Fate map and morphogenesis of presumptive neural crest and dorsal neural tube

Abstract

In contrast to the classical assumption that neural crest cells are induced in chick as the neural folds elevate, recent data suggest that they are already specified during gastrulation. This prompted us to map the origin of the neural crest and dorsal neural tube in the early avian embryo. Using a combination of focal dye injections and time-lapse imaging, we find that neural crest and dorsal neural tube precursors are present in a broad, crescent-shaped region of the gastrula. Surprisingly, static fate maps together with dynamic confocal imaging reveal that the neural plate border is considerably broader and extends more caudally than expected. Interestingly, we find that the position of the presumptive neural crest broadly correlates with the BMP4 expression domain from gastrula to neurula stages. Some degree of rostrocaudal patterning, albeit incomplete, is already evident in the gastrula. Time-lapse imaging studies show that the neural crest and dorsal neural tube precursors undergo choreographed movements that follow a spatiotemporal progression and include convergence and extension, reorientation, cell intermixing, and motility deep within the embryo. Through these rearrangement and reorganization movements, the neural crest and dorsal neural tube precursors become regionally segregated, coming to occupy predictable rostrocaudal positions along the embryonic axis. This regionalization occurs progressively and appears to be complete in the neurula by stage 7 at levels rostral to Hensen's node.

Signaling pathways and tissue interactions in neural plate border formation

“…4 Comparable fate maps have been drawn for mouse and chicken embryos. 5,6 At early neurula stages, the neural plate has been shaped and the prospective NC cells are located at the lateral borders of the neural plate in the NPB territory.…”

Mechanics of head fold formation: investigating tissue-level forces during early development

“…During neurulation, the NP elongates longitudinally and shortens transversely, a process known as convergent extension Colas and Schoenwolf, 2001;Ezin et al, 2009). This behavior appears intrinsic to the NP itself and has been attributed to both cell intercalation (Schoenwolf and Alvarez, 1989;Ezin et al, 2009) and coordinated cell division (Sausedo et al, 1997).…”

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

“…Then, due to the complex movements of neurulation that involve convergence extension, cell intermixing as well as deep movements, they are gradually displaced toward the midline of the embryo, in a stereotype pattern along the anterio-posterior axis. 23 During this process, nascent NC cells activate a specific transcriptional program, now refered to as a gene regulatory network, 24 elicited by external cues released by the neighboring ectoderm, neural tube and paraxial mesoderm, and mediated by the BMP, Wnt and FGF signaling pathways. 25,26 This program takes place in several consecutive steps throughout late gastrulation and neurulation and starts with the expression of a limited group of genes of the Pax, Msx and Zic families.…”

“…However, so far, this question remains elusive as it is only relatively recently that the fate map of NC cell progenitors has been established for the anterior regions of the embryo. 23, 50 We still do not known with precision how prospective NC cells are generated in more caudal regions, and particularly in regions of secondary neurulation. Likewise, how NC progenitors are driven to the dorsal aspect of the neural tube during formation of the neural keel in the zebrafish has not been described with precision.…”