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Cadherin 23-like polypeptide in hair bundle mechanoreceptors of sea anemones

  • Glen M. WatsonEmail author
  • Lankhanh Pham
  • Erin M. Graugnard
  • Patricia Mire
Original Paper

Abstract

We investigated hair bundle mechanoreceptors in sea anemones for a homolog of cadherin 23. A candidate sequence was identified from the database for Nematostella vectensis that has a shared lineage with vertebrate cadherin 23s. This cadherin 23-like protein comprises 6,074 residues. It is an integral protein that features three transmembrane alpha-helices and a large extracellular loop with 44 contiguous, cadherin (CAD) domains. In the second half of the polypeptide, the CAD domains occur in a quadruple repeat pattern. Members of the same repeat group (i.e., CAD 18, 22, 26, and so on) share nearly identical amino acid sequences. An affinity-purified antibody was generated to a peptide from the C-terminus of the cadherin 23-like polypeptide. The peptide is expected to lie on the exoplasmic side of the plasma membrane. In LM, the immunolabel produced punctate fluorescence in hair bundles. In TEM, immunogold particles were observed medially and distally on stereocilia of hair bundles. Dilute solutions of the antibody disrupted vibration sensitivity in anemones. We conclude that the cadherin 23-like polypeptide likely contributes to the mechanotransduction apparatus of hair bundle mechanoreceptors of anemones.

Keywords

Hair cell Tip link Sensory transduction 

Notes

Acknowledgments

We appreciate financial support from NSF IOB0542574 and critical comments on the original manuscript by two anonymous reviewers.

