An endosome-associated actin network involved in directed apical plasma membrane growth

Abstract

The subcellular membrane-trafficking system plays many roles in cell growth and morphogenesis, from bulk membrane provision to targeted delivery of membrane proteins and other cargos. In tracheal terminal cells of the Drosophila respiratory system, endocytosis and trafficking through late endosomes balances membrane delivery between the basal plasma membrane and the apical membrane that forms a subcellular tube, but it has been unclear how the direction of growth of the subcellular tube with the overall growth of the cell is coordinated. We show here that endosomes are involved in this process as coordinators of F-actin. Actin assembles around late endocytic vesicles in the growth cone of the cell, reaching from the tip of the subcellular tube to the leading filopodia of the basal membrane. Preventing actin nucleation at late endosomes disturbs the directionality of tube growth, uncoupling it from the direction of cell elongation. Severing actin in this area affects tube integrity. Our findings show a new role for late endosomes in directing cell morphogenesis by organizing actin, in addition to their known role in membrane and protein trafficking.