Local optogenetic NMYII activation within the zebrafish neural rod results in long-range, asymmetric force propagation

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Abstract

How do cellular forces propagate through tissue to allow large-scale morphogenetic events? To investigate this question, we used an in vivo optogenetic approach to reversibly manipulate actomyosin contractility at depth within the developing zebrafish neural rod. Contractility was induced along the lateral cortices of a small patch of developing neural epithelial progenitor cells, resulting in a shortening of these cells along their mediolateral axis. Imaging the immediate response of surrounding tissue uncovered a long-range, tangential, and elastic tissue deformation along the anterior-posterior axis. Unexpectedly, this was highly asymmetric, propagating in either the anterior or the posterior direction in response to local gradients in optogenetic activation. The degree of epithelialisation did not have a significant impact on the extent of force propagation via lateral cortices. We also uncovered a dynamic oscillatory expansion and contraction of the tissue along the anterior-posterior axis, with wavelength within the range of rhombomere length. Together, this study shows dynamic and wave-like propagation of force along the anterior-posterior axis. It also suggests that cell generated forces are actively propagated over long distances within the tissue, and that local anisotropies in tissue organisation and contractility are sufficient to drive directional force propagation.
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Abstract How do cellular forces propagate through tissue to allow large-scale morphogenetic events? To investigate this question, we used an in vivo optogenetic approach to reversibly manipulate actomyosin contractility at depth within the developing zebrafish neural rod. Contractility was induced along the lateral cortices of a small patch of developing neural epithelial progenitor cells, resulting in a shortening of these cells along their mediolateral axis. Imaging the immediate response of surrounding tissue uncovered a long-range, tangential, and elastic tissue deformation along the anterior-posterior axis. Unexpectedly, this was highly asymmetric, propagating in either the anterior or the posterior direction in response to local gradients in optogenetic activation. The degree of epithelialisation did not have a significant impact on the extent of force propagation via lateral cortices. We also uncovered a dynamic oscillatory expansion and contraction of the tissue along the anterior-posterior axis, with wavelength within the range of rhombomere length. Together, this study shows dynamic and wave-like propagation of force along the anterior-posterior axis. It also suggests that cell generated forces are actively propagated over long distances within the tissue, and that local anisotropies in tissue organisation and contractility are sufficient to drive directional force propagation. Competing Interest Statement The authors have declared no competing interest. Footnotes Correction to definition and decomposition of strain rate tensor in Methods Addition to Acknowledgements

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License: CC-BY-NC-ND-4.0