Apical actin filament turnover mediated by cyclase-associated protein is required for organization of non-centrosomal microtubules in epithelium

Abstract

Epithelial cells rely on the precise coordination of actin and microtubule cytoskeletons to maintain their polarized structure and function. Within polarized epithelial cells, microtubules form longitudinal non-centrosomal arrays essential for organelle positioning and facilitate directional cargo trafficking whereas the apical actin cytoskeleton supports cell shape and tissue architecture. This study investigates the interplay between disrupted apical actin dynamics and microtubule organization in vivo within Drosophila epithelial tissue. Loss of actin turnover promoting Cyclase-Associated Protein (CAP) results in the excessive accumulation of stable actin structures at the apical cortex. We show that accumulated apical actin sterically excludes microtubules and membrane-bound vesicles. Consequently, non-centrosomal microtubule-dependent processes are impaired, leading to nuclear mispositioning, disrupted apical cargo transport, and defective microvilli formation in CAP mutant cells. Our findings highlight that dense apical actin, due to impaired actin turnover catalyzed by CAP, disrupts the apical organization of non-centrosomal microtubules. This suggests that spatially regulated actin filament turnover is important for microtubule organization and sustaining the polarized functions of epithelial tissues.