Activated l-type calcium channels inhibit chemosensitized nematocyst discharge from sea anemone tentacles

Abstract

Because in vivo nematocyst discharge requires extracellular Ca2+, Ca2+ channels have been suspected to be involved; but their identity and role have not been revealed. The majority of nematocysts that discharge from sea anemone tentacles are under the control of sensitizing  hemoreceptors for N-acetylated sugars (e.g., N-acetylneuraminic acid). Activated chemoreceptors predispose contact-sensitive mechanoreceptors to trigger discharge. We show that activating L-type Ca2+ channels inhibits N-acetylneuraminic acidsensitized discharge, contrary to a previous suggestion. In addition, inhibiting L-type channels increases sensitivity to N-acetylneuraminic acid. Specifically, we showthat the L-type Ca2+ channel activator (2)-Bay K 8644 dose-dependently inhibits N-acetylneuraminic acid-sensitized discharge, as does raising ambient Ca2+ levels.We also showthat lowering extracellular Ca2+ levels or adding any of several selective and chemically distinct L-type Ca2+ channel blockers, including dihydropyridines, dose-dependently increases N-acetylneuraminic acid sensitivity and broadens the dynamic range of Nacetylneuraminic acid sensitization. Consistent with these functional findings, Aiptasia pallida expresses an L-type Ca2+ channel α subunit transcript that encodes a conserved dihydropyridine-binding site. Phylogenetic analysis confirms a close relationship of the Aiptasia Ca2+ channel a subunit sequence between anemones, anthozoans, and cnidarians that extends into protostomal and deuterostomal bilaterians. We conclude that L-type Ca2+ channel activity modulates Nacetylneuraminic acid-sensitized nematocyst discharge in a push-pull manner depending on channel activity state. Our findings suggest that L-type channel activation promotes chemosensory desensitization, and we predict that Nacetylneuraminic acid chemoreceptor signaling will activate L-type channels.