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The Journal of Neuroscience, September 8, 2004, 24(36):7931-7938; doi:10.1523/JNEUROSCI.2115-04.2004

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Cellular/Molecular
Chloride Accumulation in Mammalian Olfactory Sensory Neurons

Hiroshi Kaneko, Ilva Putzier, Stephan Frings, U. Benjamin Kaupp, and Thomas Gensch

Institute for Biological Information Processing (IBI-1), Forschungszentrum Jülich, 52425 Jülich, Germany

The generation of an excitatory receptor current in mammalian olfactory sensory neurons (OSNs) involves the sequential activation of two distinct types of ion channels: cAMP-gated Ca²⁺-permeable cation channels and Ca²⁺-gated Cl^- channels, which conduct a depolarizing Cl^- efflux. This unusual transduction mechanism requires an outward-directed driving force for Cl^-, established by active accumulation of Cl^- within the lumen of the sensory cilia. We used two-photon fluorescence lifetime imaging microscopy of the Cl^--sensitive dye 6-methoxy-quinolyl acetoethyl ester to measure the intracellular Cl^- concentration in dendritic knobs of OSNs from mice and rats. We found a uniform intracellular Cl^- concentration in the range of 40-50 mM, which is indicative of active Cl^- accumulation. Functional assays and PCR experiments revealed that NKCC1-mediated Cl^- uptake through the apical membrane counteracts Cl^- depletion in the sensory cilia, and thus maintains the responsiveness of OSNs to odor stimulation. To permit Cl^- accumulation, OSNs avoid the "chloride switch": they do not express KCC2, the main Cl^- extrusion cotransporter operating in neurons of the adult CNS. Cl^- accumulation provides OSNs with the driving force for the depolarizing Cl^- current that is the basis of the low-noise receptor current in these neurons.

Key words: olfaction; calcium-activated chloride channels; fluorescence lifetime imaging; chloride homeostasis; sensory transduction; chloride cotransport

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Received June 1, 2004; revised July 1, 2004; accepted July 18, 2004.

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