Lineage tracing of epithelial cells in developing teeth reveals two strategies for building signaling centers

Du, Wei; Hu, Jingtian; Du, Wen; Klein, Ophir D.

doi:10.1074/jbc.m117.785923

Cited by 30 publications

(44 citation statements)

References 45 publications

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“…Lineage tracing of primary knot cells in mouse indicate that primary knot cells contribute to the buccal (e.g. protoconid) (48) and possibly the lingual secondary knot (49). However, it remains uncertain whether the differential contribution of primary knot cells to these secondary centres may influence the latter’s signalling dynamics (50).…”

Section: Discussionmentioning

confidence: 99%

Predicting Evolutionary Transitions in Tooth Complexity With a Morphogenetic Model

Amc

Sears

Rücklin

2019

Preprint

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15The extent to which evolutionary transitions are shaped by developmental bias remains 16 poorly understood. Classically, morphological variation is assumed to be abundant and 17 continuous, but if morphogenesis biases how traits vary than evolutionary transitions might 18 follow somewhat predictable steps. Compared to other anatomical structures, teeth have an 19 exceptional fossil record which documents striking evolutionary trajectories toward 20 complexity. Using computer simulations of tooth morphogenesis, we examined how varying 21 developmental parameters influenced transitions from morphologically simple to complex 22 teeth. We find that as tooth complexity increases, development tends to generate 23 progressively more discontinuous variation which could make the fine-tuning of dietary 24 adaptation difficult. Transitions from simple to complex teeth required an early shift from 25 mesiodistal to lateral cusp patterning which is congruent with patterns of dental 26 complexification in early mammals. We infer that the contributions of primary enamel knot 27 cells to secondary enamel knots which are responsible for patterning lateral cusps may have 28 been an important developmental innovation in tribosphenic mammals. Our results provide 29 evidence that development can bias evolutionary transitions and highlights how 30 morphogenetic modelling can play an important role in building more realistic models of 31 morphological character evolution.32 33 34 35Despite more than two centuries of investigation the extent to which 'laws of variation'(1) 36 govern the tempo and mode of evolution remains poorly understood (2-5). Both as a 37 simplifying assumption and because of ignorance about generating processes, morphological 38 variation has traditionally been assumed to be abundant and continuous (1, 6). However, 39 several decades of evo-devo studies have highlighted how interactions between genes, cells, 40 tissues, and the external environment, favour the generation of some types of variation, whilst 41 conspiring against others (2, 4, 7, 8). This 'anisotropic' model of morphological variation 42 implies that evolutionary transitions are more likely to follow some evolutionary pathways 43 than others, and suggests that knowledge of morphogenesis can be used to predict some 44 aspects of morphological evolution (9-11). But, the extent to which these evo-devo insights 45 have penetrated other areas of evolutionary biology, such as phylogenetics, is limited (12-14), 46 at least in part because empirical models of developmental bias are sorely lacking. As an 47 example, the most widely used model of character substitution in morphological 48 phylogenetics, the Markov k (Mk) model (15), assumes equal likelihoods of transition 49 between character states as well as character independence; both assumptions which can be 50 violated by developmental correlations (11, 12, 16, 17). Despite accumulating evidence for 51 wide-spread developmental non-independence and bias in how morphological traits vary (4) 52 t...

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Section: Discussionmentioning

confidence: 99%

Predicting Evolutionary Transitions in Tooth Complexity With a Morphogenetic Model

Amc

Sears

Rücklin

2019

Preprint

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“…These molecules may promote continuing proliferation in the adjacent epithelium, resulting in epithelial elongation as the tooth enters the cap stage . Secondary EKs form during the bell stage mainly from undifferentiated epithelial cells, with the buccal secondary EK receiving contributions from cells of the primary EK . The secondary EKs are also non‐proliferative and help determine both future cusp positions and the eventual crown shape .…”

Section: Epithelial and Mesenchymal Interactions Drive Tooth Formationmentioning

confidence: 99%

“…Different from molars, in the single cuspid mouse incisor only a primary EK forms through a de novo process from cells located in the posterior lower half of the incisor bud . Incisor epithelium rotates posteriorly at the cap stage, instead of downwards as in molars.…”

