An epithelial signalling centre in sharks supports homology of tooth morphogenesis in vertebrates.
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ABSTRACT:
SUBMITTER: Thiery AP
PROVIDER: S-EPMC9249395 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:Double tooth pathologies are important indicators of trauma, disease, diet, and feeding biomechanics, and are widely documented in mammals. However, diagnosis of double tooth pathologies in extinct non-mammalian vertebrates is complicated by several compounding factors including: a lack of shared terminology reflecting shared etiology, inconsistencies in definitions and key features within and outside of mammals (e.g., gemination, fusion, twinning, concrescence); differences in tooth morphology, heterodonty, regeneration, and implantation between mammals and non-mammalian vertebrates; and the unmet need for diagnostic criteria that can be applied to isolated teeth, which are common in the fossil record. Here we report on double tooth pathologies in the lamniform and carcharhiniform Cenozoic sharks Otodus megalodon (NCSM 33639) and Carcharhinus leucas (NCSM 33640, 33641). All three teeth bear a singular bifid crown with mirrored halves and abnormal internal microstructure-a single, bifurcating pulp cavity in C. leucas and a more than tripling of vessels in O. megalodon (from two to seven main ascending canals). We identify these abnormalities as likely examples of gemination due to their symmetry, which rules out fusion of tooth buds in one tooth file in different developmental stages in polyphyodont taxa; however, we note that incomplete forms of mesiodistal tooth fusion can be morphologically indistinguishable from gemination, and thus fusion cannot be rejected. We further compile and recategorize, when possible, the diversity of tooth pathologies in sharks. The identification of double tooth pathologies in O. megalodon and C. leucas has paleobiological implications. Such pathologies in sharks are largely hypothesized to stem from trauma to developing tooth buds. Carcharhinus leucas is known to feed on prey documented to cause feeding-related oral traumas (e.g., rays, sawfish, spiny fish, and sea urchins). However, O. megalodon, is considered to have largely fed on marine mammals, and perhaps turtles and/or fish, raising the possibility that the dietary diversity of this species is, as of yet, underappreciated. The genetic underpinnings of tooth morphogenesis and regeneration is highly conserved throughout vertebrate evolution, suggesting a homologous framework can be established. However, more research is needed to link developmental, paleobiological, and/or paleoenvironmental factors to gemination/fusion in polyphyodont taxa. We argue that the definitions and diagnostic criteria for dental pathologies in vertebrates require standardization in order to advance macroevolutionary studies of feeding trauma in deep time.
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Project description:During organogenesis, cell fate specification and patterning are regulated by signaling centers, specialized clusters of morphogen-expressing cells. In many organs, initiation of development is marked by bud formation, but the cellular mechanisms involved are ill defined. Here, we use the mouse incisor tooth as a model to study budding morphogenesis. We show that a group of nonproliferative epithelial cells emerges in the early tooth primordium and identify these cells as a signaling center. Confocal live imaging of tissue explants revealed that although these cells reorganize dynamically, they do not reenter the cell cycle or contribute to the growing tooth bud. Instead, budding is driven by proliferation of the neighboring cells. We demonstrate that the activity of the ectodysplasin/Edar/nuclear factor κB pathway is restricted to the signaling center, and its inactivation leads to fewer quiescent cells and a smaller bud. These data functionally link the signaling center size to organ size and imply that the early signaling center is a prerequisite for budding morphogenesis.
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Project description:The proper positioning of organs during development is essential, yet little is known about the regulation of this process in mammals. Using murine tooth development as a model, we have found that cell migration plays a central role in positioning of the organ primordium. By combining lineage tracing, genetic cell ablation, and confocal live imaging, we identified a migratory population of Fgf8-expressing epithelial cells in the embryonic mandible. These Fgf8-expressing progenitors furnish the epithelial cells required for tooth development, and the progenitor population migrates toward a Shh-expressing region in the mandible, where the tooth placode will initiate. Inhibition of Fgf and Shh signaling disrupted the oriented migration of cells, leading to a failure of tooth development. These results demonstrate the importance of intraepithelial cell migration in proper positioning of an initiating organ.
