Skip to main content
Log in

Reorganization of actin during repair of hair bundle mechanoreceptors

  • Published:
Journal of Neurocytology

Abstract

Hair bundle mechanoreceptors can be damaged by over-stimulation or by exposure to calcium-free buffers. Provided the trauma is slight, hair bundles recover, although the subcellular mechanisms for such recovery are poorly understood. Hair bundle mechanoreceptors on tentacles of sea anemones are especially resilient, recovering from severe trauma within several hours. During the recovery period, large protein complexes are secreted called “repair proteins” containing replacement linkages for those lost during trauma. In the present study, we find that recovery requires reorganization of the actin-based cytoskeleton in hair bundles. F-actin is first partially depolymerized and then repolymerized in hair bundles based on confocal microscopy. Furthermore, stereocilia show considerable motility during repair based on field emission scanning electron microscopy of hair bundles fixed at 1 min intervals after exposure to exogenously supplied repair protein complexes. Recovery of vibration sensitivity occurs at the organismal level within 8 min. Paradoxically, a full recovery of morphology of hair bundles requires approximately 45 min and a recovery of F-actin levels requires approximately 40 min. Similarly, a full recovery of mechanoelectric responses of hair cells requires approximately 45 min. Thus, it appears that the recovery of responsiveness at the organismal level precedes a full recovery of hair bundles.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Assad, J. A., Shepherd, G. M. & Corey, D. P. (1991) Tip-link integrity and mechanical transduction in vertebrate hair cells. Neuron 7, 985–994.

    PubMed  Google Scholar 

  • Baird, R. A., Burton, M. D., Fashena, D. S. & Naegler, R. A. (2000) Hair cell recovery in mitotically blocked cultures of the bullfrog saccule. Proceedings of the National Academy of Sciences of the USA 97, 11722–11729.

    PubMed  Google Scholar 

  • Clark, J. A. & Pickles, J. O. (1996) The effects of moderate and low levels of acoustic overstimulation on stereocilia and their tip links in the guinea pig. Hearing Research 99, 119–128.

    PubMed  Google Scholar 

  • Cotanche, D. A. (1999) Structural recovery from sound and aminoglycoside damage in the avian cochlea. Audiology and Neuro-Otology 4, 271–285.

    PubMed  Google Scholar 

  • Cotanche, D. A., Lee, K. H., Stine, J. S. & Picard, D. A. (1994) Hair cell regeneration in the bird cochlea following noise damage or ototoxic drug damage. Anatomy and Embryology 189, 1–18.

    PubMed  Google Scholar 

  • Corwin, J. T. & Oberholtzer, J. C. (1997) Fish n’ chicks: Model recipes for hair cell regeneration? Neuron 19, 951–954.

    PubMed  Google Scholar 

  • Crawford, A. C., Evans, M. G. & Fettiplace, R. (1991) The actions of calcium on the mechano-electrical transducer current of turtle hair cells. Journal of Physiology 434, 369–398.

    PubMed  Google Scholar 

  • Duncan, R. K., Hernandez, H. N. & Saunders, J. C. (1995) Relative stereocilia motion of chick cochlear hair cells during high-frequency water-jet stimulation. Auditory Neuroscience 1, 321–329.

    Google Scholar 

  • Duncan, R. K. & Saunders, J. C. (2000) Stereocilium injury mediates hair bundle stiffness loss and recovery following intense water-jet stimulation. Journal of Comparative Physiology, Series A 186, 1095–1106.

    Google Scholar 

  • Gale, J. E., Marcotti, W., Kennedy, H. J., Kros, C. J. & Richardson, G. P. (2001) FM1-43 dye behaves as a permeant blocker of the hair cell mechanotransducer channel. Journal of Neuroscience 21, 7013–7025.

    PubMed  Google Scholar 

  • Gong, T. W., Hegeman, A. D., Shin, J. J., Adler, H. J., Raphael, Y. & Lomax, M. I. (1996) Identification of genes expressed after noise exposure in the chick basilar papilla. Hearing Research 96, 20–32.

    PubMed  Google Scholar 

  • Goodyear, R. & Richardson, G. (1999) The ankle-link antigen: An epitope sensitive to calcium chelation associated with the hair cell surface and the calycal processes of photoreceptors. Journal of Neuroscience 19, 3761–3772.

    PubMed  Google Scholar 

  • Hall, A. (1998) Rho GTPases and the actin cytoskeleton. Science 279, 509–514.

    PubMed  Google Scholar 

  • Husbands, J. M., Steinberg, S. A., Kurian, R. & Saunders, J. C. (1999) Tip-link integrity on chick tall hair cell stereocilia following intense sound exposure. Hearing Research 135, 135–145.

    PubMed  Google Scholar 

  • Meyer, J., Furness, D. N., Zenner, H. P., Hackney, C. M. & Gummer, A. W. (1998) Evidence for opening of hair-cell transducer channels after tip-link loss. Journal of Neuroscience 18, 6748–6756.

