Sensory transduction shares common features in widely different sensory modalities. The purpose of this article is to examine the similarities and differences in the underlying mechanisms of transduction in the sensory receptor cells for vision, olfaction, and hearing. One of the major differences between the systems relates to the nature of the stimulus. In both the visual and olfactory systems a quantal mechanism of detection is possible, because the absorption of a photon or the binding of an odorant molecule provides an energy change significantly greater than the thermal noise in the receptor molecule. In hearing, on the other hand, the energy of a phonon is far lower, and detection occurs by a "classical" mechanism. For vertebrate photoreceptors and olfactory receptor cells, sensory transduction employs a G protein cascade that is remarkably similar in the two cases, and that is closely homologous to other G protein signaling cascades. For auditory and vestibular hair cells, transduction operates via a mechanism of direct coupling of the stimulus to ion channels, in a manner reminiscent of the direct gating of post-synaptic ion channels in various synaptic mechanisms. The three classes of sensory receptor cell share similarities in their mechanisms of adaptation, and it appears in each case that cytoplasmic calcium concentration plays a major role in adaptation.
Several distinct mechanisms have evolved in the auditory periphery to extract frequency information from a sound. In the mammalian cochlea, a travelling wave on the basilar membrane enhanced by a physiologically vulnerable neuromechanical interaction performs the primary frequency separation. In lizards, tuning is likely to depend on structures in the papilla other than the basilar membrane, and tuning in the auditory nerve is correlated with the length of the stereocilia. In turtles and possibly some bird species, an electrical resonance in the receptor cells is responsible for frequency selectivity. In addition to those organs obviously specialized to detect acoustic stimuli, afferents of the vestibular system can exhibit tuning to low-frequency airborne sounds, despite the absence of mechanical frequency separation by accessory structures. I report here that in the frog saccule, a vestibular organ apparently constructed for the detection of vibratory accelerations, frequency tuning may arise from an electrical resonance intrinsic to the hair cells. The mechanism is similar to that found in turtle and ensures that a stimulus with frequency corresponding to the membrane resonant frequency will produce the largest signal in the cell. This type of tuning may thus be quite widespread. Oscillatory mechanisms have been reported in sensory cells of other modalities in several lower vertebrates, and may even contribute to their sensitivity, although such mechanisms do imply that the signal-to-noise ratio is degraded near threshold.
The mammalian cochlea contains a population of outer hair cells (OHCs) whose electromotility depends on an assembly of 'motor' molecules in the basolateral membrane of the cell. Named 'prestin', the molecule is a member of the SLC26 anion transporter superfamily. We show both directly and indirectly that SLC26A5, rat prestin, takes up hexoses when expressed in several cell lines. Direct measurements of labelled fructose transport into COS-7 cells expessing prestin are reported here. Indirect measurements, using imaging techniques, show that transfected HEK-293 or CHO-K1 cells undergo reversible volume changes when exposed to isosmotic glucose-fructose exchange. The observations are consistent with the sugar transport. A similar transport was observed using a C-terminal green fluorescent protein (GFP)-tagged pendrin (SLC26A4) construct. Cells transfected with GFP alone did not respond to sugars. The data are consistent with fructose being transported by prestin with an apparent K m = 24 mM. From the voltage-dependent capacitance of transfected cells, we estimate that 250 000 prestin molecules were present and hence that the single transport rate is not more than 3000 fructose molecules s _1. Comparison of the transfected cell swelling rates induced by fructose and by osmotic steps indicates that water was cotransported with sugar. We suggest that the structure of SLC26 family members allows them to act as neutral substrate transporters and may explain observed properties of cochlear hair cells. Journal of Physiology METHODS Cell culture and transfectionHuman embryonic kidney (HEK)-293, COS-7 and Chinese hamster ovary (CHO)-K1 cells were grown at 37°C and in 5 % CO 2 in Dulbecco's modified Eagle's medium (DMEM) supplemented with 10 % fetal calf serum. Cells were split weekly when confluent. They were transfected directly in a 75 cm 3 flask (Falcon) using LipofectAmine (Life Technologies, Gaithersburg, MD, USA) according to the manufacturer's recommendations. A plasmid coding for the six transmembrane KCNQ4 potassium channel (a gift from A. Tinker, Department of Clinical Pharmacology, UCL, UK) was used as a control for expression of a membrane protein. Plasmids containing rat prestin (a gift from B. Fakler, Department of Physiology II, University of Freiburg, Germany) and human pendrin (a gift from R. Trembath, Department of Genetics, University of Leicester, UK) cDNAs were both driven by cytomegalovirus promoter. Prestin cDNA was ligated into the eukaryotic expression plasmid vector pBK-CMV (Stratagene) with the GFP-mut3 coding sequence fused to the 3‚ end of the prestin sequence (see Ludwig et al. 2001).
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