Modeling enamel matrix secretion in mammalian teeth.
ABSTRACT: The most mineralized tissue of the mammalian body is tooth enamel. Especially in species with thick enamel, three-dimensional (3D) tomography data has shown that the distribution of enamel varies across the occlusal surface of the tooth crown. Differences in enamel thickness among species and within the tooth crown have been used to examine taxonomic affiliations, life history, and functional properties of teeth. Before becoming fully mineralized, enamel matrix is secreted on the top of a dentine template, and it remains to be explored how matrix thickness is spatially regulated. To provide a predictive framework to examine enamel distribution, we introduce a computational model of enamel matrix secretion that maps the dentine topography to the enamel surface topography. Starting from empirical enamel-dentine junctions, enamel matrix deposition is modeled as a diffusion-limited free boundary problem. Using laboratory microCT and synchrotron tomographic data of pig molars that have markedly different dentine and enamel surface topographies, we show how diffusion-limited matrix deposition accounts for both the process of matrix secretion and the final enamel distribution. Simulations reveal how concave and convex dentine features have distinct effects on enamel surface, thereby explaining why the enamel surface is not a straightforward extrapolation of the dentine template. Human and orangutan molar simulations show that even subtle variation in dentine topography can be mapped to the enamel surface features. Mechanistic models of extracellular matrix deposition can be used to predict occlusal morphologies of teeth.
Project description:The occlusal morphology of the teeth is mostly determined by the enamel-dentine junction morphology; the enamel-dentine junction plays the role of a primer and conditions the formation of the occlusal enamel reliefs. However, the accretion of the enamel cap yields thickness variations that alter the morphology and the topography of the enamel-dentine junction (i.e., the differential deposition of enamel by the ameloblasts create an external surface that does not necessarily perfectly parallel the enamel-dentine junction). This self-reliant influence of the enamel on tooth morphology is poorly understood and still under-investigated. Studies considering the relationship between enamel and dentine morphologies are rare, and none of them tackled this relationship in a quantitative way. Major limitations arose from: (1) the difficulties to characterize the tooth morphology in its comprehensive tridimensional aspect and (2) practical issues in relating enamel and enamel-dentine junction quantitative traits. We present new aspects of form representation based exclusively on 3D analytical tools and procedures. Our method is applied to a set of 21 unworn upper second molars belonging to eight extant anthropoid genera. Using geometrical analysis of polygonal meshes representatives of the tooth form, we propose a 3D dataset that constitutes a detailed characterization of the enamel and of the enamel-dentine junction morphologies. Also, for the first time, to our knowledge, we intend to establish a quantitative method for comparing enamel and enamel-dentine junction surfaces descriptors (elevation, inclination, orientation, etc.). New indices that allow characterizing the occlusal morphology are proposed and discussed. In this note, we present technical aspects of our method with the example of anthropoid molars. First results show notable individual variations and taxonomic heterogeneities for the selected topographic parameters and for the pattern and strength of association between enamel-dentine junction and enamel, the enamel cap altering in different ways the "transcription" of the enamel-dentine junction morphology.
Project description:The form of two hard tissues of the mammalian tooth, dentine and enamel, is the result of a combination of the phylogenetic inheritance of dental traits and the adaptive selection of these traits during evolution. Recent decades have been significant in unveiling developmental processes controlling tooth morphogenesis, dental variation and the origination of dental novelties. The enamel-dentine junction constitutes a precursor for the morphology of the outer enamel surface through growth of the enamel cap which may go along with the addition of original features. The relative contribution of these two tooth components to morphological variation and their respective response to natural selection is a major issue in paleoanthropology. This study will determine how much enamel morphology relies on the form of the enamel-dentine junction. The outer occlusal enamel surface and the enamel-dentine junction surface of 76 primate second upper molars are represented by polygonal meshes and investigated using tridimensional topometrical analysis. Quantitative criteria (elevation, inclination, orientation, curvature and occlusal patch count) are introduced to show that the enamel-dentine junction significantly constrains the topographical properties of the outer enamel surface. Our results show a significant correlation for elevation, orientation, inclination, curvature and occlusal complexity between the outer enamel surface and the enamel dentine junction for all studied primate taxa with the exception of four modern humans for curvature (p<0.05). Moreover, we show that, for all selected topometrical parameters apart from occlusal patch count, the recorded correlations significantly decrease along with enamel thickening in our sample. While preserving tooth integrity by providing resistance to wear and fractures, the variation of enamel thickness may modify the curvature present at the occlusal enamel surface in relation to enamel-dentine junction, potentially modifying dental functionalities such as blunt versus sharp dental tools. In terms of natural selection, there is a balance between increasing tooth resistance and maintaining efficient dental tools. In this sense the enamel cap acts as a functional buffer for the molar occlusal pattern. In primates, results suggest a primary emergence of dental novelties on the enamel-dentine junction and a secondary transposition of these novelties with no or minor modifications of dental functionalities by the enamel cap. Whereas enamel crenations have been reported by previous studies, our analysis do not support the presence of enamel tubercles without dentine relief nuclei. As is, the enamel cap is, at most, a secondary source of morphological novelty.
