Gap junctional communication in the vibration-sensitive response of sea anemones

Although gap junctions occur in auditory and vestibular systems, their function is unclear. Here we present evidence for gap junctional communication in transmitting mechanosensory signals in a sea anemone model system. Hair bundles on anemone tentacles are vibration-sensitive mechanoreceptors that regulate discharge of nematocyst from effector cells. We find that vibration-dependent nematocyst discharge is selectively and reversibly blocked by the gap junction uncouplers, heptanol and arachidonic acid. Epidermal cells within excised tentacles exhibit a low level of dye coupling which is significantly enhanced upon deflection of overlying hair bundles. Dye coupling is inhibited both by gap junction uncouplers and by agents that interfere with mechanotransduction, including streptomycin and elastase. Electrophysiological data suggest gap junctional communication between cells giving rise to different hair bundles. When hair bundles are stimulated with a sweep of vibrations, individual cells show responses to five to eight frequencies. The number of responsive frequencies is reduced to one or two by heptanol and essentially abolished with streptomycin treatment. Immunoreactivity to the gap junction protein, connexin 43, is abundant in the tentacle epidermis and localized to membranes at junctions between several cell types. Small areas of close membrane apposition are observed between these cell types with intermembrane clefts of 4–7 nm. Of the several membrane proteins isolated from tentacles, immunoreactivity to connexin 43 is observed in a single band with an apparent molecular weight of approximately 46 kDa.