Apical actin filament turnover mediated by cyclase-associated protein coordinates non-centrosomal microtubules in epithelium.

Epithelial cells rely on coordinated actin and microtubule cytoskeletons to maintain polarized architecture and function. Although non-centrosomal microtubules are essential for polarized trafficking and epithelial organization, how local actin turnover contributes to their organization in vivo remains poorly understood. Using the Drosophila follicular epithelium, we show that loss of Cyclase-Associated Protein (CAP), a conserved regulator of actin turnover, causes stabilization and accumulation of actin at the apical cortex. Rescue experiments identify the CARP domain as the principal CAP activity required to prevent apical actin accumulation, consistent with a requirement for efficient actin monomer recycling. Excess apical actin is accompanied by local depletion of apical microtubules and mislocalization of the actin-microtubule crosslinker Shot, while apical Patronin localization and microtubule polarity remain intact. Acute disruption of the accumulated actin network partially restores both microtubules and Shot to the apical domain, indicating that local actin turnover regulates microtubule positioning and cortical engagement. These cytoskeletal defects are associated with impaired polarized trafficking, defective microvillus biogenesis and nuclear mispositioning consistent with known roles of non-centrosomal microtubules. Together, our findings identify CAP-dependent actin turnover as a spatial regulator of non-centrosomal microtubule organization and reveal how local actin dynamics contribute to epithelial architecture and function in vivo.