Home LiteratureArticle Details
PMID: 11050202 Published · ppublish English Journal Article

Two mechanisms for transducer adaptation in vertebrate hair cells.

Holt JR, Corey DP

Abstract

Deflection of the hair bundle atop a sensory hair cell modulates the open probability of mechanosensitive ion channels. In response to sustained deflections, hair cells adapt. Two fundamentally distinct models have been proposed to explain transducer adaptation. Both models support the notion that channel open probability is modulated by calcium that enters via the transduction channels. Both also suggest that the primary effect of adaptation is to shift the deflection-response [I(X)] relationship in the direction of the applied stimulus, thus maintaining hair bundle sensitivity. The models differ in several respects. They operate on different time scales: the faster on the order of a few milliseconds or less and the slower on the order of 10 ms or more. The model proposed to explain fast adaptation suggests that calcium enters and binds at or near the transduction channels to stabilize a closed conformation. The model proposed to explain the slower adaptation suggests that adaptation is mediated by an active, force-generating process that regulates the effective stimulus applied to the transduction channels. Here we discuss the evidence in support of each model and consider the possibility that both may function to varying degrees in hair cells of different species and sensory organs.

MeSH Terms
Adaptation, Physiological Animals Calcium/metabolism Hair Cells, Auditory/metabolism,physiology Models, Biological Vertebrates/physiology
Chemicals
Calcium
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Holt J R
Department of Neurobiology, Howard Hughes Medical Institute, Harvard Medical School and Massachusetts General Hospital, Wellman 414, Boston, MA 02114, USA.
Corey D P
References (53)
53 references, click to expand
  1. The mechanical properties of ciliary bundles of turtle cochlear hair cells.
    J Physiol. 1985 Jul;364:359-79 PMID: 4032304
  2. Math1: an essential gene for the generation of inner ear hair cells.
    Science. 1999 Jun 11;284(5421):1837-41 PMID: 10364557
  3. Adaptation of mechanoelectrical transduction in hair cells of the bullfrog's sacculus.
    J Neurosci. 1987 Sep;7(9):2821-36 PMID: 3498016
  4. Voltage dependence of adaptation and active bundle movement in bullfrog saccular hair cells.
    Proc Natl Acad Sci U S A. 1989 Apr;86(8):2918-22 PMID: 2468161
  5. "Bundle blot" purification and initial protein characterization of hair cell stereocilia.
    Proc Natl Acad Sci U S A. 1989 Jul;86(13):4973-7 PMID: 2662191
  6. Engineering of the myosin-ibeta nucleotide-binding pocket to create selective sensitivity to N(6)-modified ADP analogs.
    J Biol Chem. 1999 Oct 29;274(44):31373-81 PMID: 10531338
  7. Characterization of the human and mouse unconventional myosin XV genes responsible for hereditary deafness DFNB3 and shaker 2.
    Genomics. 1999 Nov 1;61(3):243-58 PMID: 10552926
  8. Two components of transducer adaptation in auditory hair cells.
    J Neurophysiol. 1999 Nov;82(5):2171-81 PMID: 10561397
  9. Visualization of alpha9 acetylcholine receptor expression in hair cells of transgenic mice containing a modified bacterial artificial chromosome.
    Proc Natl Acad Sci U S A. 1999 Nov 23;96(24):14100-5 PMID: 10570205
  10. Ionic basis of the receptor potential in a vertebrate hair cell.
    Nature. 1979 Oct 25;281(5733):675-7 PMID: 45121
  11. Three sets of actin filaments in sensory cells of the inner ear. Identification and functional orientation determined by gel electrophoresis, immunofluorescence and electron microscopy.
    J Neurocytol. 1981 Feb;10(1):133-47 PMID: 7031190
  12. Analysis of the microphonic potential of the bullfrog's sacculus.
    J Neurosci. 1983 May;3(5):942-61 PMID: 6601693
  13. Kinetics of the receptor current in bullfrog saccular hair cells.
    J Neurosci. 1983 May;3(5):962-76 PMID: 6601694
  14. Cross-links between stereocilia in the guinea pig organ of Corti, and their possible relation to sensory transduction.
    Hear Res. 1984 Aug;15(2):103-12 PMID: 6436216
  15. The organization of actin filaments in the stereocilia of cochlear hair cells.
    J Cell Biol. 1980 Jul;86(1):244-59 PMID: 6893452
  16. Regulation of tension on hair-cell transduction channels: displacement and calcium dependence.
    J Neurosci. 1989 Nov;9(11):3988-97 PMID: 2555460
  17. Activation and adaptation of transducer currents in turtle hair cells.
    J Physiol. 1989 Dec;419:405-34 PMID: 2621635
  18. Compliance of the hair bundle associated with gating of mechanoelectrical transduction channels in the bullfrog's saccular hair cell.
    Neuron. 1988 May;1(3):189-99 PMID: 2483095
  19. Actin cores of hair-cell stereocilia support myosin motility.
    Proc Natl Acad Sci U S A. 1990 Nov;87(21):8627-31 PMID: 2236074
  20. Tip-link integrity and mechanical transduction in vertebrate hair cells.
    Neuron. 1991 Dec;7(6):985-94 PMID: 1764247