Project description:The effect of phytoliths on tooth wear and function has been contested in studies of animal-plant interactions. For herbivores whose occlusal chewing surface consists of enamel ridges and dentine tissue, the phytoliths might particularly erode the softer dentine, exposing the enamel ridges to different occlusal forces and thus contributing to enamel wear. To test this hypothesis, we fed guinea pigs (Cavia porcellus; n = 36 in six groups) for three weeks exclusively on dry or fresh forage of low (lucerne), moderate (fresh timothy grass) or very high (bamboo leaves) silica content representing corresponding levels of phytoliths. We quantified the effect of these treatments with measurements from micro-computed tomography scans. Tooth height indicated extreme wear due to the bamboo diet that apparently brought maxillary incisors and molars close to the minimum required for functionality. There were negative relationships between a cheek tooth's height and the depth of its dentine basin, corroborating the hypothesis that dentine erosion plays an important role in herbivore tooth wear. In spite of lower body mass, bamboo-fed animals paradoxically had longer cheek tooth rows and larger occlusal surfaces. Because ever-growing teeth can only change in shape from the base upwards, this is a strong indication that failure to compensate for wear by dental height-growth additionally triggered general expansive growth of the tooth bases. The results suggest that enamel wear may intensify after enamel has been exposed due to a faster wear of the surrounding dentine tissue (and not the other way around), and illustrate a surprising plasticity in the reactivity of this rodent's system that adjusts tooth growth to wear.
Project description:Hypsodont equine cheek teeth possess large dental crowns, resting partly in the bony alveolus. Over a horse's life cheek teeth erupt continuously to compensate for occlusal wear of 3-4 mm per year. Parts of the crown initially resting in the bony alveolus become progressively exposed at the occlusal surface with time. Hitherto, it is unclear whether the typical structure of the equine occlusal surface, composed of a complex arrangement of enamel, dentin and cementum, remains constant or undergoes structural changes with age. Therefore, we tested the hypothesis that the occlusal surface composition does not remain constant by a quantitative analysis of the dental substances at multiple levels along the dental crown of equine cheek teeth.Micro-computed tomography scans of 20 upper cheek teeth and 16 lower cheek teeth from 19 domestic horses were morphologically analysed using imaging and measurement software. Area for individual dental substances was measured at different levels from the apex to the occlusal surface. The data was statistically analysed to detect changes in the area of individual substance along the dental crown. The area of peripheral cementum was measured separately for levels inside and outside the bony alveolus.In both, upper and lower cheek teeth, enamel area decreased in an apical direction, while dentine area increased. Peripheral Cementum increased dramatically in the occlusal/coronal extra-alveolar position.With increasing age the occlusal surface content of dentine increases while the content of enamel decreases. These changes are considered relevant for the detailed explanation of forage disruption in horses as well as for the recommendation of concepts in equine dentistry.
