Abstract
Despite extensive study, the morphogenetic mechanisms of heart looping remain controversial because of a lack of information concerning precise tissue-level deformation and the quantitative relationship between tissue andcellular dynamics; this lack of information causes difficulties in evaluating previously proposed models. To overcome these limitations, we perform four-dimensional (4D) high-resolution imaging to reconstruct a tissue deformation map, which reveals that, at the tissue scale, initial heart looping is achieved by left-right (LR) asymmetry in the direction of deformation within the myocardial tube. We further identify F-actin-dependent directional cell rearrangement in the right myocardium as a major contributor to LR asymmetric tissue deformation. Our findings demonstrate that heart looping involves dynamic and intrinsic cellular behaviors within the tubular tissue and provide a significantly different viewpoint from current models that are based on LR asymmetry of growth and/or stress at the tube boundaries. Finally, we propose a minimally sufficient model for initial heart looping that is also supported by mechanical simulations.
Highlights
How organs achieve their specific morphologies during development is a major unsolved question in biology
Among the many hypothetical models proposed to date, a prevailing model describes the achievement of heart looping through a combination of ventral bending and rightward rotation based on the observation that the ventral midline becomes the outer curvature of C-shaped heart tube (Manner, 2000; Kirby, 2007; Figure 1C, left)
Previous works that analyzed heart tube morphogenesis were based on limited data due to imaging techniques that allowed, for example, only planar observations of the positions of several landmarks with low resolution (Voronov et al, 2004; Kidokoro et al, 2008)
Summary
How organs achieve their specific morphologies during development is a major unsolved question in biology. Among the many hypothetical models proposed to date (for a review on classical models, see, for example, Shi et al, 2014b), a prevailing model describes the achievement of heart looping through a combination of ventral bending and rightward rotation based on the observation that the ventral midline becomes the outer curvature of C-shaped heart tube (Manner, 2000; Kirby, 2007; Figure 1C, left). Recent high-resolution imaging using zebrafish embryos by Ocana et al, 2017 showed LR asymmetry in cell movement around the posterior pole of the
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