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.

Assessing complexity in hominid dental evolution: Fractal analysis of great ape and human molars

“…Developmental models indicate that nutrients do not arrive homogeneously to all the ameloblasts in the slightly convex areas of the EDJ, creating a pattern of differential enamel deposition. This developmental mechanism is nonlinear, so small perturbations in the initial conditions can result in large changes in the final pattern of enamel crenulations in the outer surface (Häkkinen et al, 2019). These nonlinear dynamics are well known and have been described in models of dental development (Salazar‐Ciudad & Jernvall, 2005).…”

“…The topology of both surfaces differs in some species, which indicates that the configuration of the EDJ is not the only factor determining occlusal complexity on the enamel surface (Skinner et al, 2010). One possibility is that the flow of nutrients by diffusion into ameloblasts is reduced in slightly concave areas of the EDJ, driving to irregular patterns of enamel deposition (Häkkinen et al, 2019).…”

The spatial distribution of focal stacks within the inner enamel layer of mandibular mouse incisors

“…A second problem is the presently unknown rate at which the wave of differentiation for ameloblasts (ameloblast extension rate, Shellis, 1998) spreads mesially and laterally from the first induction event occurring in the central region at the start of each new renewal cycle (Figures 11 and 12; figure 10 in Smith et al, 2019b). This is important because the same spatial sequence of development will occur when ameloblasts complete their differentiation and begin secreting enamel (Häkkinen et al, 2019; Simmer et al, 2010). The first inductive event for focal stacks per renewal cycle in unbent virtual coordinate space for inner enamel presumably occurs in one of the yellow boxes as illustrated in Figure 11 when considering renewal in just inner enamel, or one of the most apical green boxes shown in Figure 12 when considering renewal of the entire enamel layer.…”

The landscape of tooth shape: Over 20 years of dental topography in primates

“…Despite understanding the heritability of some aspects of dental morphology, 91,92 we have no understanding of the heritability of biomechanically relevant aspects of molar occlusal morphology and how it relates to EDJ shape and/or enamel secretion patterns in primates 93 . This is necessary to construct evolutionary models to (a) understand how selection is acting on dental topography and (b) perform more accurate dietary reconstructions, by understanding how long it takes teeth to become adapted to diet.…”