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Repair of hair cells following mild trauma may involve extracellular chaperones

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Abstract

Sea anemones were subjected to mild trauma consisting of a 2 min immersion in calcium-depleted seawater. The trauma caused a loss of vibration sensitivity that spontaneously recovered within 50 min of returning the anemones to calcium containing seawater. Apparently, recovery is conferred by proteins contained in fraction gamma, a chromatographic fraction of homogenized mucus collected at the base of anemones allowed to recover from similar trauma. On silver stained SDS-PAGE gels, fraction gamma consists of a single band having an estimated mass of 55 kDa. Fraction gamma is alone sufficient to repair hair bundle mechanoreceptors in anemones. Its biological activity is enhanced in the presence of exogenously supplied ATP, but not GTP nor ADP-ribose. Biotinylated fraction gamma binds to hair bundles. The hypothesis that fraction gamma consists of Hsp60 proteins was tested. Commercial antibodies to Hsp60 label a band at 55 kDa in western blots. Hsp60 antibodies label hair bundles in traumatized anemones but not in untreated controls. Dilute Hsp60 antiserum (but not nonimmune serum) delays the spontaneous recovery of vibration sensitivity in anemones subjected to mild trauma. Thus, fraction gamma likely consists of Hsp60, or a Hsp60-like protein, that functions on the extracellular face of the plasma membrane to restore function to traumatized hair bundles.

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References

  • Assad JA, Shepherd GM, Corey DP (1991) Tip-link integrity and mechanical transduction in vertebrate hair cells. Neuron 7:985–994

    Article  PubMed  CAS  Google Scholar 

  • Bayer EA, Wilchek M (1990) Protein biotinylation. Methods Enzymol 184:138–160

    Article  PubMed  CAS  Google Scholar 

  • Berg A, Watson GM (2002) Rapid recovery of sensory function in blind cave fish treated with anemone repair proteins. Hear Res 174:296–304

    Article  PubMed  CAS  Google Scholar 

  • Chitaev NA, Troyanovsky SM (1998) Adhesive but not lateral E-cadherin complexes require calcium and catenins for their formation. J Cell Biol 142:837–846

    Article  PubMed  CAS  Google Scholar 

  • Crawford AC, Evans MG, Fettiplace R (1991) The actions of calcium on the mechano-electrical transducer current of turtle hair cells. J Physiol 434:369–398

    PubMed  CAS  Google Scholar 

  • Frostegard J, Pockley AG (2005) Heat shock protein release and naturally occurring exogenous heat shock proteins. In: Henderson B, Pockley AG (eds) Molecular chaperones and cell signalling. Cambridge University Press, New York, pp 195–219

    Google Scholar 

  • Gale JE, Marcotti W, Kennedy HJ, Kros CJ, Richardson GP (2001) FM1-43 dye behaves as a permeant blocker of the hair cell mechanotransducer channel. J Neurosci 21:7013–7025

    PubMed  CAS  Google Scholar 

  • Gale JE, Piazza V, Ciubotaru CD, Mammano F (2004) A mechanism for sensing noise damage in the inner ear. Curr Biol 14:526–529

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Harrison OJ, Corps EM, Kilshaw PJ (2005) Cadherin adhesion depends on a salt bridge at the N-terminus. J Cell Sci 118:4123–4130

    Article  PubMed  CAS  Google Scholar 

  • Kachar B, Parrakal M, Kurc M, Zhao Y, Gillespie PG (2000) High-resolution structure of hair-cell tip-links. Proc Natl Acad Sci USA 97:13336–13341

    Article  PubMed  CAS  Google Scholar 

  • Mariscal RN (1974a) Nematocysts. In: Muscatine L, Lenhoff HM (eds) Coelenterate biology, reviews and new perspectives. Academic, New York pp 129–178

    Google Scholar 

  • Mariscal RN (1974b) Scanning electron microscopy of the sensory surface of the tentacles of sea anemones and corals. Z Zellforsch Mikrosk Anat 147:149–156

    Article  PubMed  CAS  Google Scholar 

  • Meyer J, Furness D, Zenner HP, Hackney CM, Gummer AW (1998) Evidence for opening of hair-cell transducer channels after tip-link loss. J Neurosci 18:6748–6756

    PubMed  CAS  Google Scholar 

  • Michel V, Goodyear RJ, Weil D, Marcotti W, Perfettini I, Wolfrum U, Kros CJ, Richardson GP, Petit C (2005) Cadherin 23 is a component of the transient lateral links in the developing hair-bundles of cochlear sensory cells. Dev Biol 280:281–294

    Article  PubMed  CAS  Google Scholar 

  • Minasian LL Jr, Mariscal RN (1979) Characteristics and regulation of fission activity in clonal cultures of the cosmopolitan sea anemone, Haliplanella luciae (Verrill). Biol Bull 157:478–493

    Article  Google Scholar 

  • Mire-Thibodeaux P, Watson GM (1994) Morphodynamic hair bundles arising from sensory cell/supporting cell complexes frequency-tune nematocyst discharge in sea anemones. J Exp Zool 268:281–292

    Article  Google Scholar 

  • Munoz DJB, Thorne PR, Housley GD, Billet TE (1995) Adenosine 5’-triphosphate (ATP) concentrations in the endolymph and perilymph of the guinea pig cochlea. Hear Res 90:119–125

