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Huycke, Tyler R.; Häkkinen, Teemu J.; Miyazaki, Hikaru; Srivastava, Vasudha; Barruet, Emilie; McGinnis, Christopher S.; Kalantari, Ali; Cornwall-Scoones, Jake; Vaka, Dedeepya; Zhu, Qin; Jo, Hyunil; Oria, Roger; Weaver, Valerie M.; DeGrado, William F.; Thomson, Matt; Garikipati, Krishna; Boffelli, Dario; Klein, Ophir D.; Gartner, Zev J.
Cell, 06/2024, Volume: 187, Issue: 12Journal Article
Tissue folds are structural motifs critical to organ function. In the intestine, bending of a flat epithelium into a periodic pattern of folds gives rise to villi, finger-like protrusions that enable nutrient absorption. However, the molecular and mechanical processes driving villus morphogenesis remain unclear. Here, we identify an active mechanical mechanism that simultaneously patterns and folds the intestinal epithelium to initiate villus formation. At the cellular level, we find that PDGFRA+ subepithelial mesenchymal cells generate myosin II-dependent forces sufficient to produce patterned curvature in neighboring tissue interfaces. This symmetry-breaking process requires altered cell and extracellular matrix interactions that are enabled by matrix metalloproteinase-mediated tissue fluidization. Computational models, together with in vitro and in vivo experiments, revealed that these cellular features manifest at the tissue level as differences in interfacial tensions that promote mesenchymal aggregation and interface bending through a process analogous to the active dewetting of a thin liquid film. Display omitted •Mesenchymal aggregates generate forces that fold the mammalian intestinal epithelium•Active and fluid-like properties of aggregates program tissue geometry and pattern•Matrix metalloproteinases fluidize the subepithelial mesenchyme to initiate aggregation•Mesenchymal patterning conceptually resembles water dewetting from a hydrophobic surface Subepithelial mesenchyme behaves like a dewetting fluid to pattern and fold the intestinal epithelium, initiating the formation of villi.
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