Cell deformations generated by stochastic actomyosin waves drive in vivo random-walk swimming migration.

Amoeboid cell migration drives many developmental and disease-related processes, including immune responses and cancer metastasis. Swimming migration is a subtype of amoeboid migration that is observed in cells in suspension ex vivo. However, the mechanism underlying swimming migration in vivo is unknown. Using Drosophila fat body cells (FBCs) as a model, we show that FBCs actively swim to patrol the pupa by random walk. Their migration is powered through actomyosin waves that exert compressive forces as they travel to the cell rear, causing cell deformations. Unlike in other types of amoeboid migration, Rho1 (the Drosophila orthologue of RhoA), Cdc42 and Rac1 are all required for regulation of formin-driven actin polymerization during FBC migration. We find that Rho1 at the cell rear induces actomyosin contractions via Rho kinase and myosin II. We show that contractile actin waves display a stochastic behaviour, inducing either cell elongation or rounding, suggesting that non-reciprocal cell deformations drive locomotion. Importantly, our work in a physiological system reveals that stochastic actomyosin waves promote random-walk swimming migration to enable fast, long-range cell dispersal. We propose that this individualist migration behaviour collectively allows patrolling of the pupal body.