Hallmarks of primary neurulation are conserved in the zebrafish forebrain

Abstract

Primary neurulation is the process by which the neural tube, the central nervous system precursor, is formed from the neural plate. Incomplete neural tube closure occurs frequently, yet underlying causes remain poorly understood. Developmental studies in amniotes and amphibians have identified hingepoint and neural fold formation as key morphogenetic events and hallmarks of primary neurulation, the disruption of which causes neural tube defects. In contrast, the mode of neurulation in teleosts has remained highly debated. Teleosts are thought to have evolved a unique mode of neurulation, whereby the neural plate infolds in absence of hingepoints and neural folds, at least in the hindbrain/trunk where it has been studied. Using high-resolution imaging and time-lapse microscopy, we show here the presence of these morphological landmarks in the zebrafish anterior neural plate. These results reveal similarities between neurulation in teleosts and other vertebrates and hence the suitability of zebrafish to understand human neurulation.

A quantitative characterization of early neuron generation in the developing zebrafish telencephalon

“…1). As described previously (Affaticati et al, 2015;Werner et al, 2021), the anterior neural tube transitioned from an initially disorganized and unpolarized epithelium into a pseudostratified polarized neural tubelike structure (Fig. 1A) with formation of optic vesicles between 14 and 18 hpf.…”

“…Based on the cell cycle length reported for zebrafish segmentation stages of ± 4 hours (Kimmel et al, 1994), we assume that during the two-hour interval a single NPC would not divide more than once. Therefore, the increase in total cells probably reflects the addition of new NPCs through the extensive neurulation cell movements that are still taking place prior to 16 hpf (Ivanovitch et al, 2013;Werner et al, 2021).…”

Neurulation in the posterior region of zebrafish, Danio rerio embryos

“…However, during the NT formation in the forebrain the hinge points and neural folds are present in the epithelialized anterior neural plate. The formation of the medial hinge point involves oscillatory apical contractions that progressively reduce the apical surface (Werner et al, 2021). The formation of dorsal lateral hinge points (DLHP) during the development of midbrain also requires actomyosin function.…”

Ubiquitin ligases: guardians of mammalian development

“…During gastrulation, an originally relatively simple and unorganized sphere of cells reorganizes into a polarized embryo with discrete ectodermal, mesodermal, and endodermal germ layers 100 (Figure 2). During neurulation, a flat sheet of ectoderm morphs into the rudiment of the mature adult nervous system, the neural tube (Figures 2, 3, 4, 5) 101 . This complex reorganization requires major cell/tissue movements alongside the coordinated differentiation of germ layer and neural precursors -processes tightly regulated by E3 ligases.…”