Ultrastructural, material and crystallographic description of endophytic masses – A possible damage response in shark and ray tessellated calcified cartilage

Abstract

The cartilaginous endoskeletons of elasmobranchs (sharks and rays) are reinforced superficially by minute, mineralized tiles, called tesserae. Unlike the bony skeletons of other vertebrates, elasmobranch skeletons have limited healing capability and their tissues' mechanisms for avoiding damage or managing it when it does occur are largely unknown. Here we describe an aberrant type of mineralized elasmobranch skeletal tissue called endophytic masses (EPMs), which grow into the uncalcified cartilage of the skeleton, but exhibit a strikingly different morphology compared to tesserae and other elasmobranch calcified tissues. We use materials and biological tissue characterization techniques, including computed tomography, electron and light microscopy, X-ray and Raman spectroscopy and histology to characterize the morphology, ultrastructure and chemical composition of tesserae-associated EPMs in different elasmobranch species. EPMs appear to develop between and in intimate association with tesserae, but lack the lines of periodic growth and varying mineral density characteristic of tesserae. EPMs are mineral-dominated (high mineral and low organic content), comprised of birefringent bundles of large calcium phosphate crystals (likely brushite) aligned end to end in long strings. Both tesserae and EPMs appear to develop in a type-2 collagen-based matrix, but in contrast to tesserae, all chondrocytes embedded or in contact with EPMs are dead and mineralized. The differences outlined between EPMs and tesserae demonstrate them to be distinct tissues. We discuss several possible reasons for EPM development, including tissue reinforcement, repair, and disruptions of mineralization processes, within the context of elasmobranch skeletal biology as well as damage responses of other vertebrate mineralized tissues.

Morphological and histological characterization of an ectopically mineralized structure in a gilthead sea bream Sparus aurata with opercular deformation

“…Recently, Seidel et al (2017) reported aberrant, mineralized structures in cartilage of elasmobranchs, which they referred to as endophytic masses (EPMs) and which phenotypically shows several resemblances with the EMS of this study. These EPMs are closely associated with tesserae but reveal distinct characteristics, such as hypermineralized dead cells, a "brushstroke-like" pattern of randomly oriented mineralized bundles in the matrix, crystal strings in the mineral phase and a frayed interface with the surrounding unmineralized cartilage (Seidel et al, 2017).…”

“…In order to assess the characteristics and origin of this structure, a comparison with other abnormal tissues that share similar traits with this EMS is provided. Although some similarities hinted towards a neoplasm derived from hyaline cartilage, the phenotype corresponds most to a similar structure found in the cartilaginous endoskeleton of elasmobranchs (Seidel et al, ).…”

“…Differences in lacunar spatial arrangement and morphology are also evident. Whereas mineralized cell lacunae in EPMs show a generally rounded morphology and often seem to have housed isogenous cell pairs [Figure 5 in Seidel et al ()], a large proportion of EMS lacunae are flattened, and the rounded lacunae still preserving cell material appear to have contained only a single cell. The degree of mineralization of EPMs varies but never exceeds the highest mineral density of tesserae, while the EMS is evidently hypermineralized relatively to the other mineralized skull elements, showing a comparable mineral density to that of otoliths.…”

Mineralisation of theCallorhinchusvertebral column (Holocephali; Chondrichthyes)

“…Cells within the neural arch, basidorsal and basiventral cartilages can be categorised with respect to morphology, and distribution within the cartilage. Chondrocytes located deeper in the cartilage interior ( Figures 2A, 3B hypertrophy, which has not been observed in chondrichthyans (Dean et al, 2015;Seidel et al, 2017b; but see Debiais-Thibaud [2019] for a summary of contrary opinions).…”

Determination of optimum Al content in HA‐Al2O3 nanocomposites coatings prepared by electrophoretic deposition on titanium substrate

“…The functions of diseased and broken calcified tissues, such as bone and teeth, can be restored by applying orthopedic and dental implants. The good fixation of these implants in the body depends on the presence of a stable and powerful interface between the bone and the implant . Bio inert metallic implants are used as high load bearing bones because of their superior strength, biocompatibility, and corrosion resistance .…”