Skip to main content
NCBI home page
Biophysical Journal logoLink to Biophysical Journal
. 2000 Mar;78(3):1240–1254. doi: 10.1016/S0006-3495(00)76681-1

Calcium currents in hair cells isolated from semicircular canals of the frog.

M Martini 1, M L Rossi 1, G Rubbini 1, G Rispoli 1
PMCID: PMC1300726  PMID: 10692313

Abstract

L-type and R-type Ca(2+) currents were detected in frog semicircular canal hair cells. The former was noninactivating and nifedipine-sensitive (5 microM); the latter, partially inactivated, was resistant to omega-conotoxin GVIA (5 microM), omega-conotoxin MVIIC (5 microM), and omega-agatoxin IVA (0.4 microM), but was sensitive to mibefradil (10 microM). Both currents were sensitive to Ni(2+) and Cd(2+) (>10 microM). In some cells the L-type current amplitude increased almost twofold upon repetitive stimulation, whereas the R-type current remained unaffected. Eventually, run-down occurred for both currents, but was prevented by the protease inhibitor calpastatin. The R-type current peak component ran down first, without changing its plateau, suggesting that two channel types generate the R-type current. This peak component appeared at -40 mV, reached a maximal value at -30 mV, and became undetectable for voltages > or =0 mV, suggestive of a novel transient current: its inactivation was indeed reversibly removed when Ba(2+) was the charge carrier. The L-type current and the R-type current plateau were appreciable at -60 mV and peaked at -20 mV: the former current did not reverse for voltages up to +60 mV, the latter reversed between +30 and +60 mV due to an outward Cs(+) current flowing through the same Ca(2+) channel. The physiological role of these currents on hair cell function is discussed.

