Abstract
Synovial joints are the lubricated connections between the bones of our body that are commonly affected in arthritis. It is assumed that synovial joints first evolved as vertebrates came to land, with ray-finned fishes lacking lubricated joints. Here, we examine the expression and function of a critical lubricating protein of mammalian synovial joints, Prg4/Lubricin, in diverse ray-finned fishes. We find that Prg4 homologs are specifically enriched at the jaw and pectoral fin joints of zebrafish, stickleback, and gar, with genetic deletion of the zebrafish prg4b gene resulting in the same age-related degeneration of joints as seen in lubricin-deficient mice and humans. Our data support lubricated synovial joints evolving much earlier than currently accepted, at least in the common ancestor of all bony vertebrates. Establishment of the first arthritis model in the highly regenerative zebrafish will offer unique opportunities to understand the aetiology and possible treatment of synovial joint disease.
Highlights
Synovial joints allow for free movement between adjacent bones and are characterized by a fluidfilled cavity separating layers of hyaline articular cartilage
Given the suggested synovial-like morphology of jaw joints in several fishes, we examined whether joints of the widely used teleost species, the zebrafish (Danio rerio), display synovial morphology (Figure 1A)
While study of zebrafish has contributed to our understanding of the embryonic development of the jaw joint, zebrafish larvae at the most commonly studied stage, 6 days postfertilization, show little evidence of a synovial cavity (Miller et al, 2003)
Summary
Synovial joints allow for free movement between adjacent bones and are characterized by a fluidfilled cavity separating layers of hyaline articular cartilage. The synovial cavity is enclosed by a membrane, which is often strengthened externally by a fibrous capsule and contains lubricating molecules, such as hyaluronic acid and lubricin, that reduce friction at the joint surface (Koyama et al, 2014; Rhee et al, 2005). Whereas previous histological studies had suggested that the jaw joints of lungfish (a lobe-finned fish like humans) (Bemis, 1986), and potentially longnose gar and sturgeon (ray-finned fishes) (Haines, 1942), have synovial-like morphology, the extent to which these joints are molecularly and functionally similar to tetrapod synovial joints had remained untested. The assumption that ray-finned fishes lack the sophisticated types of lubricated joints found in humans has hampered the use of the zebrafish model for the study of synovial joint diseases such as arthritis.
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