Skip to main content
SpringerLink
Log in

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

  • Original Paper
  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

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.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11

Similar content being viewed by others

References

  • Abedin M, King N (2008) The premetazoan ancestry of cadherins. Science 319:946–948

    Article  PubMed  CAS  Google Scholar 

  • 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 26:7022–7034

    Article  PubMed  CAS  Google Scholar 

  • Ashmore JF (1991) The electrophysiology of hair cells. Annu Rev Physiol 53:465–476

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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 27:108–112

    Article  PubMed  CAS  Google Scholar 

  • 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 68:26–37

    Article  PubMed  CAS  Google Scholar 

  • 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 27:103–107

    Article  PubMed  CAS  Google Scholar 

  • Furness DN, Hackney CM (1985) Cross-links between stereocilia in the guinea pig cochlea. Hear Res 18:177–188

    Article  PubMed  CAS  Google Scholar 

  • Howard J, Roberts WM, Hudspeth AJ (1988) Mechanoelectrical transduction by hair cells. Annu Rev Biophys Chem 17:99–124

    Article  CAS  Google Scholar 

  • Hudspeth AJ (1985) The cellular basis of hearing: the biophysics of hair cells. Science 230:745–752

    Article  PubMed  CAS  Google Scholar 

  • Hudspeth AJ (1997) How hearing happens. Neuron 19:947–950

    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 

  • 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 449:87–91

    Article  PubMed  CAS  Google Scholar 

  • 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 280:295–306

    Article  PubMed  CAS  Google Scholar 

  • LeMasurier M, Gillespie PG (2005) Hair-cell mechanotransduction and cochlear amplification. Neuron 48:403–415

    Article  PubMed  CAS  Google Scholar 

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

    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 P, Nasse J (2002) Hair bundle motility induced by chemoreceptors in anemones. Hear Res 163:111–120

    Article  PubMed  CAS  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 

  • 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 53:3–11

    Article  PubMed  CAS  Google Scholar 

  • 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 20:271–283

    Article  PubMed  CAS  Google Scholar 

  • 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 35:99–108

    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 

  • 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 15:103–112

    Article  PubMed  CAS  Google Scholar 

  • 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 89:187–193

    Article  PubMed  CAS  Google Scholar 

  • Roberts WM, Howard J, Hudspeth AJ (1988) Hair cells: transduction, tuning, and transmission in the inner ear. Annu Rev Cell Biol 4:63–92

    Article  PubMed  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 

  • Slepecky N, Chamberlain SC (1985) The cell coat of inner ear sensory and supporting cells as demonstrated by ruthenium red. Hear Res 17:281–288

    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

    Article  PubMed  CAS  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 (1989) Cnidocyte mechanoreceptors are tuned to the movements of swimming prey by chemoreceptors. Science 243:1589–1591

    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  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 

  • 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 

Download references

Acknowledgments

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

Author information

Authors and Affiliations

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

    Glen M. Watson, Lankhanh Pham, Erin M. Graugnard & Patricia Mire

Authors
  1. Glen M. Watson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lankhanh Pham
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Erin M. Graugnard
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Patricia Mire
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Glen M. Watson.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Watson, G.M., Pham, L., Graugnard, E.M. et al. Cadherin 23-like polypeptide in hair bundle mechanoreceptors of sea anemones. J Comp Physiol A 194, 811–820 (2008). https://doi.org/10.1007/s00359-008-0352-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00359-008-0352-0

Keywords

Search

Navigation