Full Text

The Full Text of this article is available as a PDF (235.3 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Armstrong C. E., Roberts W. M. Electrical properties of frog saccular hair cells: distortion by enzymatic dissociation. J Neurosci. 1998 Apr 15;18(8):2962–2973. doi: 10.1523/JNEUROSCI.18-08-02962.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Block B. M., Jones S. W. Delayed rectifier current of bullfrog sympathetic neurons: ion-ion competition, asymmetrical block and effects of ions on gating. J Physiol. 1997 Mar 1;499(Pt 2):403–416. doi: 10.1113/jphysiol.1997.sp021937. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Carbone E., Lux H. D. A low voltage-activated, fully inactivating Ca channel in vertebrate sensory neurones. Nature. 1984 Aug 9;310(5977):501–502. doi: 10.1038/310501a0. [DOI] [PubMed] [Google Scholar]
  4. Chabbert C., Canitrot Y., Sans A., Lehouelleur J. Calcium homeostasis in guinea pig type-I vestibular hair cell: possible involvement of an Na(+)-Ca2+ exchanger. Hear Res. 1995 Sep;89(1-2):101–108. doi: 10.1016/0378-5955(95)00126-2. [DOI] [PubMed] [Google Scholar]
  5. Dolphin A. C. Facilitation of Ca2+ current in excitable cells. Trends Neurosci. 1996 Jan;19(1):35–43. doi: 10.1016/0166-2236(96)81865-0. [DOI] [PubMed] [Google Scholar]
  6. Dunlap K., Luebke J. I., Turner T. J. Exocytotic Ca2+ channels in mammalian central neurons. Trends Neurosci. 1995 Feb;18(2):89–98. [PubMed] [Google Scholar]
  7. Emanuel K., Mackiewicz U., Pytkowski B., Lewartowski B. Effects of mibefradil, a blocker of T-type Ca2+ channels, in single myocytes and intact muscle of guinea-pig heart. J Physiol Pharmacol. 1998 Dec;49(4):577–590. [PubMed] [Google Scholar]
  8. Fuchs P. A., Evans M. G., Murrow B. W. Calcium currents in hair cells isolated from the cochlea of the chick. J Physiol. 1990 Oct;429:553–568. doi: 10.1113/jphysiol.1990.sp018272. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Fuchs P. A., Evans M. G. Potassium currents in hair cells isolated from the cochlea of the chick. J Physiol. 1990 Oct;429:529–551. doi: 10.1113/jphysiol.1990.sp018271. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Gioglio L., Russo G., Marcotti W., Prigioni I. Localization of Ca-ATPase in frog crista ampullaris. Neuroreport. 1998 May 11;9(7):1309–1312. doi: 10.1097/00001756-199805110-00010. [DOI] [PubMed] [Google Scholar]
  11. Green G. E., Khan K. M., Beisel D. W., Drescher M. J., Hatfield J. S., Drescher D. G. Calcium channel subunits in the mouse cochlea. J Neurochem. 1996 Jul;67(1):37–45. doi: 10.1046/j.1471-4159.1996.67010037.x. [DOI] [PubMed] [Google Scholar]
  12. Guth P. S., Fermin C. D., Pantoja M., Edwards R., Norris C. Hair cells of different shapes and their placement along the frog crista ampullaris. Hear Res. 1994 Feb;73(1):109–115. doi: 10.1016/0378-5955(94)90288-7. [DOI] [PubMed] [Google Scholar]
  13. Hamill O. P., Marty A., Neher E., Sakmann B., Sigworth F. J. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch. 1981 Aug;391(2):85–100. doi: 10.1007/BF00656997. [DOI] [PubMed] [Google Scholar]
  14. Housley G. D., Norris C. H., Guth P. S. Electrophysiological properties and morphology of hair cells isolated from the semicircular canal of the frog. Hear Res. 1989 Apr;38(3):259–276. doi: 10.1016/0378-5955(89)90070-1. [DOI] [PubMed] [Google Scholar]
  15. Hudspeth A. J., Gillespie P. G. Pulling springs to tune transduction: adaptation by hair cells. Neuron. 1994 Jan;12(1):1–9. doi: 10.1016/0896-6273(94)90147-3. [DOI] [PubMed] [Google Scholar]
  16. Hudspeth A. J., Lewis R. S. Kinetic analysis of voltage- and ion-dependent conductances in saccular hair cells of the bull-frog, Rana catesbeiana. J Physiol. 1988 Jun;400:237–274. doi: 10.1113/jphysiol.1988.sp017119. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Huguenard J. R. Low-voltage-activated (T-type) calcium-channel genes identified. Trends Neurosci. 1998 Nov;21(11):451–452. doi: 10.1016/s0166-2236(98)01331-9. [DOI] [PubMed] [Google Scholar]
  18. Kameyama A., Yazawa K., Kaibara M., Ozono K., Kameyama M. Run-down of the cardiac Ca2+ channel: characterization and restoration of channel activity by cytoplasmic factors. Pflugers Arch. 1997 Mar;433(5):547–556. doi: 10.1007/s004240050313. [DOI] [PubMed] [Google Scholar]
  19. Kameyama M., Kameyama A., Takano E., Maki M. Run-down of the cardiac L-type Ca2+ channel: partial restoration of channel activity in cell-free patches by calpastatin. Pflugers Arch. 1998 Feb;435(3):344–349. doi: 10.1007/s004240050521. [DOI] [PubMed] [Google Scholar]
  20. Lang D. G., Correia M. J. Studies of solitary semicircular canal hair cells in the adult pigeon. II. Voltage-dependent ionic conductances. J Neurophysiol. 1989 Oct;62(4):935–945. doi: 10.1152/jn.1989.62.4.935. [DOI] [PubMed] [Google Scholar]