Project description:Enamel thickness is highly susceptible to natural selection because thick enamel may prevent tooth failure. Consequently, it has been suggested that primates consuming stress-limited food on a regular basis would have thick-enameled molars in comparison to primates consuming soft food. Furthermore, the spatial distribution of enamel over a single tooth crown is not homogeneous, and thick enamel is expected to be more unevenly distributed in durophagous primates. Still, a proper methodology to quantitatively characterize enamel 3D distribution and test this hypothesis is yet to be developed. Unworn to slightly worn upper second molars belonging to 32 species of anthropoid primates and corresponding to a wide range of diets were digitized using high resolution microcomputed tomography. In addition, their durophagous ability was scored from existing literature. 3D average and relative enamel thickness were computed based on the volumetric reconstruction of the enamel cap. Geometric estimates of their average and relative enamel-dentine distance were also computed using 3D dental topography. Both methods gave different estimations of average and relative enamel thickness. This study also introduces pachymetric profiles, a method inspired from traditional topography to graphically characterize thick enamel distribution. Pachymetric profiles and topographic maps of enamel-dentine distance are combined to assess the evenness of thick enamel distribution. Both pachymetric profiles and topographic maps indicate that thick enamel is not significantly more unevenly distributed in durophagous species, except in Cercopithecidae. In this family, durophagous species such as mangabeys are characterized by an uneven thick enamel and high pachymetric profile slopes at the average enamel thickness, whereas non-durophagous species such as colobine monkeys are not. These results indicate that the distribution of thick enamel follows different patterns across anthropoids. Primates might have developed different durophagous strategies to answer the selective pressure exerted by stress-limited food.
Project description:Tooth crown tissue proportions and enamel thickness distribution are considered reliable characters for inferring taxonomic identity, phylogenetic relationships, dietary and behavioural adaptations in fossil and extant hominids. While most Pleistocene hominins display variations from thick to hyper-thick enamel, Neanderthals exhibit relatively thinner. However, the chronological and geographical origin for the appearance of this typical Neanderthal condition is still unknown. The European late Early Pleistocene species Homo antecessor (Gran Dolina-TD6 site, Sierra de Atapuerca) represents an opportunity to investigate the appearance of the thin condition in the fossil record. In this study, we aim to test the hypothesis if H. antecessor molars approximates the Neanderthal condition for tissue proportions and enamel thickness. To do so, for the first time we characterised the molar inner structural organization in this Early Pleistocene hominin taxon (n = 17) and compared it to extinct and extant populations of the genus Homo from African, Asian and European origin (n = 355). The comparative sample includes maxillary and mandibular molars belonging to H. erectus, East and North African Homo, European Middle Pleistocene Homo, Neanderthals, and fossil and extant H. sapiens. We used high-resolution images to investigate the endostructural configuration of TD6 molars (tissue proportions, enamel thickness and distribution). TD6 permanent molars tend to exhibit on average thick absolute and relative enamel in 2D and 3D estimates, both in the complete crown and the lateral enamel. This condition is shared with the majority of extinct and extant hominin sample, except for Neanderthals and some isolated specimens. However, while the total crown percentage of dentine in TD6 globally resembles the low modern values, the lateral crown percentage of dentine tends to be much higher, closer to the Neanderthal signal. Similarly, the H. antecessor molar enamel distribution maps reveal a relative distribution pattern that is more similar to the Neanderthal condition (with the thickest enamel more spread at the periphery of the occlusal basin) rather than that of other fossil specimens and modern humans (with thicker cuspal enamel). Future studies on European Middle Pleistocene populations will provide more insights into the evolutionary trajectory of the typical Neanderthal dental structural organization.
Project description:Collagen and amelogenin are two major extracellular organic matrix proteins of dentin and enamel, the mineralized tissues comprising a tooth crown. They both are present at the dentin-enamel boundary (DEB), a remarkably robust interface holding dentin and enamel together. It is believed that interactions of dentin and enamel protein assemblies regulate growth and structural organization of mineral crystals at the DEB, leading to a continuum at the molecular level between dentin and enamel organic and mineral phases. To gain insight into the mechanisms of the DEB formation and structural basis of its mechanical resiliency we have studied the interactions between collagen fibrils, amelogenin assemblies, and forming mineral in vitro, using electron microscopy. Our data indicate that collagen fibrils guide assembly of amelogenin into elongated chain or filament-like structures oriented along the long axes of the fibrils. We also show that the interactions between collagen fibrils and amelogenin-calcium phosphate mineral complexes lead to oriented deposition of elongated amorphous mineral particles along the fibril axes, triggering mineralization of the bulk of collagen fibril. The resulting structure was similar to the mineralized collagen fibrils found at the DEB, with arrays of smaller well organized crystals inside the collagen fibrils and bundles of larger crystals on the outside of the fibrils. These data suggest that interactions between collagen and amelogenin might play an important role in the formation of the DEB providing structural continuity between dentin and enamel.
