples of morphogenesis in animal development. Here, we investigate this process in the simple chordate Ciona intestinalis. Previous studies have implicated Nodal and FGF signals in the specification of lateral and ventral neural progenitors. We show that these signals also control the detailed cellular behaviors underlying morphogenesis of the neural tube. Live-imaging experiments show that FGF controls the intercalary movements of ventral neural progenitors, whereas Nodal is essential for the characteristic stacking behavior of lateral cells. Ectopic activation of FGF signaling is sufficient to induce intercalary behaviors in cells that have not received Nodal. In the absence of FGF and Nodal, neural progenitors exhibit a default behavior of sequential cell divisions, and fail to undergo the intercalary and stacking behaviors essential for normal morphogenesis. Thus, cell specification events occurring prior to completion of gastrulation coordinate the morphogenetic movements underlying the organization of the neural tube.

“…The central nervous system of urochordate ascidian consists of fewer than 400 neural cells, and the cell lineages of neural cells and neighboring surface ectodermal cells have been well described 4,35,36 . These characteristics are advantageous for the analysis of neural cell behaviors, and thus the cellular mechanism of neural fold fusion was recently revealed in the ascidian Ciona intestinalis 37 . Actomyosin-driven rearrangement of the apical cell junction is a well-established mechanism of cell shape change that can promote morphogenesis (Fig.…”

Section: Introductionmentioning

confidence: 99%

“…2B). 37 These apical junction rearrangement events between NE and SE occur repeatedly, thereby zipping-up the neural plate into a tube. Although this mechanism is primarily important for the directional progression of the zippering in Ciona , filopodia is also observed, which may support the progression of the process of zippering 33 …”

Section: Introductionmentioning

confidence: 99%

Switching the rate and pattern of cell division for neural tube closure

Ogura

Sasakura

2016

Neurogenesis

The morphogenetic movement associated with neural tube closure (NTC) requires both positive and negative regulations of cell proliferation. The dual requirement of cell division control during NTC underscores the importance of the developmental control of cell division. In the chordate ascidian, midline fusions of the neural ectoderm and surface ectoderm (SE) proceed in the posterior-to-anterior direction, followed by a single wave of asynchronous and patterned cell division in SE. Before NTC, SE exhibits synchronous mitoses; disruption of the synchrony causes a failure of NTC. Therefore, NTC is the crucial turning point at which SE switches from synchronous to patterned mitosis. Our recent work discovered that the first sign of patterned cell division in SE appears was an asynchronous S-phase length along the anterior-posterior axis before NTC: the asynchrony of S-phase is offset by the compensatory G2-phase length, thus maintaining the apparent synchrony of cell division. By the loss of compensatory G2 phase, the synchronized cell division harmoniously switches to a patterned cell division at the onset of NTC. Here we review the developmental regulation of rate and pattern of cell division during NTC with emphasis on the switching mechanism identified in our study.