Section: Micro‐ and Macro‐forces Regulate Stem Cell Proliferation Andmentioning

confidence: 99%

“…[21,22] Secondary EKs form during the bell stage mainly from undifferentiated epithelial cells, with the buccal secondary EK receiving contributions from cells of the primary EK. [23,24] The secondary EKs are also nonproliferative and help determine both future cusp positions and the eventual crown shape. [2] During the bell stage, cells in the inner enamel epithelium neighboring the secondary EK begin to differentiate into ameloblasts, and the underlying mesenchyme gives rise to odontoblasts.…”

Section: Signaling-controlled Proliferation and Differentiation Regulmentioning

confidence: 99%

“…[109,110] Different from molars, in the single cuspid mouse incisor only a primary EK forms through a de novo process from cells located in the posterior lower half of the incisor bud. [23,62] Incisor epithelium rotates posteriorly at the cap stage, instead of downwards as in molars. Molecularly, the formation of the incisor EK is dependent on alpha-catenin-mediated inhibition of YAP activity, [111] such that restriction of YAP in the cytoplasm allows cells to cease proliferation and become specialized in signal secretion.…”

Section: Differential Tissue Growth Generates Force For Tooth Morphogmentioning

confidence: 99%

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Tissue Mechanical Forces and Evolutionary Developmental Changes Act Through Space and Time to Shape Tooth Morphology and Function

Calamari

Klein

2018

BioEssays

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Efforts from diverse disciplines, including evolutionary studies and biomechanical experiments, have yielded new insights into the genetic, signaling, and mechanical control of tooth formation and functions. Evidence from fossils and non-model organisms has revealed that a common set of genes underlie tooth-forming potential of epithelia, and changes in signaling environments subsequently result in specialized dentitions, maintenance of dental stem cells, and other phenotypic adaptations. In addition to chemical signaling, tissue forces generated through epithelial contraction, differential growth, and skeletal constraints act in parallel to shape the tooth throughout development. Here we review recent advances in understanding dental development from these studies and discuss important gaps that can be filled through continued application of evolutionary and biomechanical approaches.

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Six1 is required for signaling center formation and labial‐lingual asymmetry in developing lower incisors

Takahashi

Ikeda

Ohmuraya

et al. 2020

Developmental Dynamics

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Background The structure of the mouse incisor is characterized by its asymmetric accumulation of enamel matrix proteins on the labial side. The asymmetric structure originates from the patterning of the epithelial incisor placode through the interaction with dental mesenchymal cells. However, the molecular basis for the asymmetric patterning of the incisor germ is largely unknown. Results A homeobox transcription factor SIX1 was shown to be produced in the mandibular mesenchyme, and its localization patterns changed dynamically during lower incisor development. Six1−/− mice exhibited smaller lower incisor primordia than wild‐type mice. Furthermore, Six1−/− mice showed enamel matrix production on both the lingual and labial sides and disturbed odontoblast maturation. In the earlier stages of development, the formation of signaling centers, the initiation knot and the enamel knot, which are essential for the morphogenesis of tooth germs, were impaired in Six1−/− embryos. Notably, Wnt signaling activity, which shows an anterior‐posterior gradient, and the expression patterns of genes involved in incisor formation were altered in the mesenchyme in Six1−/− embryos. Conclusion Our results indicate that Six1 is required for signaling center formation in lower incisor germs and the labial‐lingual asymmetry of the lower incisors by regulating the anterior‐posterior patterning of the mandibular mesenchyme.

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Lineage tracing of epithelial cells in developing teeth reveals two strategies for building signaling centers

Cited by 30 publications

References 45 publications

Predicting Evolutionary Transitions in Tooth Complexity With a Morphogenetic Model

Predicting Evolutionary Transitions in Tooth Complexity With a Morphogenetic Model

Tissue Mechanical Forces and Evolutionary Developmental Changes Act Through Space and Time to Shape Tooth Morphology and Function

Six1 is required for signaling center formation and labial‐lingual asymmetry in developing lower incisors

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