Calcium permeation of the turtle hair cell mechanotransducer channel and its relation to the composition of endolymph

J Physiol. 1998 Jan 1;506 ( Pt 1)(Pt 1):159-73. doi: 10.1111/j.1469-7793.1998.159bx.x.

Abstract

1. Recordings of mechanoelectrical transducer currents were combined with calcium imaging of hair bundles in turtle auditory hair cells located near the high-frequency end of the cochlea. The external face of the hair bundles was perfused with a range of Ca2+ concentrations to study the quantitative relationship between Ca2+ influx and transducer adaptation. 2. With Na+ as the monovalent ion, the peak amplitude of the transducer current decreased monotonically as the external [Ca2+] was raised from 25 microns to 20 mm. When Na+ was replaced with the impermeant Tris the transducer current increased with external [Ca2+]. These results indicate that Ca2+ can both permeate and block the transducer channels. The Ca2+ concentration for half-block of the monovalent current was 1 mm. 3. To quantify the Ca2+ influx, the fraction of transducer current carried by Ca2+ was measured using the change in bundle fluorescence in cells loaded with 1 mm Calcium Green-1. The fluorescence change was calibrated by substituting an impermeable monovalent ion to render Ca2+ the sole charge carrier. 4. In the presence of Na+, the fractional Ca2+ current was approximately 10% in 50 microns Ca2+, a concentration similar to that in endolymph, which bathes the hair bundles in vivo. The amount of Ca2+ entering was dependent on the identity of the monovalent ion, and was larger with K+, suggesting that the transducer channel is a multi-ion pore. 5. Over a range of ionic conditions, the rate of transducer adaptation was proportional to Ca2+ influx indicating that adaptation is driven by a rise in intracellular [Ca2+]. 6. Shifts in the current-displacement function along the displacement axis in different external Ca2+ concentrations were predictable from variation in the resting Ca2+ influx. We suggest that changes in the resting open probability of the transducer channels adjust the entry of Ca2+ to keep its concentration constant at an internal site. 7. The results demonstrate that endolymph containing high K+, 50 microns Ca2+ and low Mg2+ concentrations, maximizes the transducer current while still allowing sufficient Ca2+ entry to drive adaptation. The hair cell mechanotransducer channel, in its permeation and block by Ca2+, shows behaviour similar to the voltage-gated Ca2+ channel and the cyclic nucleotide-gated channel.

Publication types

  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Adaptation, Physiological
  • Animals
  • Calcium / metabolism*
  • Cochlea / physiology
  • Electric Stimulation
  • Endolymph / metabolism*
  • Hair Cells, Auditory / metabolism*
  • In Vitro Techniques
  • Ion Channels / metabolism*
  • Magnesium / metabolism
  • Mechanoreceptors / metabolism*
  • Microelectrodes
  • Potassium / metabolism
  • Rats
  • Signal Transduction / physiology*
  • Sodium / physiology
  • Spectrometry, Fluorescence
  • Turtles / physiology*

Substances

  • Ion Channels
  • Sodium
  • Magnesium
  • Potassium
  • Calcium