Skip to main content
Philosophical Transactions of the Royal Society B: Biological Sciences logoLink to Philosophical Transactions of the Royal Society B: Biological Sciences
. 2004 Dec 29;359(1452):1945–1951. doi: 10.1098/rstb.2004.1564

Myosin I and adaptation of mechanical transduction by the inner ear.

Peter G Gillespie 1
PMCID: PMC1693471  PMID: 15647170

Abstract

Twenty years ago, the description of hair-cell stereocilia as actin-rich structures led to speculation that myosin molecules participated in mechanical transduction in the inner ear. In 1987, Howard and Hudspeth proposed specifically that a myosin I might mediate adaptation of the transduction current carried by hair cells, the sensory cells of the ear. We exploited the myosin literature to design tests of this hypothesis and to show that the responsible isoform is myosin 1c. The identification of this myosin as the adaptation motor would have been impossible without thorough experimentation on other myosins, particularly muscle myosins. The sliding-filament hypothesis for muscle contraction has thus led to a detailed understanding of the behaviour of hair cells.

Full Text

The Full Text of this article is available as a PDF (516.8 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. Barylko B., Wagner M. C., Reizes O., Albanesi J. P. Purification and characterization of a mammalian myosin I. Proc Natl Acad Sci U S A. 1992 Jan 15;89(2):490–494. doi: 10.1073/pnas.89.2.490. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bishop A., Buzko O., Heyeck-Dumas S., Jung I., Kraybill B., Liu Y., Shah K., Ulrich S., Witucki L., Yang F. Unnatural ligands for engineered proteins: new tools for chemical genetics. Annu Rev Biophys Biomol Struct. 2000;29:577–606. doi: 10.1146/annurev.biophys.29.1.577. [DOI] [PubMed] [Google Scholar]
  5. Chase P. B., Martyn D. A., Hannon J. D. Activation dependence and kinetics of force and stiffness inhibition by aluminiofluoride, a slowly dissociating analogue of inorganic phosphate, in chemically skinned fibres from rabbit psoas muscle. J Muscle Res Cell Motil. 1994 Apr;15(2):119–129. doi: 10.1007/BF00130423. [DOI] [PubMed] [Google Scholar]
  6. Chase P. B., Martyn D. A., Kushmerick M. J., Gordon A. M. Effects of inorganic phosphate analogues on stiffness and unloaded shortening of skinned muscle fibres from rabbit. J Physiol. 1993 Jan;460:231–246. doi: 10.1113/jphysiol.1993.sp019469. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cooke R., Pate E. The effects of ADP and phosphate on the contraction of muscle fibers. Biophys J. 1985 Nov;48(5):789–798. doi: 10.1016/S0006-3495(85)83837-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Corey D. P., Hudspeth A. J. Analysis of the microphonic potential of the bullfrog's sacculus. J Neurosci. 1983 May;3(5):942–961. doi: 10.1523/JNEUROSCI.03-05-00942.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. 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]
  10. Dantzig J. A., Goldman Y. E. Suppression of muscle contraction by vanadate. Mechanical and ligand binding studies on glycerol-extracted rabbit fibers. J Gen Physiol. 1985 Sep;86(3):305–327. doi: 10.1085/jgp.86.3.305. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. 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]
  12. Fisher A. J., Smith C. A., Thoden J. B., Smith R., Sutoh K., Holden H. M., Rayment I. X-ray structures of the myosin motor domain of Dictyostelium discoideum complexed with MgADP.BeFx and MgADP.AlF4-. Biochemistry. 1995 Jul 18;34(28):8960–8972. doi: 10.1021/bi00028a004. [DOI] [PubMed] [Google Scholar]
  13. Garabedian T. E., Yount R. G. Direct photoaffinity labeling of gizzard myosin with vanadate-trapped adenosine diphosphate. Biochemistry. 1991 Oct 22;30(42):10126–10132. doi: 10.1021/bi00106a008. [DOI] [PubMed] [Google Scholar]
