Skip to main content
Proceedings of the Royal Society B: Biological Sciences logoLink to Proceedings of the Royal Society B: Biological Sciences
. 2000 Sep 22;267(1455):1915–1923. doi: 10.1098/rspb.2000.1230

Gating energies and forces of the mammalian hair cell transducer channel and related hair bundle mechanics.

S M van Netten 1, C J Kros 1
PMCID: PMC1690752  PMID: 11052545

Abstract

We quantified the molecular energies and forces involved in opening and closing of mechanoelectrical transducer channels in hair cells using a novel generally applicable method. It relies on a thermodynamic description of the free energy of an ion channel in terms of its open probability. The molecular gating force per channel as reflected in hair bundle mechanics is shown to equal kT/I(X) x dI(X)/dX, where I is the transducer current and X the deflection of the hair bundle. We applied the method to previously measured I(X) curves in mouse outer hair cells (OHCs) and vestibular hair cells (VHCs). Contrary to current models of transduction, gating of the transducer channel was found to involve only a finite range of free energy (< 10 kT), a consequence of our observation that the channel has a finite minimum open probability of ca. 1% for inhibitory bundle deflections. The maximum gating forces per channel of both cell types were found to be comparable (ca. 300-500 fN). Because of differences in passive restoring forces, gating forces result in very limited mechanical nonlinearity in OHC bundles compared to that in VHC bundles. A kinetic model of channel activation is proposed that accounts for the observed transducer currents and gating forces. It also predicts adaptation-like effects and spontaneous bundle movements ensuing from changes in state energy gaps possibly related to interactions of the channel with calcium ions.

Full Text

The Full Text of this article is available as a PDF (184.0 KB).

