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ScienceWeek
EVOLUTION/DEVELOPMENT: ON THE NEURAL CREST
Notes by 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
Current Biology http://www.current-biology.com
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Related Material:
DEVELOPMENTAL BIOLOGY: ON NEURAL CREST CELLS
The following points are made by M. Bronner-Fraser (Science 2004 303:966):
1) Neural crest cells, a uniquely vertebrate cell type, are characterized by their ability to migrate throughout the developing embryo and to form many diverse tissues. These cells arise within the developing central nervous system and subsequently migrate away, sometimes moving extremely long distances to populate peripheral regions of the embryo. Neural crest cells are multipotent progenitors that give rise to an impressive array of cell types, including neurons and glia of the peripheral nervous system, cartilage and bones of the face, and melanocytes (pigment cells) (1).
2) Perhaps the best studied neural crest derivatives are the peripheral ganglia, which comprise neurons and support cells that form as aggregates outside the brain and spinal cord. These contain neurons of many different types, including sensory neurons (which relay touch and pain information to the brain) and autonomic neurons (which innervate various organs and modulate their activity).
3) The fact that neural crest cells give rise to so many different progeny has raised the fascinating question of whether they are "stem cells". A stem cell divides to form one multipotent daughter cell like itself and another that is biased toward a particular cell fate. In support of the idea that neural crest cells have stem cell properties, individual neural crest cells form multiple derivative tissues both in vivo (3) and in vitro (4). Furthermore, they have some ability to self-renew, consistent with the principal characteristic of a true stem cell.
4) How is a neural crest progenitor cell driven to adopt one of its many possible fates? A variety of growth factors can bias neural crest cells grown at clonal density (~ single cell density) toward certain lineages. For example, bone morphogenetic protein (BMP) causes cloned neural crest cells to form autonomic neurons; glia growth factor (GGF, also called neuregulin) drives them to become glia or Schwann cells (5); and endothelin as well as Wnts can bias them to become melanocytes. However, the factors responsible for driving neural crest cells to become sensory neurons have remained elusive. Lee et al (2) have shed light on the mechanism through which sensory neurons are generated from multipotent neural crest progenitor cells.
References (abridged):
1. N. Le Douarin, C. Kalcheim, The Neural Crest (Cambridge Univ. Press, Cambridge, ed. 2, 1999)
2. H.-Y. Lee et al., Science 303, 1020 (2004); published online 8 January 2004 (10.1126/science.1091611)
3. M. Bronner-Fraser, S. E. Fraser, Nature 335, 161 (1988)
4. D. Anderson, Trends Genet. 13, 276 (1997)
5. N. M. Shah, D. J. Anderson, Proc. Natl. Acad. Sci. U.S.A. 94, 11369 (1997)
Science http://www.sciencemag.org
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EVOLUTIONARY BIOLOGY: ON PIGMENT PATTERNS
The following points are made by David M. Parichy (Current Biology 2003 13:R947):
1) Animal pigment patterns are one of the most obvious traits of animals and serve a variety of functions. Some provide camouflage (zebra stripes) or warnings (the colors of poison arrow frogs). Other patterns have roles in social aggregation and mate choice (guppies), and have important roles in adaptive radiations and speciation (African cichlid fishes).
2) Given their prominence and ecological functions, pigment patterns often are targets of natural selection and thus of particular interest to evolutionary biologists. They have been of long-standing interest to developmental and cell biologists as well: their accessibility to observation and manipulation has made them a classic and enduring system for studying basic genetic and cellular mechanisms.
3) Recent years have seen the emergence of pigment patterns specifically as a model for post-embryonic development. Discovering why adult organisms look the way they do is critical to understanding the evolution of morphology. Despite great strides in understanding embryogenesis, however, we still know little about the generation of adult form. In this regard, pigment patterns are an especially tractable system for identifying mechanisms of pattern formation and morphogenesis that make an adult. They also offer the prospect of truly integrative research spanning several levels of biological organization, from molecules to cells and phenotypes, and from individuals to populations and species. One prime model organism for dissecting mechanisms of pigment pattern formation and evolution is the zebrafish, Danio rerio.
4) Vertebrates exhibit a stunning array of pigment patterns, which are highly varied especially in teleost fishes. The Danio genus captures some of this diversity among its many species. The patterns in danios and other vertebrates depend on pigment cells, which have their origin in the neural crest, a transient population of cells that arises during neurulation along the dorsal neural tube. Neural crest cells then disperse throughout the embryo in one of the most dramatic examples of cell migration known. Besides pigment cells, neural crest cells also contribute to a diverse array of other cell types and organ systems. Indeed, many of the shared, derived traits of vertebrates have their origin at least in part within the neural crest. Thus, an understanding of how these remarkable cells are patterned -- and how these patterning mechanisms evolve -- should provide considerable insight into the evolution of vertebrate form.
5) The adult stripes of zebrafish result from three classes of pigment cells, or chromatophores: black melanophores (containing melanin); yellow or orange xanthophores (containing pteridines and carotenoids); and silvery iridophores (containing guanine-rich reflecting platelets). Dark stripes include melanophores and iridophores, with only a few xanthophores, whereas light stripes include xanthophores and iridophores, with few if any melanophores. The diversity of ectotherm chromatophores differs from amniotes, which exhibit just a single type of skin pigment cell: the melanocyte. However, molecular analyses are revealing a conservation between teleosts and mammals for many aspects of pigment cell development, e.g. a microphthalmia-associated transcription factor (mitf) is essential for specifying both melanocytes in mouse and melanophores in zebrafish.(1-5)
References (abridged):
1. R. Asai, E. Taguchi, Y. Kume, M. Saito and S. Kondo, Zebrafish Leopard gene as a component of the putative reaction-diffusion system. Mech. Dev. 89 (1999), pp. 87-92
2. F. Maderspacher and C. N sslein-Volhard, Formation of the adult pigment pattern in zebrafish requires leopard and obelix dependent cell interactions. Development 130 (2003), pp. 3447-3457.
3. D.M. Parichy and J.M. Turner, Temporal and cellular requirements for Fms signaling during zebrafish adult pigment pattern development. Development 130 (2003), pp. 817-833
4. D.M. Parichy and J.M. Turner, Zebrafish puma mutant decouples pigment pattern and somatic metamorphosis. Dev. Biol. 256 (2003), pp. 242-257
5. I.K. Quigley and D.M. Parichy, Pigment pattern formation in zebrafish: a model for developmental genetics and the evolution of form. Microsc. Res. Tech. 58 (2002), pp. 442-455
Current Biology http://www.current-biology.com
ScienceWeek http://scienceweek.com
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