Dynamic interplay of microtubule and actomyosin forces drive tissue extension

Singh A; Thale S; Leibner T; Lamparter L; Ricker A; Nüsse H; Klingauf J; Galic M; Ohlberger M; Matis M

Research article (journal) | Peer reviewed

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.

Details about the publication

JournalNature Communications
Volume15
Issue1
Page range3198-3198
StatusPublished
Release year2024
Language in which the publication is writtenEnglish
DOI: 10.1038/s41467-024-47596-8
Link to the full texthttps://doi.org/10.1038/s41467-024-47596-8
Keywordscell elongation; microtubule and actomyosin forces; phase field model

Authors from the University of Münster

Galic, Milos
Institute of Medical Physics and Biophysics
Klingauf, Jürgen
Institute of Medical Physics and Biophysics
Lamparter, Lucas
Institute of Medical Physics and Biophysics
Leibner, Tobias
Professorship of Applied Mathematics, especially Numerics (Prof. Ohlberger)
Matis, Maja
Institute of Cell Biology
Nüsse, Harald
Institute of Medical Physics and Biophysics
Ohlberger, Mario
Professorship of Applied Mathematics, especially Numerics (Prof. Ohlberger)
Center for Nonlinear Science
Singh, Amrita
Institute of Medical Physics and Biophysics
Thale, Sameedha
Institute of Cell Biology