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Evidence for involvement of TRPA1 in the detection of vibrations by hair bundle mechanoreceptors in sea anemones

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Abstract

A homolog of TRPA1 was identified in the genome of the anemone, Nematostella vectensis (nv-TRPA1a), and predicted to possess six ankyrin repeat domains at the N-terminus and an ion channel domain near the C-terminus. Transmembrane segments of the ion channel domain are well conserved among several known TRPA1 polypeptides. Inhibitors of TRPA1 including ruthenium red decrease vibration-dependent discharge of nematocysts in N. vectensis and Haliplanella luciae. Activators of TRPA1 including URB-597 and polygodial increase nematocyst discharge in the absence of vibrations. Co-immunoprecipitation yields a band on SDS-PAGE gels at the predicted mass of the nv-TRPA1a polypeptide among other bands. Co-immunoprecipitation performed in the presence of antigenic peptide decreases the yield of this and several other polypeptides. In untreated controls, anti-nv-TRPA1a primarily labels the base of the hair bundle with some labeling also distributed along the length of stereocilia. Tissue immunolabeled in the presence of the antigenic peptide exhibits reduced labeling. Activating chemoreceptors for N-acetylated sugars induce immunolabel to distribute distally in stereocilia. In anemones, activating chemoreceptors for N-acetylated sugars induce hair bundles to elongate among several other structural and functional changes. Taken together, these results are consistent with the possibility that nv-TRPA1a participates in signal transduction of anemone hair bundles.

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References

  • Ahmed ZM, Goodyear R, Riazuddin Sa, Lagziel A, Legan PK, Behra M, Burgess SM, Lilley KS, Wilcox ER, Riazuddin Sh, 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 

  • Asai Y, Holt JR, Geleoc GSG (2010) A quantitative analysis of the spatiotemporal pattern of transient receptor potential gene expression in the developing mouse cochlea. JARO 11:27–37

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Christensen AP, Corey DP (2007) TRP channels in mechanosensation: direct or indirect activation? Nat Rev Neurosci 7:510–521

    Article  Google Scholar 

  • Corey DP (2006) What is the hair cell transduction channel? J Physiol 576:23–28

    Article  PubMed  CAS  Google Scholar 

  • Corey DP, Garcia-Anoveros J, Holt JR, Kwan KY, Lin S-Y, Vollrath MA, Amalfitano A, Cheung EL-M, Derfler BH, Duggan A, Geleoc GSG, Gray PA, Hoffman MP, Rehm H, Tamasaukas D, Zhang D-S (2004) TRPA1 is a candidate for the mechanosensitive transduction channel of vertebrate hair cells. Nature 432:723–730

    Article  PubMed  CAS  Google Scholar 

  • Deutscher D, Meilijson I, Schuster S, Ruppin E (2008) Can single knockouts accurately single out gene functions? BMC Syst Biol 2:50

    Article  PubMed  Google Scholar 

  • Escalera J, vonHehn CA, Bessac BF, Sivula M, Jordt SE (2008) TRPA1 mediates the noxious effects of natural sesquiterpene deterrents. J Biol Chem 283:24136–24144

    Article  PubMed  CAS  Google Scholar 

  • Farris HE, LeBlanc CL, Goswami J, Ricci AJ (2004) Probing the pore of the auditory hair cell mechanotransducer channel in turtle. J Physiol 558:769–792

    Article  PubMed  CAS  Google Scholar 

  • Fettiplace R (2009) Defining features of the mechanoelectrical transducer channel. Pflugers Arch 458:1115–1123

    Article  PubMed  CAS  Google Scholar 

  • Finn RD, Mistry J, Schuster-Böckler B, Griffiths-Jones S, Hollich V, Lassmann T, Moxon S, Marshall M, Khanna A, Durbin R, Eddy SR, Sonnhammer ELL, Bateman A (2006) Pfam: clans, web tools and services. Nucleic Acids Res 34:D247–D251

    Article  PubMed  CAS  Google Scholar 

  • Germain G, Anctil M (1996) Evidence for intercellular coupling and connexin-like protein in the luminescent endoderm of Renilla koellikeri (Cnidaria, Anthozoa). Biol Bull 191:353–366

    Article  Google Scholar 

  • Gillespie PG, Muller U (2009) Mechanosensation by hair cells: models, molecules, and mechanisms. Cell 139:33–44

    Article  PubMed  CAS  Google Scholar 

  • Hand C, Uhlinger KR (1992) The culture, sexual and asexual reproduction, and growth of the sea anemone Nematostella vectensis. Biol Bull 182:169–176