  21. Masetto S., Russo G., Prigioni I. Differential expression of potassium currents by hair cells in thin slices of frog crista ampullaris. J Neurophysiol. 1994 Jul;72(1):443–455. doi: 10.1152/jn.1994.72.1.443. [DOI] [PubMed] [Google Scholar]
  22. McCleskey E. W. Calcium channels: cellular roles and molecular mechanisms. Curr Opin Neurobiol. 1994 Jun;4(3):304–312. doi: 10.1016/0959-4388(94)90090-6. [DOI] [PubMed] [Google Scholar]
  23. Mironov S. L., Lux H. D. Calmodulin antagonists and protein phosphatase inhibitor okadaic acid fasten the 'run-up' of high-voltage activated calcium current in rat hippocampal neurones. Neurosci Lett. 1991 Dec 9;133(2):175–178. doi: 10.1016/0304-3940(91)90563-9. [DOI] [PubMed] [Google Scholar]
  24. Norris C. H., Ricci A. J., Housley G. D., Guth P. S. The inactivating potassium currents of hair cells isolated from the crista ampullaris of the frog. J Neurophysiol. 1992 Nov;68(5):1642–1653. doi: 10.1152/jn.1992.68.5.1642. [DOI] [PubMed] [Google Scholar]
  25. Ohmori H. Studies of ionic currents in the isolated vestibular hair cell of the chick. J Physiol. 1984 May;350:561–581. doi: 10.1113/jphysiol.1984.sp015218. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Prigioni I., Masetto S., Russo G., Taglietti V. Calcium currents in solitary hair cells isolated from frog crista ampullaris. J Vestib Res. 1992;2(1):31–39. [PubMed] [Google Scholar]
  27. Randall A. D., Tsien R. W. Contrasting biophysical and pharmacological properties of T-type and R-type calcium channels. Neuropharmacology. 1997 Jul;36(7):879–893. doi: 10.1016/s0028-3908(97)00086-5. [DOI] [PubMed] [Google Scholar]
  28. Rennie K. J., Ashmore J. F. Ionic currents in isolated vestibular hair cells from the guinea-pig crista ampullaris. Hear Res. 1991 Feb;51(2):279–291. doi: 10.1016/0378-5955(91)90044-a. [DOI] [PubMed] [Google Scholar]
  29. Rispoli G., Navangione A., Vellani V. Transport of K+ by Na(+)-Ca2+, K+ exchanger in isolated rods of lizard retina. Biophys J. 1995 Jul;69(1):74–83. doi: 10.1016/S0006-3495(95)79877-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Rossi M. L., Bonifazzi C., Martini M., Fesce R. Static and dynamic properties of synaptic transmission at the cyto-neural junction of frog labyrinth posterior canal. J Gen Physiol. 1989 Aug;94(2):303–327. doi: 10.1085/jgp.94.2.303. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Rossi M. L., Martini M., Pelucchi B., Fesce R. Quantal nature of synaptic transmission at the cytoneural junction in the frog labyrinth. J Physiol. 1994 Jul 1;478(Pt 1):17–35. doi: 10.1113/jphysiol.1994.sp020227. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Schmid R., Seydl K., Baumgartner W., Groschner K., Romanin C. Trypsin increases availability and open probability of cardiac L-type Ca2+ channels without affecting inactivation induced by Ca2+. Biophys J. 1995 Nov;69(5):1847–1857. doi: 10.1016/S0006-3495(95)80055-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Seydl K., Karlsson J. O., Dominik A., Gruber H., Romanin C. Action of calpastatin in prevention of cardiac L-type Ca2+ channel run-down cannot be mimicked by synthetic calpain inhibitors. Pflugers Arch. 1995 Feb;429(4):503–510. doi: 10.1007/BF00704155. [DOI] [PubMed] [Google Scholar]
  34. Sherman A., Keizer J., Rinzel J. Domain model for Ca2(+)-inactivation of Ca2+ channels at low channel density. Biophys J. 1990 Oct;58(4):985–995. doi: 10.1016/S0006-3495(90)82443-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Steinacker A., Monterrubio J., Perez R., Mensinger A. F., Marin A. Electrophysiology and pharmacology of outward potassium currents in semicircular canal hair cells of toadfish, Opsanus tau. Hear Res. 1997 Jul;109(1-2):11–20. doi: 10.1016/s0378-5955(97)00038-5. [DOI] [PubMed] [Google Scholar]
  36. Stern M. D. Buffering of calcium in the vicinity of a channel pore. Cell Calcium. 1992 Mar;13(3):183–192. doi: 10.1016/0143-4160(92)90046-u. [DOI] [PubMed] [Google Scholar]
  37. Su Z. L., Jiang S. C., Gu R., Yang W. P. Two types of calcium channels in bullfrog saccular hair cells. Hear Res. 1995 Jul;87(1-2):62–68. doi: 10.1016/0378-5955(95)00079-j. [DOI] [PubMed] [Google Scholar]
  38. Wu L. G., Borst J. G., Sakmann B. R-type Ca2+ currents evoke transmitter release at a rat central synapse. Proc Natl Acad Sci U S A. 1998 Apr 14;95(8):4720–4725. doi: 10.1073/pnas.95.8.4720. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Yamoah E. N., Lumpkin E. A., Dumont R. A., Smith P. J., Hudspeth A. J., Gillespie P. G. Plasma membrane Ca2+-ATPase extrudes Ca2+ from hair cell stereocilia. J Neurosci. 1998 Jan 15;18(2):610–624. doi: 10.1523/JNEUROSCI.18-02-00610.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Zidanic M., Fuchs P. A. Kinetic analysis of barium currents in chick cochlear hair cells. Biophys J. 1995 Apr;68(4):1323–1336. doi: 10.1016/S0006-3495(95)80305-X. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Biophysical Journal are provided here courtesy of The Biophysical Society

RESOURCES