Mineralization patterns in elasmobranch fish

Abstract

This article reviews current findings on the organic matrix and the mineralization patterns in elasmobranchs, including an analysis of the role of the dental epithelial cells and the odontoblasts during odontogenesis. Our electron micrographs demonstrated that tubular vesicles limited by a unit membrane occupied the bulk of the elasmobranch enameloid matrix during the stage of enameloid matrix formation. It is likely that the tubular vesicles originated from the odontoblast processes. Two types of electron-dense fibrils, with cross-striations at intervals of approximately either 17 nm or 55 nm, respectively, were detected in the enameloid matrix. These data suggest that odontoblasts were strongly involved in enameloid matrix formation and in initial enameloid mineralization. Two types of odontoblasts, dark and light cells, were recognized during the stage of dentinogenesis. The light cells contained numerous mitochondria, intermediate filaments, and microtubules that extended their processes into the dentin. The dark cells possessed a well-developed Golgi apparatus and many cisternae in the rough endoplasmic reticulum, which suggests that the dark cells are involved in the formation of dentin. The inner dental epithelial (IDE) cells exhibited a well-developed Golgi apparatus, many mitochondria, cisternae of smooth endoplasmic reticulum, vesicles, vacuoles, and granules during the mineralization and maturation stages. During the stages of mineralization and early maturation, ACPase-positive granules were visible in the IDE cells and ALPase and Ca-ATPase activities were found at the lateral and proximal cell membrane of the IDE cells, suggesting that the IDE cells are involved in the removal of enameloid organic matrix and in the process of mineralization during later stages of enameloid formation. Our data indicate that elasmobranch enameloid is distinct from teleost enameloid, based on its organic content, on the mechanisms of its mineralization, and on the role of IDE cells concerning enameloid formation.

The homology and phylogeny of chondrichthyan tooth enameloid

“…In contrast, actinopterygian enameloid crystallites precipitate initially upon matrix vesicles, and accumulate subsequently along collagen fibers (Sasagawa, 1997). Furthermore, the mineralization of actinopterygian enameloid commences at the enameloid-dentine junction and progresses toward the outer enameloid surface, while mineralization of elasmobranch enameloid generally occurs throughout the layer, with no discrete front (Sasagawa, 2002-though see Fossé et al, 1974Risnes, 1990;Cuny and Risnes, 2005). These differences in matrix composition and mineralization patterns have led many to regard elasmobranch enameloid (''coronoïn'' [Bendix-Almgreen, 1983]) and actinopterygian enameloid (''acrodin'' [Ørvig, 1978]) as two distinct products of convergent evolution, despite previous assertions of homology .…”

“…Reif (1979) postulated that the organic matrix of the thin layer of SCE overlying the PFE of neoselachian teeth is derived almost exclusively from ameloblastic cell products, due to its position at the outer enameloid surface and probable formation in complete isolation from odontoblast cell secretions. While there is still much debate regarding the specific control of enameloid crystallite orientation and the development of ''higher order structures'' (i.e., crystallite bundles) within the layer, it is broadly accepted that odontoblast-derived cell products (namely, tubular vesicles) play a fundamental role in the initiation and direction of crystallite growth (Prostak et al, 1990;Sasagawa, 2002). If a mixed matrix composed of both ameloblast cell secretions and odontoblast-derived tubular vesicles is, in fact, critical to the development of higher order enameloid structures, then a deficiency of such vesicles (i.e., their presence below a ''threshold quantity'') may inhibit the development of enameloid that is microstructurally more complex than a monolayer of randomly oriented single crystallites.…”

“…While broad developmental and histological similarities between the tissues in the two taxa have led some to argue for their homology , subtle differences in organic composition and mineralization patterns between chondrichthyan and actinopterygian enameloid (Sasagawa, 2002), as well as the purported absence of enameloid on the teeth of basal elasmobranchs (Øvig, 1966;Gross, 1973), have led others to speculate that these tissues may, instead, be the products of convergent evolution (Bendix-Almgreen, 1983;Sasagawa, 2002). Indeed, this view accords with recent suggestions that, far from being a shared primitive character of jawed vertebrates, teeth have evolved independently among chondrichthyans and osteichthyans (Smith, 2003;Johanson and Smith, 2003;Smith and Johanson, 2003) and, thus, scenarios in which teeth and jaws are the key innovations underpinning an adaptive radiation of jawed vertebrates may be entirely unfounded.…”

“…A comprehensive survey of tooth microstructure in chondrichthyans would undoubtedly clarify the phylogenetic relationship between chondrichthyan and actinopterygian enameloid BendixAlmgreen, 1983;Sasagawa, 2002). The primitive actinopterygian condition is already well established (Janvier, 1978;Smith, 1992;Richter and Smith, 1995).…”

Histology of the heterostracan dermal skeleton: Insight into the origin of the vertebrate mineralised skeleton

“…In accordance with this interpretation, he regarded the capping layer of heterostracans as enamel (Moss, 1968a). However, true enamel is genetically and developmentally distinct from 'enameloid' present in living teleosts or chondricthyans (Poole, 1967;Sasagawa, 2002;Kawasaki et al, 2004;Kawasaki and Weiss, 2006;Kawasaki et al, 2007) and is restricted to osteichthyans (Donoghue, 2001).…”