Neural crest ontogeny during secondary neurulation: a gene expression pattern study in the chick embryo

Abstract

In the prospective lumbo-sacral region of the chick embryo, neurulation is achieved by cavitation of the medullary cord, a process called secondary neurulation. Neural crest cells (NCC) are generated in this region and they give rise to the same types of derivatives as in more rostral parts of the trunk where neurulation occurs by dorsal fusion of the neural plate borders (primary neurulation). However, no molecular data were available concerning the different steps of their ontogeny. We thus performed a detailed expression study of molecular players likely to participate in the generation of secondary NCC in chick embryos between Hamburger and Hamilton stages 18-20 (HH18-20) at the level of somites 30 to 43. We found that specification of secondary NCC involves, as in primary neurulation, the activity of several transcription factors such as Pax3, Pax7, Snail2, FoxD3 and Sox9, which are all expressed in the dorsal secondary neural tube as soon as full cavitation is achieved. Moreover, once specification has occurred, emigration of NCC from the dorsal neuroepithelium starts facing early dissociating somites and involves a series of changes in cell shape and adhesion, as well as interactions with the extracellular matrix. Furthermore, Bmp4 and Wnt1 expression precedes the detection of migratory secondary NCC and is coincident with maturation of adjacent somites. Altogether, this first study of molecular aspects of secondary NCC ontogeny has revealed that the mechanisms of neural crest generation occurring along the trunk region of the chick embryo are generally conserved and independent of the type of neurulation involved. KEY WORDS: epithelium-to-mesenchyme transition, delamination, BMP/WNT signalingNeurulation, the developmental process leading to the formation of the vertebrate neural tube (NT), classically follows two spatially and temporally distinct processes in amniote embryos. In the anterior part of the body, which corresponds to the cephalic and cervico-thoracic regions, neurulation involves bending of the neural plate, a thickened epithelium that rapidly folds up into a groove, giving rise to a tube by dorsal fusion of its lateral borders. This process, called primary neurulation, ends up as early as 15-somite stage (stage 12 of Hamburger and Hamilton (1951) (HH12)) at the prospective level of the 27 th pair of somites, where the posterior neuropore is located in the chick embryo (Schoenwolf, 1979). In contrast, during secondary neurulation, occurring at the level of the presumptive lumbo-sacro-caudal region, formation of the NT occurs by cavitation of a solid rod of cells, the medullary cord (Schoenwolf and Delongo, 1980;Catala et al., 1995). Fate mapping and transplantation experiments have shown that, deInt. J. Dev. Biol. 53: 641-648 (2009) Abbreviations used in this paper: AP, antero-posterior; DSHB, Developmental Study Hybridoma Bank; E, embryonic day; ECM, extracellular matrix; EDS, early dissociating somites; EMT, epithelium-to-mesenchyme transition; HH, Hamburger and Hamilton; NC, ...

Role of noggin as an upstream signal in the lack of neuronal derivatives found in the avian caudal-most neural crest

“…All of these characteristics of NCC generation have been described principally in regions of primary neurulation. We recently showed that the same events occur more caudally in regions belonging to secondary neurulation (Osorio et al, 2009).…”

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

“…Intriguingly, a very similar kinetics of NC cell delamination has been described for the zebrafish trunk or for regions of secondary neurulation in amniotes, even though they differ in their neurulation processes. 53,64 In conclusion, while the cellular events accompanying NC cell formation and delamination are likely to be influenced by the mode of neurulation (i.e., primary vs. secondary), the timing when delamination occurs seems defined by rules independent of neurulation (i.e., cranial vs. truncal/somitic), thus raising the possibility that the regulatory events triggering EMT may be governed by processes independent of the mode of neurulation and conserved among vertebrates.…”

“…At levels posterior to the otic placode, i.e., at somitic levels, including in regions of secondary neurulation, NC cell migration starts well after neural tube closure and ectoderm healing, and this is true for all amphibian and amniote species studied so far. 29,53 The consequence of the different time lags between NC cell delamination and neural tube closure in the head and trunk is that the relative spatial positioning of the NC, ectodermal and neural tube populations, their organizations and mutual interactions, as well as their states of differentiation are different. At cranial levels and particularly in the chick midbrain (Fig.…”

Effects of Alcohol During Secondary Neurulation in Chick Embryos

“…This happens possibly to enable free migration of neural crest cells. Changes in the amount of laminin with time have been shown to affect cell differentiation (11) . Sometimes the lumen has been observed to develop even from a cavity.…”

“…It has been shown that laminin is present in mesenchymalepithelial transition zones throughout HH-18 and 20 stages and that it provides polarization of cells there and contributed to the development of the basement membrane. This environment with these cells produces secondary neurulation (11) . However, exact effect of laminin in this period is yet to be established.…”