On-demand delivery of fibulin-1 protects the basement membrane during cyclic stretching in C. elegans

Basement membrane (BM) extracellular matrices enwrap and structurally support tissues. Whether BMs are uniquely constructed for tissues to undergo repetitive stretching and recoil events is unknown. During C. elegans ovulation, the spermathecal BM stretches ∼1.7-fold and then recoils to its original shape every 20 min to passage hundreds of oocytes. Fluorescence microscopy demonstrated that ovulating oocytes deliver the extracellular matrix protein fibulin-1 (FBL-1) through the spermathecal cell junctions to the BM during stretching, where it forms a dynamic overlapping network with type IV collagen. FBL-1 depletion led to a breakdown in type IV collagen and BM organization, resulting in a more deformable BM and extended spermatheca. Moreover, perturbation to FBL-1 network formation via mutagenesis was sufficient to disrupt tissue recoil and shape. Together, our study identifies an on-demand FBL-1 delivery system that protects the BM network when it is stretched, thereby allowing repeated rounds of tissue expansion and recovery.