Secondary neurulation: Fate‐mapping and gene manipulation of the neural tube in tail bud

Abstract

The body tail is a characteristic trait of vertebrates, which endows the animals with a variety of locomotive functions. During embryogenesis, the tail develops from the tail bud, where neural and mesodermal tissues make a major contribution. The neural tube in the tail bud develops by the process known as secondary neurulation (SN), where mesenchymal cells undergo epithelialization and tubulogenesis. These processes contrast with the well known primary neurulation, which is achieved by invagination of an epithelial cell sheet. In this study we have identified the origin of SN-undergoing cells, which is located caudo-medially to Hensen's node of early chicken embryo. This region is distinctly fate-mapped from tail-forming mesoderm. The identification of the presumptive SN region has allowed us to target this region with exogenous genes using in ovo electroporation techniques. The SN-transgenesis has further enabled an exploration of molecular mechanisms underlying mesenchymal-to-epithelial transition during SN, where activity levels of Cdc42 and Rac1 are critical. This is the first demonstration of molecular and cellular analyses of SN, which can be performed at a high resolution separately from tail-forming mesoderm.

Secondary neurulation-fated cells in the tail bud undergo self-renewal and tubulogenesis regulated by a Sox2 gradient

“…The tail bud has long been appreciated to be critical for the posterior body 27 elongation, and the existence of precursors has been shown that give rise to the In this study, we have extended our previous findings that the SN precursors 4 can directly be traced in the tail bud (Shimokita and Takahashi, 2011). These SN 5 precursors derive from the preSN region in the epiblast at HH8, which is located in 6 between Hensen's node and the anterior end of the primitive streak (Fig.…”

“…We previously used direct cell labeling in the embryonic chicken tail bud 33 (Shimokita & Takahashi, 2011) to show that SN-precursors are derived from a specific 1 region of the epiblast, called the presumptive SN (preSN). This preSN is located along 2 the midline posterior to the Hensen's node at Hamburger and Hamilton stage 8 (HH 8; 3 Fig.…”

“…EGFP-electroporation revealed that the preSN-derived ingressed cells constitute the tail 10 bud where they remain mesenchymal until they are incorporated into the secondary 11 neural tube (Shimokita & Takahashi, 2011). Little or no mesodermal cells are derived 12 from the preSN region.…”

New classification of spinal lipomas based on embryonic stage

“…Instead, secondary neurulation is the process in which mesenchymal cells undergo epithelialization and tubulogenesis. 25 As a prelude to this, pluripotent tissues of the caudal eminence (tail bud), consisting of neural and mesodermal tissues, appear distal to the caudal neuropore at POD 20-22. The caudal eminence gives rise to the caudal portion of the digestive tube, blood vessels, and the future somites of the S1-2 vertebral level and below-and eventually the spinal cord.…”

Cell segregation, mixing, and tissue pattern in the spinal cord of the Xenopus laevis neurula

“…The anterior neural plate in most amniotes is single‐layered, but posterior to the hindlimb, the neural tube is formed from a mesenchymal mass of cells by means of secondary neurulation (Schoenwolf and Delongo, ; Schoenwolf, ). The chick posterior neural tube arises from a multilayered mesenchymal medullary cord (Shimokita and Takahashi, ), and neurulation in zebrafish, at all levels, bears some similarity to the process of secondary neurulation, beginning from a mesenchymal neural keel rather than epithelial sheet (Lowery, ).…”