Selected References

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

  1. Assad J. A., Corey D. P. An active motor model for adaptation by vertebrate hair cells. J Neurosci. 1992 Sep;12(9):3291–3309. doi: 10.1523/JNEUROSCI.12-09-03291.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Assad J. A., Hacohen N., Corey D. P. Voltage dependence of adaptation and active bundle movement in bullfrog saccular hair cells. Proc Natl Acad Sci U S A. 1989 Apr;86(8):2918–2922. doi: 10.1073/pnas.86.8.2918. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bezanilla F., Stefani E. Voltage-dependent gating of ionic channels. Annu Rev Biophys Biomol Struct. 1994;23:819–846. doi: 10.1146/annurev.bb.23.060194.004131. [DOI] [PubMed] [Google Scholar]
  4. Corey D. P., Howard J. Models for ion channel gating with compliant states. Biophys J. 1994 Apr;66(4):1254–1257. doi: 10.1016/S0006-3495(94)80909-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Corey D. P., Hudspeth A. J. Kinetics of the receptor current in bullfrog saccular hair cells. J Neurosci. 1983 May;3(5):962–976. doi: 10.1523/JNEUROSCI.03-05-00962.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Crawford A. C., Evans M. G., Fettiplace R. Activation and adaptation of transducer currents in turtle hair cells. J Physiol. 1989 Dec;419:405–434. doi: 10.1113/jphysiol.1989.sp017878. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Crawford A. C., Evans M. G., Fettiplace R. The actions of calcium on the mechano-electrical transducer current of turtle hair cells. J Physiol. 1991 Mar;434:369–398. doi: 10.1113/jphysiol.1991.sp018475. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Crawford A. C., Fettiplace R. The mechanical properties of ciliary bundles of turtle cochlear hair cells. J Physiol. 1985 Jul;364:359–379. doi: 10.1113/jphysiol.1985.sp015750. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Denk W., Holt J. R., Shepherd G. M., Corey D. P. Calcium imaging of single stereocilia in hair cells: localization of transduction channels at both ends of tip links. Neuron. 1995 Dec;15(6):1311–1321. doi: 10.1016/0896-6273(95)90010-1. [DOI] [PubMed] [Google Scholar]
  10. Eatock R. A., Corey D. P., Hudspeth A. J. Adaptation of mechanoelectrical transduction in hair cells of the bullfrog's sacculus. J Neurosci. 1987 Sep;7(9):2821–2836. doi: 10.1523/JNEUROSCI.07-09-02821.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Flock A., Strelioff D. Graded and nonlinear mechanical properties of sensory hairs in the mammalian hearing organ. Nature. 1984 Aug 16;310(5978):597–599. doi: 10.1038/310597a0. [DOI] [PubMed] [Google Scholar]
  12. French R. J., Prusak-Sochaczewski E., Zamponi G. W., Becker S., Kularatna A. S., Horn R. Interactions between a pore-blocking peptide and the voltage sensor of the sodium channel: an electrostatic approach to channel geometry. Neuron. 1996 Feb;16(2):407–413. doi: 10.1016/s0896-6273(00)80058-6. [DOI] [PubMed] [Google Scholar]
  13. Furness D. N., Zetes D. E., Hackney C. M., Steele C. R. Kinematic analysis of shear displacement as a means for operating mechanotransduction channels in the contact region between adjacent stereocilia of mammalian cochlear hair cells. Proc Biol Sci. 1997 Jan 22;264(1378):45–51. doi: 10.1098/rspb.1997.0007. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Garcia-Anoveros J., Corey D. P. The molecules of mechanosensation. Annu Rev Neurosci. 1997;20:567–594. doi: 10.1146/annurev.neuro.20.1.567. [DOI] [PubMed] [Google Scholar]
  15. Géléoc G. S., Lennan G. W., Richardson G. P., Kros C. J. A quantitative comparison of mechanoelectrical transduction in vestibular and auditory hair cells of neonatal mice. Proc Biol Sci. 1997 Apr 22;264(1381):611–621. doi: 10.1098/rspb.1997.0087. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hackney C. M., Furness D. N. Mechanotransduction in vertebrate hair cells: structure and function of the stereociliary bundle. Am J Physiol. 1995 Jan;268(1 Pt 1):C1–13. doi: 10.1152/ajpcell.1995.268.1.C1. [DOI] [PubMed] [Google Scholar]
  17. Holton T., Hudspeth A. J. The transduction channel of hair cells from the bull-frog characterized by noise analysis. J Physiol. 1986 Jun;375:195–227. doi: 10.1113/jphysiol.1986.sp016113. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Howard J., Hudspeth A. J. Compliance of the hair bundle associated with gating of mechanoelectrical transduction channels in the bullfrog's saccular hair cell. Neuron. 1988 May;1(3):189–199. doi: 10.1016/0896-6273(88)90139-0. [DOI] [PubMed] [Google Scholar]
  19. Howard J., Roberts W. M., Hudspeth A. J. Mechanoelectrical transduction by hair cells. Annu Rev Biophys Biophys Chem. 1988;17:99–124. doi: 10.1146/annurev.bb.17.060188.000531. [DOI] [PubMed] [Google Scholar]
  20. Jaramillo F., Hudspeth A. J. Displacement-clamp measurement of the forces exerted by gating springs in the hair bundle. Proc Natl Acad Sci U S A. 1993 Feb 15;90(4):1330–1334. doi: 10.1073/pnas.90.4.1330. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Markin V. S., Hudspeth A. J. Gating-spring models of mechanoelectrical transduction by hair cells of the internal ear. Annu Rev Biophys Biomol Struct. 1995;24:59–83. doi: 10.1146/annurev.bb.24.060195.000423. [DOI] [PubMed] [Google Scholar]
  22. Merkel R., Nassoy P., Leung A., Ritchie K., Evans E. Energy landscapes of receptor-ligand bonds explored with dynamic force spectroscopy. Nature. 1999 Jan 7;397(6714):50–53. doi: 10.1038/16219. [DOI] [PubMed] [Google Scholar]
  23. Nishizaka T., Miyata H., Yoshikawa H., Ishiwata S., Kinosita K., Jr Unbinding force of a single motor molecule of muscle measured using optical tweezers. Nature. 1995 Sep 21;377(6546):251–254. doi: 10.1038/377251a0. [DOI] [PubMed] [Google Scholar]
  24. Pickles J. O. A model for the mechanics of the stereociliar bundle on acousticolateral hair cells. Hear Res. 1993 Aug;68(2):159–172. doi: 10.1016/0378-5955(93)90120-p. [DOI] [PubMed] [Google Scholar]
  25. Pickles J. O., Comis S. D., Osborne M. P. Cross-links between stereocilia in the guinea pig organ of Corti, and their possible relation to sensory transduction. Hear Res. 1984 Aug;15(2):103–112. doi: 10.1016/0378-5955(84)90041-8. [DOI] [PubMed] [Google Scholar]
  26. Russell I. J., Kössl M., Richardson G. P. Nonlinear mechanical responses of mouse cochlear hair bundles. Proc Biol Sci. 1992 Dec 22;250(1329):217–227. doi: 10.1098/rspb.1992.0152. [DOI] [PubMed] [Google Scholar]
  27. Shepherd G. M., Corey D. P. The extent of adaptation in bullfrog saccular hair cells. J Neurosci. 1994 Oct;14(10):6217–6229. doi: 10.1523/JNEUROSCI.14-10-06217.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Wu Y. C., Ricci A. J., Fettiplace R. Two components of transducer adaptation in auditory hair cells. J Neurophysiol. 1999 Nov;82(5):2171–2181. doi: 10.1152/jn.1999.82.5.2171. [DOI] [PubMed] [Google Scholar]
  29. van Netten S. M., Khanna S. M. Stiffness changes of the cupula associated with the mechanics of hair cells in the fish lateral line. Proc Natl Acad Sci U S A. 1994 Feb 15;91(4):1549–1553. doi: 10.1073/pnas.91.4.1549. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Proceedings of the Royal Society B: Biological Sciences are provided here courtesy of The Royal Society

RESOURCES