Kinesin-3 and kinesin-1 motors direct basement membrane protein secretion to a basal sub-region of the basolateral plasma membrane in epithelial cells

Abstract

SUMMARYBasement membranes (BMs) are sheet-like extracellular matrices that line the basal surfaces of all epithelia. Since BM proteins form networks, they likely need to be secreted near the basal surface. However, the location of their secretion site and how it is selected are unknown. Working in the Drosophila follicular epithelium, we identified two kinesins essential for normal BM formation. Our data suggest the two kinesins work together to transport Rab10+ BM protein-filled secretory vesicles towards the basal surface along the polarized microtubule array common to epithelia. This kinesin transport biases BM protein secretion basally. When kinesins are depleted, BM proteins are mis-secreted to more apical regions of the lateral membrane, creating ectopic BM protein networks between cells that disrupt cell movements and tissue architecture. These results introduce a new transport step in the BM protein secretion pathway and highlight the importance of controlling the sub-cellular exocytic site of network-forming proteins.HighlightsA kinesin-3 and a kinesin-1 are required for normal basement membrane (BM) assemblyKinesins move Rab10+ BM secretory vesicles basally on polarized microtubule arraysTransport biases BM exocytosis to basal subregions of the basolateral membraneLoss of kinesins creates ectopic BM networks that disrupt tissue architecture

Apical–basal polarity and the control of epithelial form and function

“…Epithelial cells typically contain apical-basal arrays of microtubules that play important roles in nuclear positioning, the dynein-dependent transport of exocytic cargoes to the apical side of the cell and the kinesin-dependent transport of basal cargoes 158,159 . In polarising cells, microtubules are initially nucleated by the centrosome.…”

An online gathering about the latest on molecular membrane biology

“…David Murray (University of Dundee, United Kingdom) presented exciting unpublished data about the functional characterization of the exocyst tethering complex and its cross talk with phosphoinositide signaling. The session was closed by Allison Zajac (University of Chicago, USA), whose latest preprint ( 10 ) highlights the role of Kinesin-3 and -1 motors in basolateral secretion in epithelial cells. The first day wrapped up with a session focused on mitochondria/peroxisomal membranes packed with excellent unpublished findings.…”