Project description:Quantification of dental long-period growth lines (Retzius lines in enamel and Andresen lines in dentine) and matching of stress patterns (internal accentuated lines and hypoplasias) are used in determining crown formation time and age at death in juvenile fossil hominins. They yield the chronology employed for inferences of life history. Synchrotron virtual histology has been demonstrated as a non-destructive alternative to conventional invasive approaches. Nevertheless, fossil teeth are sometimes poorly preserved or physically inaccessible, preventing observation of the external expression of incremental lines (perikymata and periradicular bands). Here we present a new approach combining synchrotron virtual histology and high quality three-dimensional rendering of dental surfaces and internal interfaces. We illustrate this approach with seventeen permanent fossil hominin teeth. The outer enamel surface and enamel-dentine junction (EDJ) were segmented by capturing the phase contrast fringes at the structural interfaces. Three-dimensional models were rendered with Phong's algorithm, and a combination of directional colored lights to enhance surface topography and the pattern of subtle variations in tissue density. The process reveals perikymata and linear enamel hypoplasias on the entire crown surface, including unerupted teeth. Using this method, highly detailed stress patterns at the EDJ allow precise matching of teeth within an individual's dentition when virtual histology is not sufficient. We highlight that taphonomical altered enamel can in particular cases yield artificial subdivisions of perikymata when imaged using X-ray microtomography with insufficient resolution. This may complicate assessments of developmental time, although this can be circumvented by a careful analysis of external and internal structures in parallel. We further present new crown formation times for two unerupted canines from South African Australopiths, which were found to form over a rather surprisingly long time (> 4.5 years). This approach provides tools for maximizing the recovery of developmental information in teeth, especially in the most difficult cases.
Project description:Tapinocephalids were one of the earliest therapsid clades to evolve herbivory. In acquiring derived tooth-to-tooth occlusion by means of an exaggerated heel and talon crown morphology, members of this family have long been considered herbivorous, yet little work has been done to describe their dentition. Given the early occurrence of this clade and their acquisition of a dentition with several derived features, tapinocephalids serve as an important clade in understanding adaptations to herbivory as well as macroevolutionary patterns of dental trait acquisition. Here we describe the histology of tapinocephalid jaws and incisors to assess adaptations to herbivory. Our results yield new dental characters for tapinocephalids including a peculiar enamel structure and reduced enamel deposition on the occlusal surface. These traits are convergent with other specialized herbivorous dentitions like those found in ornithischian dinosaurs and ungulates. Furthermore, these results demonstrate that while acquiring some specializations, tapinocephalids also retained plesiomorphic traits like alternate, continuous replacement. We interpret these findings as an example of how different combinations of traits can facilitate a derived and specialized dentition and then discuss their implications in the acquisition of a mammal-like dentition.
Project description:BACKGROUND: Equine incisors are subjected to continuous occlusal wear causing multiple, age related changes of the extragingival crown. It is assumed that the occlusal wear is compensated by continued tooth elongation at the apical ends of the teeth. In this study, ?CT-datasets offered the opportunity to analyze the three-dimensional appearance of the extra- and intraalveolar parts of the enamel containing dental crown as well as of the enamel-free dental root. Multiple morphometric measurements elucidated age related, morphological changes within the intraalveolar part of the incisors. RESULTS: Equine incisors possess a unique enamel cover displaying large indentations on the mesial and distal sides. After eruption tooth elongation at the apical end outbalances occlusal wear for two to four years resulting in increasing incisor length in this period of time. Remarkably, this maximum length is maintained for about ten years, up to a tooth age of 13 to 15 years post eruption. Variances in the total length of individual teeth are related to different Triadan positions (central-, middle- and corner incisors) as well as to the upper and lower arcades. CONCLUSION: Equine incisors are able to fully compensate occlusal wear for a limited period of time. However, after this ability ceases, it is expected that a diminished intraalveolar tooth length will cause massive changes in periodontal biomechanics. The time point of these morphodynamic and biomechanical changes (13 to 15 years post eruption) occurs in coincidence with the onset of a recently described destructive disease of equine incisor (equine odontoclastic tooth resorption and hypercementosis) in aged horses. However, further biomechanical, cell biological and microbiological investigations are needed to elucidate a correlation between age related changes of incisor morphology and this disease.