References

  1. Abedin M, King N (2008) The premetazoan ancestry of cadherins. Science 319:946–948PubMedCrossRefGoogle Scholar
  2. Ahmed ZM, Goodyear R, Riazuddin S, Lagziel A, Legan PK, Behra M, Burgess SM, Lilley KS, Wilcox ER, Riazuddin S, Griffith AJ, Frolenkov GJ, Belyantseva IA, Richardson GP, Friedman TB (2006) The tip link antigen, a protein associated with the transduction complex of sensory hair cells, is protocadherin 15. J Neurosci 26:7022–7034PubMedCrossRefGoogle Scholar
  3. Ashmore JF (1991) The electrophysiology of hair cells. Annu Rev Physiol 53:465–476PubMedCrossRefGoogle Scholar
  4. Assad JA, Shepherd GM, Corey DP (1991) Tip-link integrity and mechanical transduction in vertebrate hair cells. Neuron 7:985–994PubMedCrossRefGoogle Scholar
  5. Bolz H, von Brederlow B, Ramirez A, Bryda EC, Kutsche K, Nothwang HG, Seeliger M, Cabrera M, Vila MC, Molina OP (2001) Mutation of CDH23, encoding a new member of the cadherin gene family, causes Usher syndrome type 1D. Nat Genet 27:108–112PubMedCrossRefGoogle Scholar
  6. Bork JM, Peters LM, Riazuddin S, Bernstein SL, Ahmed ZM, Ness SL, Polomeno R, Ramesh A, Schloss M, Srisailpathy CR (2001) Usher syndrome 1D and nonsyndromic autosomal recessive deafness DFNB12 are caused by allelic mutations of the novel cadherin-like gene CDH23. Am J Hum Genet 68:26–37PubMedCrossRefGoogle Scholar
  7. Di Palma F, Holme RH, Bryda EC, Belyantseva IA, Pellegrino R, Kachar B, Steel KP, Noben-Trauth K (2001) Mutations in Cdh23, encoding a new type of cadherin, cause stereocilia disorganization in waltzer, the mouse model for Usher syndrome type 1D. Nat Genet 27:103–107PubMedCrossRefGoogle Scholar
  8. Furness DN, Hackney CM (1985) Cross-links between stereocilia in the guinea pig cochlea. Hear Res 18:177–188PubMedCrossRefGoogle Scholar
  9. Howard J, Roberts WM, Hudspeth AJ (1988) Mechanoelectrical transduction by hair cells. Annu Rev Biophys Chem 17:99–124CrossRefGoogle Scholar
  10. Hudspeth AJ (1985) The cellular basis of hearing: the biophysics of hair cells. Science 230:745–752PubMedCrossRefGoogle Scholar
  11. Hudspeth AJ (1997) How hearing happens. Neuron 19:947–950PubMedCrossRefGoogle Scholar
  12. Kachar B, Parrakal M, Kurc M, Zhao Y, Gillespie PG (2000) High-resolution structure of hair-cell tip-links. Proc Natl Acad Sci USA 97:13336–13341PubMedCrossRefGoogle Scholar
  13. Kazmierczak P, Sakaguchi H, Tokita J, Wilson-Kubalek EM, Milligan RA, Muller U, Kachar B (2007) Cadherin 23 and protocadherin 15 interact to form tip-link filaments in sensory hair cells. Nature 449:87–91PubMedCrossRefGoogle Scholar
  14. Lagziel A, Ahmed ZM, Schultz JM, Morell RJ, Belyantseva IA, Friedman TB (2005) Spatiotemporal pattern and isoforms of cadherin 23 in wild type and waltzer mice during inner ear hair cell development. Dev Biol 280:295–306PubMedCrossRefGoogle Scholar
  15. LeMasurier M, Gillespie PG (2005) Hair-cell mechanotransduction and cochlear amplification. Neuron 48:403–415PubMedCrossRefGoogle Scholar
  16. Mariscal RN (1974) Nematocysts. In: Muscatine L, Lenhoff HM (eds) Coelenterate biology, reviews and new perspectives. Academic, New York, pp 129–178Google Scholar
  17. 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 280:281–294PubMedCrossRefGoogle Scholar
  18. 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 157:478–493CrossRefGoogle Scholar
  19. Mire P, Nasse J (2002) Hair bundle motility induced by chemoreceptors in anemones. Hear Res 163:111–120PubMedCrossRefGoogle Scholar
  20. 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 268:281–292CrossRefGoogle Scholar
  21. Namimatsu S, Ghazizadeh M, Sugisaki Y (2005) Reversing the effects of formalin fixation with citraconic anhydride and heat: a universal antigen retrieval method. J Histochem Cytochem 53:3–11PubMedCrossRefGoogle Scholar
  22. Nicolson T, Rusch A, Friedrich RW, Granato M, Ruppersberg JP, Nüsslein-Volhand C (1998) Genetic analysis of vertebrate sensory hair cell mechanosensation: the zebrafish circler mutants. Neuron 20:271–283PubMedCrossRefGoogle Scholar
  23. Osborne MP, Comis SD, Pickles JO (1988) Further observations on the fine structure of tip links between stereocilia of the guinea pig cochlea. Hear Res 35:99–108PubMedCrossRefGoogle Scholar
  24. Peteya DJ (1975) The ciliary-cone sensory cell of anemones and cerianthids. Tissue Cell 7:243–252PubMedCrossRefGoogle Scholar
  25. Pickles JO, Comis SD, Osborne MP (1984) Cross-links between stereocilia in the guinea pig Organ of Corti, and their possible relation to sensory transduction. Hear Res 15:103–112PubMedCrossRefGoogle Scholar
  26. Preyer S, Hemmert W, Zenner HP, Gummer AW (1995) Abolition of the receptor potential response of isolated mammalian outer hair cells by hair-bundle treatment with elastase: a test of the tip-link hypothesis. Hear Res 89:187–193PubMedCrossRefGoogle Scholar
  27. Roberts WM, Howard J, Hudspeth AJ (1988) Hair cells: transduction, tuning, and transmission in the inner ear. Annu Rev Cell Biol 4:63–92PubMedCrossRefGoogle Scholar
  28. 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 428:950–955PubMedCrossRefGoogle Scholar
  29. Slepecky N, Chamberlain SC (1985) The cell coat of inner ear sensory and supporting cells as demonstrated by ruthenium red. Hear Res 17:281–288PubMedCrossRefGoogle Scholar
  30. 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 428:955–959PubMedCrossRefGoogle Scholar
  31. Sotomayor M, Corey DP, Schulten K (2005) In search of the hair cell gating spring: elastic properties of ankyrin and cadherin repeats. Structure 13:669–682PubMedCrossRefGoogle Scholar
  32. Tsuprun V, Goodyear RJ, Richardson GP (2004) The structure of tip links and kinocilial links in avian sensory hair bundles. Biophys J 87:4106–4112PubMedCrossRefGoogle Scholar
  33. Watson GM, Hessinger DA (1989) Cnidocyte mechanoreceptors are tuned to the movements of swimming prey by chemoreceptors. Science 243:1589–1591PubMedCrossRefGoogle Scholar
  34. Watson GM, Mire P (2004) Dynamic tuning of hair bundle mechanoreceptors in a sea anemone during predation. Hydrobiologica 530(531):123–128CrossRefGoogle Scholar
  35. Watson GM, Mire P, Hudson RR (1997) Hair bundles of sea anemones as a model system for vertebrate hair bundles. Hear Res 107:53–66PubMedCrossRefGoogle Scholar
  36. Watson GM, Mire P, Hudson RR (1998a) Repair of hair bundles in sea anemones by secreted proteins. Hear Res 115:119–128PubMedCrossRefGoogle Scholar
  37. Watson GM, Mire P, Hudson RR (1998b) Frequency specificity of vibration dependent discharge of nematocysts in sea anemones. J Exp Zool 281:582–593PubMedCrossRefGoogle Scholar
  38. 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 94:15469–15474CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Glen M. Watson
    • 1
    Email author
  • Lankhanh Pham
    • 1
  • Erin M. Graugnard
    • 1
  • Patricia Mire
    • 1
  1. 1.Department of BiologyUniversity of Louisiana at LafayetteLafayetteUSA

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