DAAM mediates the assembly of long-lived, treadmilling stress fibers in collectively migrating epithelial cells in Drosophila

Abstract

Stress fibers (SFs) are actomyosin bundles commonly found in individually migrating cells in culture. However, whether and how cells use SFs to migrate in vivo or collectively is largely unknown. Studying the collective migration of the follicular epithelial cells in Drosophila, we found that the SFs in these cells show a novel treadmilling behavior that allows them to persist as the cells migrate over multiple cell lengths. Treadmilling SFs grow at their fronts by adding new integrin-based adhesions and actomyosin segments over time. This causes the SFs to have many internal adhesions along their lengths, instead of adhesions only at the ends. The front-forming adhesions remain stationary relative to the substrate and typically disassemble as the cell rear approaches. By contrast, a different type of adhesion forms at the terminus of the SF that slides with the trailing edge of the cell as the actomyosin ahead of it shortens. We further show that SF treadmilling depends on cell movement and identify a developmental switch in the formins that mediate SF assembly, with DAAM acting during migratory stages and Diaphanous acting during post-migratory stages. We propose that treadmilling SFs keep each cell on a linear trajectory, thereby promoting the collective motility required for epithelial migration.

The emergence of spontaneous coordinated epithelial rotation on cylindrical curved surfaces

“…A recent study reveals the existence of immobile actin SFs in Drosophila and their role in promoting parallel cell trajectories during collective rotational migration ( 18 ). The authors propose a treadmilling behavior that enables SFs to persist in a moving epithelium.…”

“…In previous works using 3D epithelial acini, molecular analysis reveals a relationship between coordinated rotation and actin polymerization, cell-cell adhesion, and cell apical-basal polarity ( 5 , 8 ). In addition, during Drosophila oogenesis ( 1 – 3 ), circumferentially aligned actin filaments lining the inner surface of the follicular epithelium are found to aid the persisting azimuthal rotation ( 1 , 2 , 18 ). In parallel, this global rotation of follicle cells is coupled to the maintenance of actin stress fiber (SF) alignment, lamellipodial protrusions, and remodeling of the extracellular matrix (ECM) ( 2 ).…”