    Article  PubMed  CAS  Google Scholar 

  • Pertz O, Bozic D, Koch AW, Fauser C, Brancaccio A, Engel J (1999) A new crystal structure, Ca2+ dependence and mutational analysis reveal molecular details of E-cadherin homoassociation. EMBO J 18:1738–1747

    Article  PubMed  CAS  Google Scholar 

  • Peteya DJ (1975) The ciliary-cone sensory cell of anemones and cerianthids. Tissue Cell 7:243–252

    Article  PubMed  CAS  Google Scholar 

  • Repass JJ, Watson GM (2001) Anemone repair proteins as a potential therapeutic agent for vertebrate hair cells: Facilitated recovery of the lateral line of blind cave fish. Hear Res 154:98–107

    Article  PubMed  CAS  Google Scholar 

  • Sand O (1975) Effects of different ionic environments on the mechano-sensitivity of the lateral line organs in the mud-puppy. J Comp Physiol Ser A 102:27–42

    Article  CAS  Google Scholar 

  • Siemens J, Lillo C, Dumont RA, Reynolds A, Williams DS, Gillespie PG, Muller U (2004) Cadherin 23 is a component of the tip link in hair-cell stereocilia. Nature 428:950–955

    Article  PubMed  CAS  Google Scholar 

  • Sollner C, Rauch GJ, Siemens J, Geisler R, Schuster SC, Muller U, Nicolson T, Tubingen 2000-Screening Consortium (2004) Mutations in cadherin 23 affect tip links in zebrafish sensory hair cells. Nature 428:955–959

    Google Scholar 

  • Sotomayor M, Corey DP, Schulten K (2005) In search of the hair cell gating spring: elastic properties of ankyrin and cadherin repeats. Structure 13:669–682

    Article  PubMed  CAS  Google Scholar 

  • Tsuprun V, Goodyear RJ, Richardson GP (2004) The structure of tip links and kinocilial links in avian sensory hair bundles. Biophys J 87:4106–4112

    Article  PubMed  CAS  Google Scholar 

  • Watson GM, Hessinger DA (1987) Receptor-mediated endocytosis of a chemoreceptor involved in triggering the discharge of cnidae in a sea anemone tentacle. Tissue Cell 19:747–755

    Article  PubMed  CAS  Google Scholar 

  • Watson GM, Hessinger DA (1989) Cnidocyte mechanoreceptors are tuned to the movements of swimming prey by chemoreceptors. Science 243:1589–1591

    Article  PubMed  CAS  Google Scholar 

  • Watson GM, Hudson RR (1994) Frequency and amplitude tuning of nematocyst discharge by proline. J Exp Zool 268:177–185

    Article  CAS  Google Scholar 

  • Watson GM, Mire P (2001) Reorganization of actin during repair of hair bundle mechanoreceptors. J Neurocytol 30:895–906

    Article  PubMed  CAS  Google Scholar 

  • Watson GM, Mire P (2004) Dynamic tuning of hair bundle mechanoreceptors in a sea anemone during predation. Hydrobiologica 530/531:123–128

    Article  CAS  Google Scholar 

  • Watson GM, Roberts J (1994) Localization of proline receptors involved in regulating nematocyst discharge. J Exp Zool 270:527–537

    Article  CAS  Google Scholar 

  • Watson GM, Mire P, Hudson RR (1997) Hair bundles of sea anemones as a model system for vertebrate hair bundles. Hear Res 107:53–66

    Article  PubMed  CAS  Google Scholar 

  • Watson GM, Mire P, Hudson RR (1998a) Repair of hair bundles in sea anemones by secreted proteins. Hear Res 115:119–128

    Article  PubMed  CAS  Google Scholar 

  • Watson GM, Mire P, Hudson RR (1998b) Frequency specificity of vibration dependent discharge of nematocysts in sea anemones. J Exp Zool 281:582–593

    Article  PubMed  CAS  Google Scholar 

  • Watson GM, Venable S, Hudson RR, Repass JJ (1999) ATP enhances repair of hair bundles in sea anemones. Hear Res 136:1–12

    Article  PubMed  CAS  Google Scholar 

  • Watson GM, Graugnard EM, Mire P (2007) The involvement of Arl-5b in the repair of hair cells in sea anemones. JARO 8:183–193

    Article  PubMed  Google Scholar 

  • Zhao Y, Yamoah EN, Gillespie PG (1996) Regeneration of broken tip links and restoration of mechanical transduction in hair cells. Proc Natl Acad Sci USA 94:15469–15474

    Article  Google Scholar 

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Acknowledgments

We gratefully acknowledge financial support of this project by the NOHR Foundation and NSF IOB0542574.

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  1. Department of Biology, The University of Louisiana at Lafayette, Lafayette, LA, 70504-2451, USA

    Kamalika Nag & Glen M. Watson

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  1. Kamalika Nag
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  2. Glen M. Watson
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Correspondence to Glen M. Watson.

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Nag, K., Watson, G.M. Repair of hair cells following mild trauma may involve extracellular chaperones. J Comp Physiol A 193, 1045–1053 (2007). https://doi.org/10.1007/s00359-007-0255-5

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  • DOI: https://doi.org/10.1007/s00359-007-0255-5

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