Transient opening of tricellular vertices controls paracellular transport through the follicle epithelium during Drosophila oogenesis

Dev Cell. 2021 Apr 19;56(8):1083-1099.e5. doi: 10.1016/j.devcel.2021.03.021. Epub 2021 Apr 7.

Abstract

Paracellular permeability is regulated to allow solute transport or cell migration across epithelial or endothelial barriers. However, how cell-cell junction dynamics controls paracellular permeability is poorly understood. Here, we describe patency, a developmentally regulated process in Drosophila oogenesis, during which cell vertices in the follicular epithelium open transiently to allow paracellular transport of yolk proteins for uptake by the oocyte. We show that the sequential removal of E-cadherin, N-cadherin, NCAM/Fasciclin 2, and Sidekick from vertices precedes their basal-to-apical opening, while the subsequent assembly of tricellular occluding junctions marks the termination of patency and seals the paracellular barrier. E-cadherin-based adhesion is required to limit paracellular channel size, whereas stabilized adherens junctions, prolonged NCAM/Fasciclin 2 expression, blocked endocytosis, or increased actomyosin contractility prevent patency. Our findings reveal a key role of cell vertices as gateways controlling paracellular transport and demonstrate that dynamic regulation of adhesion and actomyosin contractility at vertices governs epithelial barrier properties.

Keywords: Drosophila; cell adhesion; cell-cell junction; endocytosis; epithelium; junction remodeling; oogenesis; paracellular transport; tricellular junction; vertex.