Abstract
Growth plate and articular cartilage constitute a single anatomical entity early in development but later separate into two distinct structures by the secondary ossification center (SOC). The reason for such separation remains unknown. We found that evolutionarily SOC appears in animals conquering the land - amniotes. Analysis of the ossification pattern in mammals with specialized extremities (whales, bats, jerboa) revealed that SOC development correlates with the extent of mechanical loads. Mathematical modeling revealed that SOC reduces mechanical stress within the growth plate. Functional experiments revealed the high vulnerability of hypertrophic chondrocytes to mechanical stress and showed that SOC protects these cells from apoptosis caused by extensive loading. Atomic force microscopy showed that hypertrophic chondrocytes are the least mechanically stiff cells within the growth plate. Altogether, these findings suggest that SOC has evolved to protect the hypertrophic chondrocytes from the high mechanical stress encountered in the terrestrial environment.
Highlights
The mammalian skeleton articulates via articular cartilage, covering the ends of long bones, and grows in length via epiphyseal cartilage, presented as tiny discs of chondrocytes referred to as growth plates and located near the ends of long bones
We show here that the secondary ossification center (SOC) protects hypertrophic chondrocytes from mechanical stress and likely appeared in evolution in association with this function
We found that hypertrophic chondrocytes are characterized by very low mechanical stiffness and high vulnerability to loading
Summary
The mammalian skeleton articulates via articular cartilage, covering the ends of long bones, and grows in length via epiphyseal cartilage, presented as tiny discs of chondrocytes referred to as growth plates and located near the ends of long bones. This skeletal element forms during early postnatal development and splits the initially contiguous cartilaginous element (the cartilaginous epiphysis) into distinct articular and growth plate cartilage (Hall, 2015) (see Figure 1—figure supplement 1A–B for orientation) This spatial separation of articular and growth plate structures is not always required for articulation or bone growth, since it is absent in several vertebrate taxa, such as stem tetrapods (Sanchez et al, 2014; Sanchez et al, 2016), Chelonians, Crocodilians, and Urodeles (salamanders) (Frobisch and Shubin, 2011; Haines, 1938) (see examples of salamander cartilage in Figure 1—figure supplement 1C–D)
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