Dynamic interplay of microtubule and actomyosin forces drive tissue extension

Amrita Singh, Sameedha Thale, Tobias Leibner, Lucas Lamparter, Andrea Ricker, Harald Nüsse, Jürgen Klingauf, Milos Galic, Mario Ohlberger and Maja Matis ()
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Amrita Singh: University of Münster
Sameedha Thale: University of Münster
Tobias Leibner: University of Münster
Lucas Lamparter: University of Münster
Andrea Ricker: University of Münster
Harald Nüsse: University of Münster
Jürgen Klingauf: University of Münster
Milos Galic: University of Münster
Mario Ohlberger: University of Münster
Maja Matis: University of Münster

Nature Communications, 2024, vol. 15, issue 1, 1-14

Abstract: Abstract In order to shape a tissue, individual cell-based mechanical forces have to be integrated into a global force pattern. Over the last decades, the importance of actomyosin contractile arrays, which are the key constituents of various morphogenetic processes, has been established for many tissues. Recent studies have demonstrated that the microtubule cytoskeleton mediates folding and elongation of the epithelial sheet during Drosophila morphogenesis, placing microtubule mechanics on par with actin-based processes. While these studies establish the importance of both cytoskeletal systems during cell and tissue rearrangements, a mechanistic understanding of their functional hierarchy is currently missing. Here, we dissect the individual roles of these two key generators of mechanical forces during epithelium elongation in the developing Drosophila wing. We show that wing extension, which entails columnar-to-cuboidal cell shape remodeling in a cell-autonomous manner, is driven by anisotropic cell expansion caused by the remodeling of the microtubule cytoskeleton from apico-basal to planarly polarized. Importantly, cell and tissue elongation is not associated with Myosin activity. Instead, Myosin II exhibits a homeostatic role, as actomyosin contraction balances polarized microtubule-based forces to determine the final cell shape. Using a reductionist model, we confirm that pairing microtubule and actomyosin-based forces is sufficient to recapitulate cell elongation and the final cell shape. These results support a hierarchical mechanism whereby microtubule-based forces in some epithelial systems prime actomyosin-generated forces.

Date: 2024
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DOI: 10.1038/s41467-024-47596-8

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