Hydrodynamic stress and phenotypic plasticity of the zebrafish regenerating fin

Abstract

Understanding how extrinsic factors modulate genetically encoded information to produce a specific phenotype is of prime scientific interest. In particular, the feedback mechanism between abiotic forces and locomotory organs during morphogenesis to achieve efficient movement is a highly relevant example of such modulation. The study of this developmental process can provide unique insights on the transduction of cues at the interface between physics and biology. Here, we take advantage of the natural ability of adult zebrafish to regenerate their amputated fins to assess its morphogenic plasticity upon external modulations. Using a variety of surgical and chemical treatments, we are able to induce phenotypic responses to the structure of the fin. Through the ablation of specific rays in regenerating caudal fins, we generate artificially narrowed appendages in which the fin cleft depth and the positioning of rays bifurcations are perturbed compared to normal regenerates. To dissect the role of mechanotransduction in this process, we investigate the patterns of hydrodynamic forces acting on the surface of a zebrafish fin during regeneration by using particle tracking velocimetry on a range of biomimetic hydrofoils. This experimental approach enables us to quantitatively compare hydrodynamic stress distributions over flapping fins of varying sizes and shapes. As a result, viscous shear stress acting on the distal margin of regenerating fins and the resulting internal tension are proposed as suitable signals for guiding the regulation of ray growth dynamics and branching pattern. Our findings suggest that mechanical forces are involved in the fine-tuning of the locomotory organ during fin morphogenesis.

Mitochondria-Assisted Photooxidation to Track Singlet Oxygen at Homeostatic Membrane Microviscosity

“…This also highlights the crucial role that the different homeostatic membrane order status plays in the mitochondrial ROS monitoring for different models. This finding also indicates that MitoT1 is a more sensitive dual-color microviscosity reporter due to the benz­[ e ]­indole moiety, which is affected by the high viscous hydrodynamic stress as reported in caudal fin cells …”

“…This finding also indicates that MitoT1 is a more sensitive dual-color microviscosity reporter due to the benz[e]indole moiety, which is affected by the high viscous hydrodynamic stress as reported in caudal fin cells. 43 To further showcase the MitoT1-and MitoT2-sensing features of native 1 O 2 production, we analyzed the injury response at a caudal fin wound (Figure 4). Zebrafish is a model system for tissue regeneration studies, helping to understand tissue maintenance and turnover.…”

Fin ray branching is defined by TRAP+ osteolytic tubules

“…Ablation of mpeg1 -positive macrophages, a potential source and/or regulator of the OLTs, resulted in a reduced number of bifurcated rays (Petrie et al, 2014). Interestingly, a recent study proposed that ray branching is modulated by biomechanical forces (Dagenais et al, 2021). In fact, bone formation is well known to rely on the mechanosensitive properties of bone-forming cells that, in addition to bone deposition, are also involved in the recruitment of osteoclasts and, therefore, regulate bone resorption (Xiao and Quarles, 2015).…”

“…Importantly, among the signaling pathways controling bone patterning, such as during limb development (Capdevila and Belmonte, 2001; Riddle et al, 1993), Sonic hedgehog (Shh) has been described as a key factor controling ray bifurcation during fin regeneration (Armstrong et al, 2017; Laforest et al, 1998). However, repetitive amputations (Azevedo et al, 2012), macrophage activity (Petrie et al, 2014), actinotrichia organization (Nakagawa et al, 2022), and hydrodynamics (Dagenais et al, 2021) are able to alter the proximo-distal position of ray branchpoints through apparently Shh-independent mechanisms. Thus, the formation and shaping of bifurcated bony structures and the cellular contribution to these processes remain unclear.…”

Regeneration of the dermal skeleton and wound epidermis formation depend on BMP signaling in the caudal fin of platyfish

“…Although the regenerated fin recapitulates its initial form, the primary ray bifurcations are distally shifted relative to the original developmental position ( Akimenko et al, 2003 ; Azevedo et al, 2011 ). Furthermore, ray branching might be further distally displaced or even suppressed through a physical separation of adjacent rays during regeneration ( Marí-Beffa et al, 1999 ; Murciano et al, 2002 ; Dagenais et al, 2021 ). Another interesting observation is that the newly formed twin rays can be gradually stitched together, depending on the balance between bone mineralization and resorption during ray branching formation ( Cardeira-da-Silva et al, 2022 ).…”