  21. Ultrastructural correlates of mechanoelectrical transduction in hair cells of the bullfrog's internal ear.
    Cold Spring Harb Symp Quant Biol. 1990;55:547-61 PMID: 1983446
  22. An active motor model for adaptation by vertebrate hair cells.
    J Neurosci. 1992 Sep;12(9):3291-309 PMID: 1527581
  23. 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):1330-4 PMID: 7679501
  24. Adenine nucleoside diphosphates block adaptation of mechanoelectrical transduction in hair cells.
    Proc Natl Acad Sci U S A. 1993 Apr 1;90(7):2710-4 PMID: 8464880
  25. Calmodulin and calmodulin-binding proteins in hair bundles.
    Proc Natl Acad Sci U S A. 1993 Apr 1;90(7):2807-11 PMID: 8385344
  26. Spatial calcium buffering in saccular hair cells.
    Nature. 1993 May 6;363(6424):74-6 PMID: 8479539
  27. Identification of a 120 kd hair-bundle myosin located near stereociliary tips.
    Neuron. 1993 Oct;11(4):581-94 PMID: 8398149
  28. Localization of calcium signals by a mobile calcium buffer in frog saccular hair cells.
    J Neurosci. 1994 May;14(5 Pt 2):3246-62 PMID: 8182469
  29. The extent of adaptation in bullfrog saccular hair cells.
    J Neurosci. 1994 Oct;14(10):6217-29 PMID: 7931574
  30. A type VII myosin encoded by the mouse deafness gene shaker-1.
    Nature. 1995 Mar 2;374(6517):62-4 PMID: 7870172
  31. The mouse Snell's waltzer deafness gene encodes an unconventional myosin required for structural integrity of inner ear hair cells.
    Nat Genet. 1995 Dec;11(4):369-75 PMID: 7493015
  32. Calcium imaging of single stereocilia in hair cells: localization of transduction channels at both ends of tip links.
    Neuron. 1995 Dec;15(6):1311-21 PMID: 8845155
  33. Functional expression of mammalian myosin I beta: analysis of its motor activity.
    Biochemistry. 1996 Jan 16;35(2):513-22 PMID: 8555222
  34. Calmodulin controls adaptation of mechanoelectrical transduction by hair cells of the bullfrog's sacculus.
    Proc Natl Acad Sci U S A. 1996 Mar 5;93(5):2203-7 PMID: 8700909
  35. Rapid, active hair bundle movements in hair cells from the bullfrog's sacculus.
    J Neurosci. 1996 Sep 15;16(18):5629-43 PMID: 8795619
  36. Phosphate analogs block adaptation in hair cells by inhibiting adaptation-motor force production.
    Neuron. 1996 Sep;17(3):523-33 PMID: 8816715
  37. Regeneration of broken tip links and restoration of mechanical transduction in hair cells.
    Proc Natl Acad Sci U S A. 1996 Dec 24;93(26):15469-74 PMID: 8986835
  38. ATPase activity of myosin in hair bundles of the bullfrog's sacculus.
    Biophys J. 1997 Jan;72(1):263-71 PMID: 8994611
  39. The effects of calcium buffering and cyclic AMP on mechano-electrical transduction in turtle auditory hair cells.
    J Physiol. 1997 May 15;501 ( Pt 1):111-24 PMID: 9174998
  40. Unconventional myosins in inner-ear sensory epithelia.
    J Cell Biol. 1997 Jun 16;137(6):1287-307 PMID: 9182663
  41. Mechanoelectrical transduction and adaptation in hair cells of the mouse utricle, a low-frequency vestibular organ.
    J Neurosci. 1997 Nov 15;17(22):8739-48 PMID: 9348343
  42. The selectivity of the hair cell's mechanoelectrical-transduction channel promotes Ca2+ flux at low Ca2+ concentrations.
    Proc Natl Acad Sci U S A. 1997 Sep 30;94(20):10997-1002 PMID: 9380748
  43. Myosin and adaptation by hair cells.
    Neuron. 1997 Nov;19(5):955-8 PMID: 9390509
  44. Plasma membrane Ca2+-ATPase extrudes Ca2+ from hair cell stereocilia.
    J Neurosci. 1998 Jan 15;18(2):610-24 PMID: 9425003
  45. 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):159-73 PMID: 9481679
  46. Myosin Ibeta is located at tip link anchors in vestibular hair bundles.
    J Neurosci. 1998 Jun 15;18(12):4603-15 PMID: 9614235
  47. Balance and hearing deficits in mice with a null mutation in the gene encoding plasma membrane Ca2+-ATPase isoform 2.
    J Biol Chem. 1998 Jul 24;273(30):18693-6 PMID: 9668038
  48. Mutations in a plasma membrane Ca2+-ATPase gene cause deafness in deafwaddler mice.
    Nat Genet. 1998 Aug;19(4):390-4 PMID: 9697703
  49. Regulation of free Ca2+ concentration in hair-cell stereocilia.
    J Neurosci. 1998 Aug 15;18(16):6300-18 PMID: 9698322
  50. The endogenous calcium buffer and the time course of transducer adaptation in auditory hair cells.
    J Neurosci. 1998 Oct 15;18(20):8261-77 PMID: 9763471
  51. Localization of myosin-Ibeta near both ends of tip links in frog saccular hair cells.
    J Neurosci. 1998 Nov 1;18(21):8637-47 PMID: 9786971
  52. Functional expression of exogenous proteins in mammalian sensory hair cells infected with adenoviral vectors.
    J Neurophysiol. 1999 Apr;81(4):1881-8 PMID: 10200223
  53. Mechanical relaxation of the hair bundle mediates adaptation in mechanoelectrical transduction by the bullfrog's saccular hair cell.
    Proc Natl Acad Sci U S A. 1987 May;84(9):3064-8 PMID: 3495007
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
2000-10-24
Pages
11730-5
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC34342
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]