Strategies of vertebrate neurulation and a re-evaluation of teleost neural tube formation

Abstract

The vertebrate neural tube develops by two distinct mechanisms. Anteriorly, in the brain and future trunk (cervicothoracic) region, 'primary neurulation' occurs, where an epithelial sheet rolls or bends into a tube. Posteriorly, in the future lumbar and tail region, the neural tube forms by 'secondary neurulation', where a mesenchymal cell population condenses to form a solid rod that undergoes transformation to an epithelial tube. Teleost neurulation has been described as different from that of other vertebrates. This is principally because the teleost trunk neural tube initially forms a solid rod (the neural keel) that later develops a lumen. This process has also been termed secondary neurulation. However, this description is not accurate since the teleost neural tube derives from an epithelial sheet that folds. This best fits the description of primary neurulation. It has also been suggested that teleost neurulation is primitive, however, both primary and secondary neurulation are found in groups with a more ancient origin than the teleosts. The similarity between neurulation in teleosts and other vertebrates indicates that this group includes viable models (such as the zebrafish) for understanding human neural tube development.

Early lens development in the zebrafish: A three‐dimensional time‐lapse analysis

“…Within zebrafish organogenesis, the lack of a vesicle stage is not unique. The neural "tube," optic "vesicle," and otic "vesicle" form as solid masses of cells and later undergo cavitation to develop lumina (Schmitt and Dowling, 1994;Haddon and Lewis, 1996;Lowery and Sive, 2004). Even earlier in embryogenesis, the zebrafish blastocyst lacks a blastocoele and the gastrula lacks an archenteron (Kimmel et al, 1995).…”

Timing and kinetics of E‐ to N‐cadherin switch during neurulation in the avian embryo

“…In the chick, the neural tube is formed by two independent mechanisms involving different morphogenetitc movements and termed primary and secondary neurulations (Colas and Schoenwolf, 2001;Lowery and Sive, 2004). Primary neurulation occurs in the head and upper trunk by rolling of the neural plate and formation of neural folds that then fuse dorsally, resulting in the typical hollow shape of the neural tube.…”

Diversity in the molecular and cellular strategies of epithelium-to-mesenchyme transitions: Insights from the neural crest

“…3A). [38][39][40][41] The neural tube forms by bending of the neural plate along the midline, resulting in a groove. Then, owing to forces exerted medially by the ectoderm, the lateral margins of the plate elevate into neural folds which later come in apposition in the midline and fuse.…”

“…3C). 40,45 The neural plate starts out as a multilayered tissue, composed of deep and superficial cells. Deep cells have a columnar, epithelial-like morphology and are anchored to a basement membrane whereas superficial cells are more cuboidal in shape.…”