Abstract
Epimorphic regeneration of lost body segments is a widespread phenomenon across annelids. However, the molecular inducers of the cell sources for this reparative morphogenesis have not been identified. In this study, we focused on the role of fibroblast growth factor (FGF) signaling in the posterior regeneration of Alitta virens. For the first time, we showed an early activation of FGF ligands and receptor expression in an annelid regenerating after amputation. The expression patterns indicate that the entire regenerative bud is competent to FGFs, whose activity precedes the initiation of cell proliferation. The critical requirement of FGF signaling, especially at early stages, is also supported by inhibitor treatments followed by proliferation assay, demonstrating that induction of blastemal cells depends on FGFs. Our results show that FGF signaling pathway is a key player in regenerative response, while the FGF-positive wound epithelium, ventral nerve cord and some mesodermal cells around the gut could be the inducing tissues. This mechanism resembles reparative regeneration of vertebrate appendages suggesting such a response to the injury may be ancestral for all bilaterians.
Highlights
Annelids are known for their exceptional regenerative abilities
Our results show that fibroblast growth factor (FGF) signaling pathway is a key player in regenerative response, while the FGF-positive wound epithelium, ventral nerve cord and some mesodermal cells around the gut could be the inducing tissues
We focused on the role of FGF signaling in the posterior regeneration of Alitta virens
Summary
Annelids are known for their exceptional regenerative abilities. Their potential to restore considerable body parts, derived from all germ layers, outmatches other classical regeneration models. FGFs bind to tyrosine-kinase receptors (FGFRs) and activate multiple intracellular pathways, such as MAP-kinase, PI3-Akt, and PLCγ These pathways regulate different cellular responses: proliferation, differentiation, migration, epithelial-mesenchymal transition, suppression of apoptosis and inflammation [17,18,19]. Vertebrate models of limb, tail and fin regeneration demonstrate that FGF molecules mediate the signal to initiate the formation of the blastema and subsequent proliferation of its cells [8,10,28]. In the context of invertebrate regeneration, FGF activity is described for cnidarians [9,35,36], planarians [37,38] and a brittle star [12] These works demonstrate that FGFs have a specific expression and play distinct roles in these organisms. These findings are important for understanding when and how FGFs acquired their incredible capacity to promote regeneration across the whole bilaterian clade
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