Evolution and developmental diversity of tooth regeneration

Tucker, Abigail S.; Fraser, Gareth J.

doi:10.1016/j.semcdb.2013.12.013

Cited by 93 publications

(124 citation statements)

References 67 publications

(141 reference statements)

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“…Sox2 (Sex-determining region Y-box 2) is a transcription factor known for its role in maintaining cell pluripotency and stem cell renewal (23). It is expressed in epithelial dental progenitors in the dental lamina of all polyphyodont vertebrates (2,4,16,17) and is thought to regulate dental progenitor cell state (16). Therefore we investigated its expression during pufferfish tooth formation to determine the location of epithelial dental progenitors in pufferfishes.…”

Section: Source Of Epithelial Dental Progenitors In Intraosseous Puffmentioning

confidence: 99%

“…Our understanding of tooth development is based largely on study of the mouse, which continuously renews its incisors but is unable to produce new tooth generations (monophyodonty) (4). In contrast, most vertebrates exhibit lifelong dental replacement (polyphyodonty) (5).…”

mentioning

confidence: 99%

“…Teleosts are exceptionally diverse, as reflected in the morphological variation in their dentitions (4). The extremes of dental diversity are exemplified within the teleost order Tetraodontiformes (10)(11)(12)(13).…”

mentioning

confidence: 99%

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Spatially restricted dental regeneration drives pufferfish beak development

Thiery

Shono

Kurokawa

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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Vertebrate dentitions are extraordinarily diverse in both morphology and regenerative capacity. The teleost order Tetraodontiformes exhibits an exceptional array of novel dental morphologies, epitomized by constrained beak-like dentitions in several families, i.e., porcupinefishes, three-toothed pufferfishes, ocean sunfishes, and pufferfishes. Modification of tooth replacement within these groups leads to the progressive accumulation of tooth generations, underlying the structure of their beaks. We focus on the dentition of the pufferfish (Tetraodontidae) because of its distinct dental morphology. This complex dentition develops as a result of (i) a reduction in the number of tooth positions from seven to one per quadrant during the transition from first to second tooth generations and (ii) a dramatic shift in tooth morphogenesis following the development of the firstgeneration teeth, leading to the elongation of dental units along the jaw. Gene expression and 1,1′-Dioctadecyl-3,3,3′,3′-tetramethylindocarbocyanine perchlorate (DiI) lineage tracing reveal a putative dental epithelial progenitor niche, suggesting a highly conserved mechanism for tooth regeneration despite the development of a unique dentition. MicroCT analysis reveals restricted labial openings in the beak, through which the dental epithelium (lamina) invades the cavity of the highly mineralized beak. Reduction in the number of replacement tooth positions coincides with the development of only four labial openings in the pufferfish beak, restricting connection of the oral epithelium to the dental cavity. Our data suggest the spatial restriction of dental regeneration, coupled with the unique extension of the replacement dental units throughout the jaw, are primary contributors to the evolution and development of this unique beak-like dentition.tooth development | diversity | dental regeneration | stem cells | novelty

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Section: Source Of Epithelial Dental Progenitors In Intraosseous Puffmentioning

confidence: 99%

mentioning

confidence: 99%

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Spatially restricted dental regeneration drives pufferfish beak development

Thiery

Shono

Kurokawa

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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“…In both cases, replacement teeth can be present on the tooth plate before the previous tooth is shed and can contribute to the functional dentition. Recently, Tucker and Fraser (2014) proposed that dental diversity could arise in a system of continuous tooth replacement by shifting the replacement program to produce an adaptive advantage. Supporting that proposal, here we find that the rate of new tooth formation is significantly higher in both freshwater populations than in their marine counterpart, resulting in increased tooth number late in development.…”

Section: Unique Genetic Basis Of Evolved Tooth Gainmentioning

confidence: 99%

“…However, since mice are monophyodont rodents that do not replace their teeth, other vertebrate models are needed to study the developmental basis of tooth replacement. The ancestral vertebrate dental phenotype is polyphyodonty, or continuous tooth replacement, a trait retained in sharks, fish and reptiles (Jernvall and Thesleff, 2012;Tucker and Fraser, 2014). These replacement teeth may appear adjacent or beneath primary teeth and are often retained in the tooth field before the primary tooth is shed.…”

Section: Introductionmentioning

confidence: 99%

Distinct developmental and genetic mechanisms underlie convergently evolved tooth gain in sticklebacks

et al. 2015

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Teeth are a classic model system of organogenesis, as repeated and reciprocal epithelial and mesenchymal interactions pattern placode formation and outgrowth. Less is known about the developmental and genetic bases of tooth formation and replacement in polyphyodonts, which are vertebrates with continual tooth replacement. Here, we leverage natural variation in the threespine stickleback fish Gasterosteus aculeatus to investigate the genetic basis of tooth development and replacement. We find that two derived freshwater stickleback populations have both convergently evolved more ventral pharyngeal teeth through heritable genetic changes. In both populations, evolved tooth gain manifests late in development. Using pulse-chase vital dye labeling to mark newly forming teeth in adult fish, we find that both high-toothed freshwater populations have accelerated tooth replacement rates relative to lowtoothed ancestral marine fish. Despite the similar evolved phenotype of more teeth and an accelerated adult replacement rate, the timing of tooth number divergence and the spatial patterns of newly formed adult teeth are different in the two populations, suggesting distinct developmental mechanisms. Using genome-wide linkage mapping in marine-freshwater F2 genetic crosses, we find that the genetic basis of evolved tooth gain in the two freshwater populations is largely distinct. Together, our results support a model whereby increased tooth number and an accelerated tooth replacement rate have evolved convergently in two independently derived freshwater stickleback populations using largely distinct developmental and genetic mechanisms.

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On the Materials Science of Nature's Arms Race

2018

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Biological material systems have evolved unique combinations of mechanical properties to fulfill their specific function through a series of ingenious designs. Seeking lessons from Nature by replicating the underlying principles of such biological materials offers new promise for creating unique combinations of properties in man-made systems. One case in point is Nature's means of attack and defense. During the long-term evolutionary "arms race," naturally evolved weapons have achieved exceptional mechanical efficiency with a synergy of effective offense and persistence-two characteristics that often tend to be mutually exclusive in many synthetic systems-which may present a notable source of new materials science knowledge and inspiration. This review categorizes Nature's weapons into ten distinct groups, and discusses the unique structural and mechanical designs of each group by taking representative systems as examples. The approach described is to extract the common principles underlying such designs that could be translated into man-made materials. Further, recent advances in replicating the design principles of natural weapons at differing lengthscales in artificial materials, devices and tools to tackle practical problems are revisited, and the challenges associated with biological and bioinspired materials research in terms of both processing and properties are discussed.

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Evolution and developmental diversity of tooth regeneration

Cited by 93 publications

References 67 publications

Spatially restricted dental regeneration drives pufferfish beak development

Spatially restricted dental regeneration drives pufferfish beak development

Distinct developmental and genetic mechanisms underlie convergently evolved tooth gain in sticklebacks

On the Materials Science of Nature's Arms Race

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