EVOLUTION/DEVELOPMENT: ON THE NEURAL CREST - Stem Cell Research in Dentistry

EVOLUTION/DEVELOPMENT: ON THE NEURAL CREST
February 2005
ScienceWeek
The term "neural crest" refers to a band of embryonic ectoderm tissue on both sides of the developing neural tube. It gives rise to dorsal root ganglia, chromaffin cells, Schwann cells, and other specialized cell types. Neural crest cells often attain their final positions after lengthy migration. The neural crest itself has been believed to distinguish vertebrates from protochordates and invertebrates.
The following points are made by Anthony Graham (Current Biology 2004 14:R956):
1) It has long been held that the neural crest is a defining feature of vertebrates. The neural crest arises at the dorsal aspect of the neural tube and then migrates widely in the embryo, giving rise to a range of derivatives which are distinctly vertebrate, such as the neurons and glia of the peripheral nervous system, melanocytes, and, additionally in the head, cartilage, bone and teeth. The other members of the phylum Chordata, the urochordates and the cephalochordates, the nearest living relatives of the vertebrates, have been thought to lack neural crest cells. Indeed, the evolution of the neural crest was believed to have been concomitant with, and pivotal to, the evolution of the vertebrates [1].
2) But recent work [2] has directly challenged these ideas with the demonstration that urochordates possess neural-crest-like cells. Thus it would seem that neural crest cells did not evolve with the vertebrates but that they have a more ancient history. The results also have serious implications for how we view the relationships between the vertebrates, the cephalochordates, and the urochordates, as they suggest that it is the urochordates that are the true sister group of the vertebrates and not, as is generally accepted, the cephalochordates.
3) Given the importance of the neural crest to vertebrates, there have been numerous previous studies looking at how neural crest cells evolved. By and large, these studies focused on a cephalochordate, amphioxus, and on a few urochordate species, primarily Ciona intestinalis. They found that cells at the neural plate border in these species express orthologues of some of the genes known to be involved in specifying dorsal neural tube fates, including neural crest cells, in vertebrates [3-5]. They did not, however, find direct evidence for the existence of migratory neural crest cells. Rather, these studies suggested that the neural crest evolved, with the vertebrates, from dorsal neural tube cells, and that both are linked by a shared developmental program.
4) In their search for neural crest cells in urochordates, Jeffery et al[2] used the colonial ascidian Ecteinascidia turbinata, rather than focus on species such as Ciona. Ciona has small larvae that exhibit the conventional mode of development; the larvae exist as free swimming members of the plankton, and during metamorphosis, the larval head attaches to the substrate, the tail is lost and the tissues of the head are reorganized into a sessile filter feeder. In contrast, Ecteinascidia has a giant larva, and adult development is initiated in the head during the embryonic phase, with the pharynx, heart, siphons and body pigment cells forming precociously.
5) The fact that the Ecteinascidia larva is so large allowed Jeffery et al [2] to look for migratory neural-crest-like cells in this ascidian using a cell-tracing method used to study neural crest cells in vertebrates. They found that if they injected the fluorescent lipophilic dye DiI into the anterior neural tube at the early tailbud stage, they could, with time, observe cells migrating away from the neural primordium towards the developing siphons and body wall. Although the posterior neural tube was not found to release migratory cells at these early stages, injections at later stages did highlight the production of such cells by this region, and again these cells migrated into the body wall. Just as in vertebrates, therefore, migratory cells emerge from the neural tube during Ecteinascidia development and, again like vertebrates, they do so in an anterior to posterior sequence.
References (abridged):
1. Gans, C. and Northcutt, R.G. (1983). Neural crest and the origin of vertebrates: a new head. Science 220, 268-274
2. Jeffery, W.R., Strickler, A.G. and Yamamoto, Y. (2004). Migratory neural crest-like cells form body pigmentation in a urochordate embryo. Nature 431, 696-699
3. Panopoulou, G.D., Clark, M.D., Holland, L.Z., Lehrach, H. and Holland, N.D. (1998). AmphiBMP2/4, an amphioxus bone morphogenetic protein closely related to Drosophila decapentaplegic and vertebrate BMP2 and BMP4: insights into evolution of dorsoventral axis specification. Dev. Dyn. 213, 130-139
4. Miya, T., Morita, K., Suzuki, A., Ueno, N. and Satoh, N. (1997). Functional analysis of an ascidian homologue of vertebrate Bmp-2/Bmp-4 suggests its role in the inhibition of neural fate specification. Development 124, 5149-5159
5. Langeland, J.A., Tomsa, J.M., Jackman, W.R.Jr. and Kimmel, C.B. (1998). An amphioxus snail gene: expression in paraxial mesoderm and neural plate suggests a conserved role in patterning the chordate embryo. Dev. Genes Evol. 208, 569-577
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