    PubMed  Google Scholar 

  • Mire, P. & Watson, G. M. (1997) Mechanotransduction of hair bundles arising from multicellular complexes in anemones. Hearing Research 113, 224–234.

    PubMed  Google Scholar 

  • Niemiec, A. J., Raphael, Y. & Moody, D. B. (1994) Return of auditory function following structural regeneration after acoustic trauma: Behavioral measures from quail. Hearing Research 75, 209–224.

    PubMed  Google Scholar 

  • Pickles, J. O., Osborne, M. P. & Comis, S. D. (1987) Vulnerability of tip links between stereocilia to acoustic trauma in the guinea pig. Hearing Research 25, 173–183.

    PubMed  Google Scholar 

  • Repass, J. J. & Watson, G. M. (2001) Anemone repair proteins as a potential therapeutic agent for vertebrate hair cells: Facilitated recovery of the lateral line of blind cave fish. Hearing Research 154, 98–107.

    PubMed  Google Scholar 

  • Sand, O. (1975) Effects of different ionic environments on the mechano-sensitivity of lateral line organs in the mud-puppy. Journal of Comparative Physiology, Series A, 102, 27–42.

    Google Scholar 

  • Sobkowicz, H. M., August, B. K. & Slapnick, S. M. (1992) Epithelial repair following mechanical injury of the developing organ of Corti in culture: An electron microscopic and autoradiographic study. Experimental Neurology 115, 44–49.

    PubMed  Google Scholar 

  • Stone, J. S., Oesterle, E. C. & Rubel, E. W. (1998) Recent insights into regeneration of auditory and vestibular hair cells. Current Opinion of Neurology 11, 17–24.

    Google Scholar 

  • Stone, J. S. & Rubel, E. W. (2000) Cellular studies of auditory hair cell regeneration in birds. Proceedings of the National Academy of Sciences of the USA 97, 11714–11721.

    PubMed  Google Scholar 

  • Tsue, T. T., Oesterle, E. C. & Rubel, E. W. (1994) Hair cell regeneration in the inner ear. Otolaryngology-Head and Neck Surgery 111, 281–301.

    PubMed  Google Scholar 

  • Watson, G. M. (2001) How a living hair cell repairs itself: Involvement of purinoceptors in the repair of hair bundle mechanoreceptors of sea anemones. In: Hair Cells: Micromechanics and Hearing (edited by Berlin, C. I. & Bobbin, R. P.) pp. 27–44, San Diego: Singular Press.

    Google Scholar 

  • Watson, G. M. & Hessinger, D. A. (1989) Cnidocyte mechanoreceptors are tuned to the movements of swimming prey by chemoreceptors. Science 243, 1589–1591.

    PubMed  Google Scholar 

  • Watson, G. M. & Hudson, R. R. (1994) Frequency and amplitude tuning of nematocyst discharge by proline. Journal of Experimental Zoology 268, 177–185.

    Google Scholar 

  • Watson, G. M., Mire, P. & Hudson, R. R. (1997) Hair bundles of sea anemones as a model system for vertebrate hair bundles. Hearing Research 107, 53–66.

    PubMed  Google Scholar 

  • Watson, G. M., Mire, P. & Hudson, R. R. (1998a) Repair of hair bundles in sea anemones by secreted proteins. Hearing Research 115, 119–128.

    PubMed  Google Scholar 

  • Watson, G. M., Mire, P. & Hudson, R. R. (1998b) Frequency specificity of vibration dependent discharge of nematocysts in sea anemones. Journal of Experimental Zoology 281, 582–593.

    PubMed  Google Scholar 

  • Watson, G. M. & Roberts, J. (1995) Chemoreceptormediated polymerization and depolymerization of actin in hair bundles of sea anemones. Cell Motility and the Cytoskeleton 30, 208–220.

    PubMed  Google Scholar 

  • Watson, G. M., Venable, S., Hudson, R. R. & Repass, J. J. (1999) ATP enhances repair of hair bundles in sea anemones. Hearing Research 136, 1–12.

    PubMed  Google Scholar 

  • Watson, G. M. & Venable-Thibodeaux, S. (2000) Immunological evidence that anemone repair proteins include replacement linkages. Hearing Research 146, 35–46.

    PubMed  Google Scholar 

  • Zhao, Y., Yamoah, E. N. & Gillespie, P. G. (1996) Regeneration of broken tip links and restoration of mechanical transduction in hair cells. Proceedings of the National Academy of Sciences of the USA 94, 15469–15474.

    Google Scholar 

Download references

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Watson, G.M., Mire, P. Reorganization of actin during repair of hair bundle mechanoreceptors. J Neurocytol 30, 895–906 (2001). https://doi.org/10.1023/A:1020665116719

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1020665116719

Keywords

Navigation