Sox2+ Stem Cells Contribute to All Epithelial Lineages of the Tooth via Sfrp5+ Progenitors

Juuri, Emma; Saito, Kan; Ahtiainen, Laura; Seidel, Kerstin; Tümmers, Mark; Hochedlinger, Konrad; Klein, Ophir D.; Thesleff, Irma; Michon, Frédéric

doi:10.1016/j.devcel.2012.05.012

Cited by 215 publications

(326 citation statements)

References 54 publications

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“…Sharks, like other polyphyodont vertebrates, must use multipotent odontogenic stem cells to enable the lifelong successional regeneration of teeth (17)(18)(19)(20)(21)(22). Previous studies demonstrated the role of Sox2 in regulating adult epithelial stem cells, including those required for both tooth ameloblast and taste-bud regeneration in mouse (23)(24)(25)(26). Polyphyodont osteichthyans (17,20,21,26) also express sox2 in the developing DL during tooth regeneration within putative epithelial stem cell populations.…”

Section: Successional Regeneration Is a Property Unique To Teeth Amongmentioning

confidence: 99%

Sox2+ progenitors in sharks link taste development with the evolution of regenerative teeth from denticles

Martin

Rasch

Cooper

et al. 2016

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

146

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Teeth and denticles belong to a specialized class of mineralizing epithelial appendages called odontodes. Although homology of oral teeth in jawed vertebrates is well supported, the evolutionary origin of teeth and their relationship with other odontode types is less clear. We compared the cellular and molecular mechanisms directing development of teeth and skin denticles in sharks, where both odontode types are retained. We show that teeth and denticles are deeply homologous developmental modules with equivalent underlying odontode gene regulatory networks (GRNs). Notably, the expression of the epithelial progenitor and stem cell marker sex-determining region Y-related box 2 (sox2) was tooth-specific and this correlates with notable differences in odontode regenerative ability. Whereas shark teeth retain the ancestral gnathostome character of continuous successional regeneration, new denticles arise only asynchronously with growth or after wounding. Sox2+ putative stem cells associated with the shark dental lamina (DL) emerge from a field of epithelial progenitors shared with anteriormost taste buds, before establishing within slow-cycling cell niches at the (i) superficial taste/tooth junction (T/TJ), and (ii) deep successional lamina (SL) where tooth regeneration initiates. Furthermore, during regeneration, cells from the superficial T/TJ migrate into the SL and contribute to new teeth, demonstrating persistent contribution of taste-associated progenitors to tooth regeneration in vivo. This data suggests a trajectory for tooth evolution involving cooption of the odontode GRN from nonregenerating denticles by sox2+ progenitors native to the oral taste epithelium, facilitating the evolution of a novel regenerative module of odontodes in the mouth of early jawed vertebrates: the teeth.regeneration | stem cells | odontogenesis | chondrichthyes | evolutionary novelty

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Section: Successional Regeneration Is a Property Unique To Teeth Amongmentioning

confidence: 99%

Sox2+ progenitors in sharks link taste development with the evolution of regenerative teeth from denticles

Martin

Rasch

Cooper

et al. 2016

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

146

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“…co-inducer of iPS (induced pluripotent stem cells) cells [71]. In the mouse incisor Sox2 is localised to the labial cervical loop, a known site for epithelial stem cells for the continuously growing incisor [4]. In regenerating dentitions, Sox2 expression has been proposed to mark epithelial competence to generate teeth in both mammals and reptiles [14].…”

Section: The Conserved Genetic Basis For Tooth Replacementmentioning

confidence: 99%

“…Many genes expressed during the process of tooth replacement are highly conserved from the emergence of the first generation and appear to be essential for epithelial maintenance necessary for the cyclical regeneration of the dental system. Recent dental research has identified novel markers of tooth replacement and renewal that appear to be regulators of other regenerative systems such as hair, feather and wound healing [4,12,14,46,68]. In this age of stem cell and regenerative biological research many studies are based on the knowledge of adult stem cell populations following the principle that many of the same genes are involved in maintenance and regulation of stem cells.…”

