Defensive slime formation in Pacific hagfish requires Ca2+ and aquaporin mediated swelling of released mucin vesicles

Abstract

Hagfishes defend themselves from fish predators via the rapid deployment of a fibrous slime that adheres to and clogs gills. The slime transforms from a thick glandular exudate to a fully hydrated product in a fraction of a second through a process that involves the swelling and rupture of numerous mucin vesicles. Here we demonstrate that the vesicle membrane plays an important role in regulating the swelling of mucin granules, and provide evidence that the membrane contains proteins that facilitate the movement of ions and water molecules. By exposing isolated mucin vesicles to varying combinations of inorganic ions, organic compounds and membrane channel inhibitors, we found that the majority of hagfish mucin vesicles require Ca 2+ to rupture. We also show that Ca 2+-dependent rupture can be pharmacologically inhibited, which suggests a role for Ca 2+ -activated membrane transporters. We demonstrate that the aquaporin inhibitor mercuric chloride reduces the rate of vesicle swelling by an order of magnitude, which suggests that aquaporins facilitate the influx of water during vesicle deployment. Molecular evidence of two aquaporin homologues expressed in the slime glands further supports this idea. We propose a model of hagfish slime mucin vesicle rupture that involves Ca 2+ -activated transporters and aquaporins, and suggest that the presence of these proteins is an adaptation for increasing the speed of vesicle rupture and, consequently, the speed of the sliming response of hagfishes.

Self-Assembly of Recombinant Hagfish Thread Keratins Amenable to a Strain-Induced α-Helix to β-Sheet Transition

“…10.1021/acs.biomac.5b00552 Biomacromolecules XXXX, XXX, XXX−XXX B the assembly, structure, functional mechanics, and evolution of the keratin gene/protein family.…”

Unravelling hagfish slime

“…Although it is known that flow is required to accelerate unravelling to t dep,50% , 1 s, it is not yet clear whether flow-enhanced ion transport may also contribute to a faster unravelling, in addition to the drag effects. The effects of various salt ions on the swelling and rupture of mucin vesciles have been studied in the past [18,19], but the influence of such ionic effects on the skeins and their deployment is not yet known. If ion transport and chemistry are important, this would modify the F P behaviour and require royalsocietypublishing.org/journal/rsif J. R. Soc.…”

Conservation and phylogenetic stepwise changes of aquaporin (AQP) 4 palmitoylation in vertebrate evolution

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