The contribution of neural crest cells to the nuchal bone and plastron of the turtle shell

Gilbert, Scott F.; Bender, Günes; Betters, Erin; Yin, Melinda; Cebra‐Thomas, Judith A.

doi:10.1093/icb/icm020

Cited by 47 publications

(43 citation statements)

References 44 publications

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“…However, this property may have been lost during evolution, because avian trunk neural crest progenitors cultured in media that promotes bone differentiation will, in fact, form both bone and cartilage cells, albeit at low frequency (McGonnell and Graham 2002 (Mitsiadis et al 2003). Interestingly, the turtle plastron, whose nine bones have been homologized to the exoskeletal components of the clavicles, interclavicular bone, and gastralia, has recently been shown to be derived from late-migrating trunk NCCs (Cebra- Gilbert et al 2007). The skeletogenic potential of trunk neural crest cells is of considerable evolutionary significance, because early vertebrates, many of which have been identified in the Burgess Shale in Canada, together with fossilized fish had extensive postcranial exoskeletal coverings, and this external armor is likely to have been trunk neural crest-derived.…”

Section: Ectomesenchymal Fate-differences Between Cranial and Trunk Nmentioning

confidence: 99%

Signals and Switches in Mammalian Neural Crest Cell Differentiation

Bhatt

Díaz

Trainor

2013

Cold Spring Harbor Perspectives in Biology

183

155

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SUMMARYNeural crest cells (NCCs) comprise a multipotent, migratory cell population that generates a diverse array of cell and tissue types during vertebrate development. These include cartilage and bone, tendons, and connective tissue, as well as neurons, glia, melanocytes, and endocrine and adipose cells; this remarkable lineage potential persists into adult life. Taken together with a limited capacity for self-renewal, neural crest cells bear the hallmarks of stem and progenitor cells and are considered to be synonymous with vertebrate evolution. The neural crest has provided a system for exploring the mechanisms that govern developmental processes such as morphogenetic induction, cell migration, and fate determination. Today, much of the focus on neural crest cells revolves around their stem cell-like characteristics and potential for use in regenerative medicine. A thorough understanding of the signals and switches that govern mammalian neural crest patterning is central to potential therapeutic application of these cells and better appreciation of the role that neural crest cells play in vertebrate evolution, development, and disease.

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Section: Ectomesenchymal Fate-differences Between Cranial and Trunk Nmentioning

confidence: 99%

Signals and Switches in Mammalian Neural Crest Cell Differentiation

Bhatt

Díaz

Trainor

2013

Cold Spring Harbor Perspectives in Biology

183

155

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“…The turtle scapula is regularly referenced as being uniquely located 'inside' the dorsal ribcage [2,5,6], or at least 'deep' to the ribcage [7 -9]. This topological relationship, however, is confounded by the fact that the scapula is located inside the turtle shell, of which only a portion is formed by the turtle's ribcage, whereas the rest is composed of intramembranously ossified dermis [4].…”

Section: Introductionmentioning

confidence: 99%

Evolution of the turtle bauplan: the topological relationship of the scapula relative to the ribcage

Lyson

Joyce

2012

Biol. Lett.

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The turtle shell and the relationship of the shoulder girdle inside or ‘deep’ to the ribcage have puzzled neontologists and developmental biologists for more than a century. Recent developmental and fossil data indicate that the shoulder girdle indeed lies inside the shell, but anterior to the ribcage. Developmental biologists compare this orientation to that found in the model organisms mice and chickens, whose scapula lies laterally on top of the ribcage. We analyse the topological relationship of the shoulder girdle relative to the ribcage within a broader phylogenetic context and determine that the condition found in turtles is also found in amphibians, monotreme mammals and lepidosaurs. A vertical scapula anterior to the thoracic ribcage is therefore inferred to be the basal amniote condition and indicates that the condition found in therian mammals and archosaurs (which includes both developmental model organisms: chickens and mice) is derived and not appropriate for studying the developmental origin of the turtle shell. Instead, among amniotes, either monotreme mammals or lepidosaurs should be used.

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“…In order to corroborate our data with a method independent of manipulation with its possible artefacts we used NC markers, e.g., HNK-1 and PDGFRα that were used previously in detecting NC cell populations in the developing skeleton of turtles (Cebra- Gilbert et al, 2007). Although these markers are not universal and the work on turtles has questioned their reliability for this purpose (Nagashima, Shibata, et al, 2014), they are quite usual markers employed in the chick model to reveal NC (Rickmann et al, 1985;Bronner-Fraser, 1986).…”

Section: Nc Markers Hnk-1 and Pdgfrα Do Not Express In Shoulder Girdlmentioning

confidence: 71%

Neural crest contribution to the avian shoulder girdle and implications to girdle evolution in vertebrates

Ponomartsev

Valášek

Patel

et al. 2017

BioComm

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Neural crest (NC) is an established source for many endochondral and intramembranous bones in the skull and postcranial skeleton in vertebrates. Neural crest cells also contribute to the trapezius/cleidohyoideus muscle attachment sites on the shoulder girdle of the mouse, where they are found in the scapula, clavicle, and sternum. In the avian shoulder girdle, NC cells from the level of the first two cranial−most somites were only found so far in the clavicle, while in the axolotl, the NC contribution to the shoulder girdle was not found at all. In this study we aimed to determine whether NC cells caudal to the level of the second somite contribute to the cartilaginous shoulder girdle in birds and to analyse the phylogenetic distribution of NC cells in the vertebrate shoulder girdle. Homotopic quail to chick embryos and GFP+ to white chick embryos transplantations of the neural tube including presumptive NC, as well as immunohistochemical detection of NC markers, such as HNK-1 and PDGFRα revealed no contribution of NC cells from somite levels 3−27 to the skeletal elements of the shoulder girdle, including, but not restricting to muscle attachment sites, despite abundance of other NC derivatives. Thus, in birds, NC does not contribute to the formation of the cartilaginous shoulder girdle. The negative result is discussed in a broad evolutionary aspect. It supports the notion of the uniqueness of NC contribution to the variety of endochondral bones in mice (or mammals). In other vertebrates, including birds, only the cells of the cranial NC seem to migrate to the shoulder girdle and contribute to the intramembranous clavicles and/or interclavicle. We critically evaluate the existing hypotheses on evolution of NC contribution to the shoulder girdle in vertebrates.

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The contribution of neural crest cells to the nuchal bone and plastron of the turtle shell

Cited by 47 publications

References 44 publications

Signals and Switches in Mammalian Neural Crest Cell Differentiation

Signals and Switches in Mammalian Neural Crest Cell Differentiation

Evolution of the turtle bauplan: the topological relationship of the scapula relative to the ribcage

Neural crest contribution to the avian shoulder girdle and implications to girdle evolution in vertebrates

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