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

Forschungsartikel (Zeitschrift) | Peer reviewed

Zusammenfassung

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 zur Publikation

FachzeitschriftNature Communications
Jahrgang / Bandnr. / Volume15
Ausgabe / Heftnr. / Issue1
Seitenbereich3198-3198
StatusVeröffentlicht
Veröffentlichungsjahr2024
Sprache, in der die Publikation verfasst istEnglisch
DOI: 10.1038/s41467-024-47596-8
Link zum Volltexthttps://doi.org/10.1038/s41467-024-47596-8
Stichwörtercell elongation; microtubule and actomyosin forces; phase field model

Autor*innen der Universität Münster

Galic, Milos
Institut für Medizinische Physik und Biophysik
Klingauf, Jürgen
Institut für Medizinische Physik und Biophysik
Lamparter, Lucas
Institut für Medizinische Physik und Biophysik
Leibner, Tobias
Professur für Angewandte Mathematik, insbesondere Numerik (Prof. Ohlberger)
Matis, Maja
Institut für Zellbiologie
Nüsse, Harald
Institut für Medizinische Physik und Biophysik
Ohlberger, Mario
Professur für Angewandte Mathematik, insbesondere Numerik (Prof. Ohlberger)
Center for Nonlinear Science (CeNoS)
Singh, Amrita
Institut für Medizinische Physik und Biophysik
Thale, Sameedha
Institut für Zellbiologie