Section: The Conserved Genetic Basis For Tooth Replacementmentioning

confidence: 99%

“…Regulation of Wnt signalling therefore appears important in mammals and reptiles. Sox2 is also linked to the successional development of molars in the mouse, with Sox2+ve cells of the 1st molar contributing to the 2nd and 3rd molars [4,14], linking the genetic regulation of dental replacement and serial addition. A number of stem cells markers (Dkk3, Lgfbp5, Lgr5) have been identified in the gecko dental lamina [12], supporting the dental lamina as a source of stem cells for dental regeneration.…”

Section: The Conserved Genetic Basis For Tooth Replacementmentioning

confidence: 99%

“…The mouse, the main mammalian model for development, does not have the capacity to replace its dentition de novo. Instead of replacing whole teeth the mouse counteracts the problems of tooth wear by having continuously growing incisors, with a continuous production of enamel and dentine tissue secreting cells -a tooth renewal system [1][2][3][4]. The mouse is therefore insufficient to understand how mammals replace teeth.…”

Section: Introductionmentioning

confidence: 99%

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Evolution and developmental diversity of tooth regeneration

Tucker

Fraser

2014

Seminars in Cell & Developmental Biology

123

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a b s t r a c tThis review considers the diversity observed during both the development and evolution of tooth replacement throughout the vertebrates in a phylogenetic framework from basal extant chondrichthyan fish and more derived teleost fish to mammals. We illustrate the conservation of the tooth regeneration process among vertebrate clades, where tooth regeneration refers to multiple tooth successors formed de novo for each tooth position in the jaws from a common set of retained dental progenitor cells. We discuss the conserved genetic mechanisms that might be modified to promote morphological diversity in replacement dentitions. We review current research and recent progress in this field during the last decade that have promoted our understanding of tooth diversity in an evolutionary developmental context, and show how tooth replacement and dental regeneration have impacted the evolution of the tooth-jaw module in vertebrates.

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Tooth Induction

Balic

2017

Encyclopedia of Life Sciences

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Tooth development is a sequential process governed by reciprocal interactions between ectoderm and neural crest‐derived mesenchyme. Initially, the inductive signal resides in the epithelium, but during subsequent developmental stages, it shifts to the mesenchyme. The complex signalling and cellular cross‐talk generate differentiated cell lineages which will ultimately form the intricate tooth structure, composed of heterogeneous cellular compartments and mineralised matrices, namely enamel, dentin and cementum. The first morphological sign of tooth development is dental lamina, a thickening of the oral epithelium at the sites of future tooth rows. Humans generate two separate dentitions: primary and permanent teeth which are formed from primary dental lamina and its extension (successional dental lamina), respectively. Many signalling pathways involved in tooth development have been identified and characterised. While some molecules demonstrate transient expression during tooth morphogenesis, many signalling pathways are active at all stages of tooth development and regulate tooth induction, morphogenesis and cytodifferentiation. Key Concepts Tooth development is regulated by a chain of epithelial–mesenchymal interactions that generate unique morphological features which mark different stages of development. The first sign of tooth formation is an epithelial thickening known as the dental lamina. In humans, the initial dental lamina generates primary dentition and extends into a structure called successional lamina from which permanent teeth develop. Budding morphogenesis and crown formation are regulated by signals emanating from the epithelial signalling centres called initiation knots and enamel knots, respectively. Many signalling molecules and receptors are expressed at different stages of tooth development and have been shown to play important roles in the regulation of tooth morphogenesis and in induction of the differentiation of odontoblasts and ameloblasts. Morphogenesis of the replacement and successionally formed teeth is similar to the morphogenesis of the primary teeth and is regulated by the same signalling pathways.

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Sox2+ Stem Cells Contribute to All Epithelial Lineages of the Tooth via Sfrp5+ Progenitors

Cited by 215 publications

References 54 publications

Sox2+ progenitors in sharks link taste development with the evolution of regenerative teeth from denticles

Sox2+ progenitors in sharks link taste development with the evolution of regenerative teeth from denticles

Evolution and developmental diversity of tooth regeneration

Tooth Induction

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