  14. García J. A., Yee A. G., Gillespie P. G., Corey D. P. Localization of myosin-Ibeta near both ends of tip links in frog saccular hair cells. J Neurosci. 1998 Nov 1;18(21):8637–8647. doi: 10.1523/JNEUROSCI.18-21-08637.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Gillespie P. G., Hudspeth A. J. Adenine nucleoside diphosphates block adaptation of mechanoelectrical transduction in hair cells. Proc Natl Acad Sci U S A. 1993 Apr 1;90(7):2710–2714. doi: 10.1073/pnas.90.7.2710. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Gillespie P. G., Hudspeth A. J. High-purity isolation of bullfrog hair bundles and subcellular and topological localization of constituent proteins. J Cell Biol. 1991 Feb;112(4):625–640. doi: 10.1083/jcb.112.4.625. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Gillespie P. G., Wagner M. C., Hudspeth A. J. Identification of a 120 kd hair-bundle myosin located near stereociliary tips. Neuron. 1993 Oct;11(4):581–594. doi: 10.1016/0896-6273(93)90071-x. [DOI] [PubMed] [Google Scholar]
  18. Goodno C. C. Myosin active-site trapping with vanadate ion. Methods Enzymol. 1982;85(Pt B):116–123. doi: 10.1016/0076-6879(82)85014-3. [DOI] [PubMed] [Google Scholar]
  19. Hasson T., Gillespie P. G., Garcia J. A., MacDonald R. B., Zhao Y., Yee A. G., Mooseker M. S., Corey D. P. Unconventional myosins in inner-ear sensory epithelia. J Cell Biol. 1997 Jun 16;137(6):1287–1307. doi: 10.1083/jcb.137.6.1287. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Holt Jeffrey R., Gillespie Susan K. H., Provance D. William, Shah Kavita, Shokat Kevan M., Corey David P., Mercer John A., Gillespie Peter G. A chemical-genetic strategy implicates myosin-1c in adaptation by hair cells. Cell. 2002 Feb 8;108(3):371–381. doi: 10.1016/s0092-8674(02)00629-3. [DOI] [PubMed] [Google Scholar]
  21. Howard J., Hudspeth A. J. 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):3064–3068. doi: 10.1073/pnas.84.9.3064. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Hudspeth A. J. How the ear's works work. Nature. 1989 Oct 5;341(6241):397–404. doi: 10.1038/341397a0. [DOI] [PubMed] [Google Scholar]
  23. Liu Y., Shah K., Yang F., Witucki L., Shokat K. M. Engineering Src family protein kinases with unnatural nucleotide specificity. Chem Biol. 1998 Feb;5(2):91–101. doi: 10.1016/s1074-5521(98)90143-0. [DOI] [PubMed] [Google Scholar]
  24. Maruta H., Korn E. D. Direct photoaffinity labeling by nucleotides of the apparent catalytic site on the heavy chains of smooth muscle and Acanthamoeba myosins. J Biol Chem. 1981 Jan 10;256(1):499–502. [PubMed] [Google Scholar]
  25. Pate E., Cooke R. A model of crossbridge action: the effects of ATP, ADP and Pi. J Muscle Res Cell Motil. 1989 Jun;10(3):181–196. doi: 10.1007/BF01739809. [DOI] [PubMed] [Google Scholar]
  26. Reizes O., Barylko B., Li C., Südhof T. C., Albanesi J. P. Domain structure of a mammalian myosin I beta. Proc Natl Acad Sci U S A. 1994 Jul 5;91(14):6349–6353. doi: 10.1073/pnas.91.14.6349. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Rybin V., Ullrich O., Rubino M., Alexandrov K., Simon I., Seabra M. C., Goody R., Zerial M. GTPase activity of Rab5 acts as a timer for endocytic membrane fusion. Nature. 1996 Sep 19;383(6597):266–269. doi: 10.1038/383266a0. [DOI] [PubMed] [Google Scholar]
  28. Shah K., Liu Y., Deirmengian C., Shokat K. M. Engineering unnatural nucleotide specificity for Rous sarcoma virus tyrosine kinase to uniquely label its direct substrates. Proc Natl Acad Sci U S A. 1997 Apr 15;94(8):3565–3570. doi: 10.1073/pnas.94.8.3565. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Siemens Jan, Lillo Concepcion, Dumont Rachel A., Reynolds Anna, Williams David S., Gillespie Peter G., Müller Ulrich. Cadherin 23 is a component of the tip link in hair-cell stereocilia. Nature. 2004 Mar 31;428(6986):950–955. doi: 10.1038/nature02483. [DOI] [PubMed] [Google Scholar]
  30. Wagner M. C., Barylko B., Albanesi J. P. Tissue distribution and subcellular localization of mammalian myosin I. J Cell Biol. 1992 Oct;119(1):163–170. doi: 10.1083/jcb.119.1.163. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Weijland A., Parmeggiani A. Toward a model for the interaction between elongation factor Tu and the ribosome. Science. 1993 Feb 26;259(5099):1311–1314. doi: 10.1126/science.8446899. [DOI] [PubMed] [Google Scholar]
  32. Yamoah E. N., Gillespie P. G. Phosphate analogs block adaptation in hair cells by inhibiting adaptation-motor force production. Neuron. 1996 Sep;17(3):523–533. doi: 10.1016/s0896-6273(00)80184-1. [DOI] [PubMed] [Google Scholar]

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

RESOURCES