Abstract
Understanding the mechanisms by which the zebrafish pectoral fin develops is expected to produce insights on how vertebrate limbs grow from a 2D cell layer to a 3D structure. Two mechanisms have been proposed to drive limb morphogenesis in tetrapods: a growth-based morphogenesis with a higher proliferation rate at the distal tip of the limb bud than at the proximal side, and directed cell behaviors that include elongation, division and migration in a non-random manner. Based on quantitative experimental biological data at the level of individual cells in the whole developing organ, we test the conditions for the dynamics of pectoral fin early morphogenesis. We found that during the development of the zebrafish pectoral fin, cells have a preferential elongation axis that gradually aligns along the proximodistal (PD) axis of the organ. Based on these quantitative observations, we build a center-based cell model enhanced with a polarity term and cell proliferation to simulate fin growth. Our simulations resulted in 3D fins similar in shape to the observed ones, suggesting that the existence of a preferential axis of cell polarization is essential to drive fin morphogenesis in zebrafish, as observed in the development of limbs in the mouse, but distal tip-based expansion is not. Upon publication, biological data will be available at http://bioemergences.eu/modelingFin, and source code at https://github.com/guijoe/MaSoFin. Supplementary data are available at Bioinformatics online.
Highlights
Vertebrate limb development is a classical model system for understanding pattern formation: the process in which spatial organization of differentiated cells and tissues is generated in the embryo
We found that during the development of the zebrafish pectoral fin, cells have a preferential elongation axis that gradually aligns along the proximodistal axis (PD) of the organ
3 Results 3.1 Zebrafish pectoral fin morphogenesis is proximal distal oriented Using the approach described in the methods, we computed the pectoral fin’s main axes for each time point
Summary
Vertebrate limb development is a classical model system for understanding pattern formation: the process in which spatial organization of differentiated cells and tissues is generated in the embryo. How the limb bud lateral plate mesoderm (LPM), which gives rise to skeletal elements and tendons, grows outward from the body trunk and acquires its particular shape remains unclear. The formation of the zebrafish pectoral fin bud is a model for limb development, as it is especially suited for long-term imaging owing to its external embryonic development and translucent body. The formation of the pectoral fin initiates at 18 hours post fertilization (hpf), when LPM cells condense at the prospective fin location as a flat 2D cell layer under a single layer of ectodermal cells. Over the course of the 30 hours, the fin bud grows and forms a 3D structure. LPM cells proliferate and myoblasts coming from neighbouring somites enter the fin bud, where they will give rise to muscle bundles. At the distal tip of the fin bud, ectodermal cells align to form the so-called apical ectodermal ridge (AER) known to act as a source of molecular signaling required for the fin growth
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