Abstract
The epiphysis of femur and tibia in the lizard Podarcis muralis can extensively regenerate after injury. The process involves the articular cartilage and metaphyseal (growth) plate after damage. The secondary ossification center present between the articular cartilage and the growth plate is replaced by cartilaginous epiphyses after about one month of regeneration at high temperature. The present study analyzes the origin of the chondrogenic cells from putative stem cells located in the growing centers of the epiphyses. The study is carried out using immunocytochemistry for the detection of 5BrdU-labeled long retaining cells and for the localization of telomerase, an enzyme that indicates stemness. The observations show that putative stem cells retaining 5BrdU and positive for telomerase are present in the superficial articular cartilage and metaphyseal growth plate located in the epiphyses. This observation suggests that these areas represent stem cell niches lasting for most of the lifetime of lizards. In healthy long bones of adult lizards, the addition of new chondrocytes from the stem cells population in the articular cartilage and the metaphyseal growth plate likely allows for slow, continuous longitudinal growth. When the knee is injured in the adult lizard, new populations of chondrocytes actively producing chondroitin sulfate proteoglycan are derived from these stem cells to allow for the formation of completely new cartilaginous epiphyses, possibly anticipating the re-formation of secondary centers in later stages. The study suggests that in this lizard species, the regenerative ability of the epiphyses is a pre-adaptation to the regeneration of the articular cartilage.
Highlights
It is largely established that the regenerative power present in some regions of the body of vertebrates depends on the presence of resident stem cells localized in micro-regions known as stem cell niches [1,2,3]
This study showed that proliferating cells are localized in the articular cartilage and in the metaphyseal growth plate of the epiphyses of the long bones, likely as a part of the continuous growth in this species
The femur and tibia contained secondary ossification centers, seen in sections intercepting the medial axis of these bones, and located between the articular cartilage facing the synovial cavity and the metaphyseal growth plate
Summary
It is largely established that the regenerative power present in some regions of the body of vertebrates depends on the presence of resident stem cells localized in micro-regions known as stem cell niches [1,2,3]. The number, extension, and duration of the niches during lifetimes in different vertebrates may vary and be higher in anamniotes such as amphibians and fish that grow for most of their lifespan in comparison to birds and mammals (homethermic amniotes) that instead possess a determinate growth. Tissue regeneration is generally higher than in mammals and birds, and the tail can broadly regenerate, imperfectly, in many lizards [4,5,6,7]. It is likely that skeletally mature reptiles possess stem cell niches in body regions where growth is still active, whereas stem cell niches are reduced in mammals at skeletal maturity. One of the tissues capable of regeneration in lizards is the cartilaginous tissue of the tail vertebrae, which recovers after lesions and gives rise to a long cartilaginous tube in the regenerated tail [9,10,11,12,13,14]
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