Olfactory response termination involves Ca2+-ATPase in vertebrate olfactory receptor neuron cilia

Abstract

In vertebrate olfactory receptor neurons (ORNs), odorant-induced activation of the transduction cascade culminates in production of cyclic AMP, which opens cyclic nucleotide-gated channels in the ciliary membrane enabling Ca(2+) influx. The ensuing elevation of the intraciliary Ca(2+) concentration opens Ca(2+)-activated Cl(-) channels, which mediate an excitatory Cl(-) efflux from the cilia. In order for the response to terminate, the Cl(-) channel must close, which requires that the intraciliary Ca(2+) concentration return to basal levels. Hitherto, the extrusion of Ca(2+) from the cilia has been thought to depend principally on a Na(+)-Ca(2+) exchanger. In this study, we show using simultaneous suction pipette recording and Ca(2+)-sensitive dye fluorescence measurements that in fire salamander ORNs, withdrawal of external Na(+) from the solution bathing the cilia, which incapacitates Na(+)-Ca(2+)exchange, has only a modest effect on the recovery of the electrical response and the accompanying decay of intraciliary Ca(2+) concentration. In contrast, exposure of the cilia to vanadate or carboxyeosin, a manipulation designed to block Ca(2+)-ATPase, has a substantial effect on response recovery kinetics. Therefore, we conclude that Ca(2+)-ATPase contributes to Ca(2+) extrusion in ORNs, and that Na(+)-Ca(2+)exchange makes only a modest contribution to Ca(2+) homeostasis in this species.