Phenotypic plasticity and mechano-transduction in the teleost skeleton

Abstract

The proper formation, growth and maintenance of many bones depends on the mechanical loads generated by gravity and muscles. Mechanical loading by muscle forces does not only affect bone growth and maintenance in adult and juvenile vertebrates, but also affects larval and embryonic bone development. We have reviewed the current understanding of mechanotransduction in birds and mammals and compared it to teleosts. The major mechanosensing cells in the adult mammalian and avian skeleton are osteocytes. They are interconnected via cell processes and are contained within a canalicular network. Basal teleosts have osteocytes but their connectivity is questionable and the presence of a functional canalicular network is unlikely. Advanced teleosts have acellular bone and therefore lack osteocytes. Yet the skeleton of teleosts does show adaptive responses to changes in mechanical load. In these animals it is likely that osteoblasts, bone surface cells and chondrocytes act as mechanosensors. The factors expressed by osteocytes upon mechanical stimulation have been extensively investigated in vitro and in vivo in adult mammals and birds. Less is, however, known about the mechanotransduction pathway during embryonic bone development. The zebrafish presents new opportunities to analyze the mechanotransduction pathway during early (larval) bone formation due to the ex utero development and genetic analyses.

Dynamic skeletogenesis in fishes: Insight of exercise training on developmental plasticity

“…Indeed, we found out that the effect of an increase of water velocity mainly induces changes in the developmental progress in all fins; the responsive elements ossify at comparatively smaller size at faster velocity. It is suggested that rearing fish in differential water velocity may affect their locomotion and thus may change the mechanical stress exerted on developing endoskeletal elements (Fischer-Rousseau et al, 2009;Cloutier et al, 2010;Fiaz et al, 2010Fiaz et al, , 2012. In this context, several lines of evidences have shown the correlative link between environmental changes such as differential water velocity and plasticity in timing of skeletogenesis (rather than changes in the relative order of developmental events) in fishes.…”

“…In the case of developing skeletal tissues, time is necessary to cope with environmental changes. However, fish endoskeleton is remarkable in that it develops relatively late in ontogeny compared to mammals and birds; most of it occurs after hatching (Fiaz et al, 2010;Saele and Pittman, 2010). Even post-hatching exposure to increased water velocity is sufficient to induce plastic responses in timing, primarily with respect to later formed bones and cartilages to a lesser extent.…”

“…Responsive elements display a relative trend towards a delayed chondrification at higher velocity compared to the other treatments, but with concomitant shorter transitions between the cartilaginous and bony states. These observations suggest that chondrocytes of the cartilage precursor may act as mechanosensors, and thus may actively participate in the regulation of the transition of skeletal states in differential mechanical loading environments [see Fiaz et al (2010) for a recent review on mechanosensing of vertebrate skeleton]. Various experiments on chondrocytes have demonstrated that mechanical loading promotes chondrogenesis (Takahashi et al, 1998(Takahashi et al, , 2009Wu et al, 2001;Wong et al, 2003).…”

“…However, in contrast to mammals, two major types of bone are encountered in fishes: acellular or anosteocytic (devoid of osteocytes) and cellular or osteocytic (with osteocytes) (Huysseune, 2000). The occurrence of acellular and cellular bones differs between young [larval teleosts often lack osteocytes (Fiaz et al, 2010)] and old fishes. Generally, salmonid endoskeleton is recognized as cellular (Witten and Huysseune, 2009).…”

“…It has been further stated, at least in guenons, that the chondrocranium is the cranial skeletal system less influenced by epigenetic factors in response to changes in environmental conditions (Cardini and Elton, 2008). However, the diversity of cartilaginous tissues in fish (Witten and Huysseune, 2007;Witten et al, 2010), the mechanisms involved in bone resorption and remodeling (Witten and Huysseune, 2009), the presence or absence of osteocytes and cell processes in basal versus derived teleosts (Parenti, 1986) that mediates mechanostimulation (Fiaz et al, 2010), as well as the lower weightbearing role because of lower gravity pressure (Moss, 1963;Huysseune, 2000) make the fish endoskeleton highly different from that of terrestrial vertebrates. Consequently, the genetic-epigenetic relationships in developing chondral bones may differ between fish and terrestrial vertebrates.…”