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Project description:Embryonic signalling centres are specialized clusters of non-proliferating cells that direct the development of many organs. However, the mechanisms that establish these essential structures in mammals are not well understood. Here we report, using the murine incisor as a model, that αE-catenin is essential for inhibiting nuclear YAP localization and cell proliferation. This function of αE-catenin is required for formation of the tooth signalling centre, the enamel knot (EK), which maintains dental mesenchymal condensation and epithelial invagination. EK formation depends primarily on the signalling function of αE-catenin through YAP and its homologue TAZ, as opposed to its adhesive function, and combined deletion of Yap and Taz rescues the EK defects caused by loss of αE-catenin. These findings point to a developmental mechanism by which αE-catenin restricts YAP/TAZ activity to establish a group of non-dividing and specialized cells that constitute a signalling centre.
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Project description:The dentition of elasmobranchs (sharks, skates and rays) is uniquely productive, capable of both rapid and continuous, lifelong regeneration. Elasmobranchs represent an important group of vertebrates with a deep evolutionary history, possessing several ancient and basal characters, i.e., the continuously regenerative dentition from a specialized dental lamina. The dental lamina is an expanded component of the oral epithelia that is responsible for initiating and producing new teeth among all toothed-vertebrates. In sharks, this dynamic epithelial unit is permanent and continuous – meaning it extends to cover the entirety of each jaw (jaw-wide) and develops early during embryogenesis and retained to produce teeth for the life of the shark. It is rare for a truly embryonic vertebrate tissue to be retained for its original function for the life of the organism. The dental lamina in sharks is unique and houses teeth in a developmental series from the deepest part, where teeth are initiated, through stages of tooth development in the form of a related, family of teeth to eruption and functionality of the advanced teeth at the jaw margin. How teeth are made and regenerated is an important question in vertebrate biology; here we investigated this question in the small spotted catshark (Scyliorhinus canicula), a new model in the field of developmental biology. Specifically, we divided the shark dental lamina into stage-compartments as follows: (i) the initiation site – the successional lamina (SL); (ii) the early developing teeth (ET); (iii) the late stage developing teeth (LT); (iv) the tooth-taste junction between the superficial oral and dental epithelium at the jaw margin that separates the taste territory and the dental lamina proper (TTJ); and basi-hyal oral epithelium that is strictly non-dental and only contains taste buds (BHTB). These 5 compartments each house both a shared and unique signature of gene transcripts. This study aims to understand the transcriptomic basis of continuous tooth regeneration in the shark. In this study we combine X-ray computed tomography, classic histology, insitu hybridization, immunohistochemistry, and functional assays of novel markers, and de novo and genome guided transcriptome assemblies for each of these 5 dental lamina compartments of the hatchling (stage 34) catshark (S. canicula).
2022-07-01 | GSE198580 | GEO
Project description:The Notch signalling pathway is an evolutionarily conserved intercellular signalling mechanism that is essential for cell fate specification and proper embryonic development. We have analysed the expression, regulation and function of the jagged 2 (Jag2) gene, which encodes a ligand for the Notch family of receptors, in developing mouse teeth. Jag2 is expressed in epithelial cells that give rise to the enamel-producing ameloblasts from the earliest stages of tooth development. Tissue recombination experiments showed that its expression in epithelium is regulated by mesenchyme-derived signals. In dental explants cultured in vitro, the local application of fibroblast growth factors upregulated Jag2 expression, whereas bone morphogenetic proteins provoked the opposite effect. Mice homozygous for a deletion in the Notch-interaction domain of Jag2 presented a variety of severe dental abnormalities. In molars, the crown morphology was misshapen, with additional cusps being formed. This was due to alterations in the enamel knot, an epithelial signalling structure involved in molar crown morphogenesis, in which Bmp4 expression and apoptosis were altered. In incisors, cytodifferentiation and enamel matrix deposition were inhibited. The expression of Tbx1 in ameloblast progenitors, which is a hallmark for ameloblast differentiation and enamel formation, was dramatically reduced in Jag2(-/-) teeth. Together, these results demonstrate that Notch signalling mediated by Jag2 is indispensable for normal tooth development.
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