Microtubule-dependent protein trafficking promotes apical constriction during tissue invagination

Abstract

The formation of an epithelial tube is a fundamental process for organogenesis. Coordination between actomyosin and microtubule (MT) networks is critical for tube formation, but its underlying mechanisms are still unclear. During Drosophila embryonic salivary gland (SG) invagination, Folded gastrulation (Fog)-dependent Rho-associated kinase (Rok) promotes contractile apical myosin formation to drive apical constriction. MTs are also crucial for the effective change in apical area and are required for forming and maintaining apicomedial myosin. Here, we show that MT-dependent intracellular trafficking has a role in regulating apical constriction during SG invagination. Key components involved in protein trafficking, including dynein heavy chain, Rab11 and Nuclear fallout (Nuf), are apically enriched near the invagination pit in a MT-dependent manner during SG invagination. This enrichment is crucial for apical constriction as disruption of the MT networks or intracellular trafficking impairs formation of apicomedial myosin. We show that apical transport of several proteins along MTs, either in a Rab11-dependent or independent manner, mediates clustered apical constriction during SG invagination. Key proteins that are transported include the Fog ligand, the apical determinant protein Crumbs (Crb), the key adherens junction protein E-Cadherin (E-Cad) and the scaffolding protein Bazooka/Par3, and knockdown of these genes in the SG results in apical constriction defects. These results define a role of MT-dependent intracellular trafficking in regulating actomyosin networks and cell junctions to coordinate cell behaviors during tubular organ formation.