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Actin-Driven Nanotopography Promotes Stable Integrin Adhesion Formation in Developing Tissue

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Chen, Tianchi | Huertas Fernández-Espartero, Cecilia | Illand, Abigail | Tsai, Ching-Ting | Yang, Yang | Klapholz, Benjamin | Jouchet, Pierre | Fabre, Mélanie | Rossier, Olivier | Cui, Bianxiao | Lévêque-Fort, Sandrine | Brown, Nicholas, H | Giannone, Grégory

Edité par CCSD ; Nature Publishing Group -

International audience. Morphogenesis requires building stable macromolecular structures from highly dynamic proteins. Muscles are anchored by long-lasting integrin adhesions to resist contractile force. However, the mechanisms governing integrin diffusion, immobilization, and activation within developing tissue remain elusive. Here, we show that actin polymerisation-driven membrane protrusions form nanotopographies resulting in strong adhesions in the Drosophila muscle attachment site. Super-resolution microscopy revealed that integrins assemble adhesive belts around Arp2/3-dependent actin protrusions, forming an invadosomes-like structure with membrane nanotopographies. Single protein tracking showed that, during MAS development, integrins exhibit enhanced molecular immobilization and confinement in diffusion traps formed by these membrane nanotopographies. Actin filaments also display restricted motion and confinement, indicating strong mechanical connection with integrins. Using isolated muscle cells, we show that substrate nanotopography, instead of rigidity, drives adhesion maturation by regulating actin protrusion, integrin diffusion and immobilization. These results point to the existence of a molecular clutch in developing tissue required for the formation of stable adhesions and highlight the importance of geometrical information in cellular and tissue morphogenesis.

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