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bioRxiv · 10.1101/2020.09.22.304451

Degenerating Drosophila Larval Epidermal Cells Drive Thorax Closure

Abstract

Adult thorax formation in Drosophila begins during pre-pupal development by fusion of its two contralateral progenitor halves, the heminotal epithelia (HE). HEs migrate and replace an underlying cell layer of thoracic larval epidermal cells (LECs) during a morphogenetic process called thorax closure. The LEC layer has so far been proposed to be a passive substrate over which HEs migrate before their zipping. By contrast, here we show that the pull forces generated within the LEC layer drive HE migration. During thorax closure, the LECs display actomyosin-mediated contraction, via enrichment of non-muscle myosin-II and actin, besides squamous-to-pseudostratified columnar epithelial transition and tissue shrinkage. This shrinkage of the LEC layer is further accompanied by cell extrusion and death, that prevent overcrowding of LECs, thereby promoting further shrinkage. The pull forces thus generated by the shrinking LEC layer are then relayed to the HEs by their mutual adhesions via {beta}PS1 (Mys) and PS3 (Scb) integrins. Suppression of cell death in the LEC layer by a gain of p35 leads to cell overcrowding, which impedes HE migration and zipping. Further, knockdown of sqh, the light chain of non-muscle myosin II, in LECs or integrins (mys or scb) in either the LEC layer or in the HEs, or both abrogate thorax closure. Mathematical modeling also reveals the biophysical underpinnings of the forces that drive this tissue closure process wherein a degenerating LEC layer mediates its succession by the future adult primodia. These essential principles of thorax closure appear ancient in origin and recur in multiple morphogenetic contexts and tissue repair.

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BibTeXRIS

Athilingam, T., Parihar, S. S., Bhattacharya, R., Rizvi, M. S., Kumar, A., Sinha, P.. 2020-09-22. Degenerating Drosophila Larval Epidermal Cells Drive Thorax Closure. https://doi.org/10.1101/2020.09.22.304451

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