    Article  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 

  • Kahsay RY, Gao G, Liao L (2005) An improved hidden Markov model for transmembrane protein detection and topology prediction and its application to complete genomes. Bioinformatics 21:1853–1858

    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 

  • Krayesky SL, Mahoney JL, Kinler KM, Peltier S, Calais W, Allaire K, Watson GM (2010) Regulation of spirocyst discharge in the model sea anemone Nematostella vectensis. Mar Biol 157:1041–1047

    Article  CAS  Google Scholar 

  • Kwan KY, Allchorne AJ, Vollrath MA, Christensen AP, Zhang DS, Woolf CJ, Corey DP (2006) TRPA1 contributes to cold, mechanical, and chemical nociception but is not essential for hair cell transduction. Neuron 50:277–289

    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 

  • Minasian LL Jr, Mariscal RN (1979) Characteristics and regulation of fission activity in clonal cultures of the cosmopolitan sea anemone Haliplanella luciae. 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 P, Watson GM (1997) Mechanotransduction of hair bundles arising from multicellular complexes in anemones. Hear Res 113:224–234

    Article  PubMed  CAS  Google Scholar 

  • Mire P, Nasse J, Venable-Thibodeaux S (2000) Gap junctional communication in the vibration-sensitive response of sea anemones. Hear Res 144:109–123

    Article  PubMed  CAS  Google Scholar 

  • Mire-Thibodeaux P, Watson GM (1993) Direct monitoring of intracellular calcium ions in sea anemone tentacles suggests regulation of nematocyst discharge by remote, rare epidermal cells. Biol Bull 185:335–345

    Article  Google Scholar 

  • Mire-Thibodeaux P, Watson GM (1994a) Cyclical morphodynamics of hair bundles in sea anemones: second messenger pathways. J Exp Zool 270:517–526

    Article  Google Scholar 

  • Mire-Thibodeaux P, Watson GM (1994b) Morphodynamic hair bundles arising from sensory cell/supporting cell complexes frequency-tune nematocyst discharge in sea anemones. J Exp Zool 268:282–292

    Article  PubMed  CAS  Google Scholar 

  • Nagata K, Duggan A, Kumar G, Garcia-Anoveros J (2005) Nociceptor and hair cell transducer properties of TRPA1, a channel for pain and hearing. J Neurosci 25:4052–4061

    Article  PubMed  CAS  Google Scholar 

  • Niforatos W, Zhang XF, Lake MR, Walter KA, Neelands T, Holzman TF, Scott VE, Faltynek CR, Moreland RB, Chen J (2007) Activation of TRPA1 channels by the fatty acid amide hydrolase inhibitor 3′-carbamoylbiphenyl-3yl cyclohexylcarbamate (URB597). Mol Pharmacol 71:1209–1216

    Article  PubMed  CAS  Google Scholar 

  • Owsianik G, D’hoedt D, Voets T, Nilius B (2006) Structure–function relationship of the TRP superfamily. Rev Physiol Biochem Pharmacol 156:61–90

    Article  PubMed  CAS  Google Scholar 

  • Ozacmak VH, Thorington GU, Fletcher WH, Hessinger DA (2001) N-acetylneuraminic acid (NANA) stimulates in situ cyclic AMP production in tentacles of the sea anemone (Aiptasia pallida): possible role in chemosensitization of nematocyst discharge. J Exp Biol 204:2011–2020

    PubMed  CAS  Google Scholar 

  • Prober DA, Zimmerman S, Myers BR, McDermott BM Jr, Kim SH, Caron S, Rihel J, Solnica-Krezel L, Julius D, Hudspeth AJ, Schler AF (2008) Zebrafish TRPA1 channels are required for chemosensation but not for thermosensation or mechanosensory hair cell function. J Neurosci 28:10102–10110

    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 

  • Russell TJ, Watson GM (1995) Evidence for intracellular stores of calcium ions involved in regulating nematocyst discharge. J Exp Zool 273:175–185

    Article  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 

  • Staruschenko A, Jeske NA, Akopian AN (2010) Contribution of TRPV1-TRPA1 interaction to single channel properties of the TRPA1 channel. J Biol Chem 285:15167–15177

    Article  PubMed  CAS  Google Scholar 

  • Sullivan JC, Ryan JF, Watson JA, Webb J, Mullikan JC, Rokhsar D, Finnerty JR (2006) Stellabase: The Nematostella vectensis genomics database. Nucleic Acids Res 34:D495–D499

    Article  PubMed  CAS  Google Scholar 

  • Thorington GU, Hessinger DA (1988) Control of cnida discharge: I. Evidence for two classes of chemoreceptor. Biol Bull 174:163–171

    Article  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, Hessinger DA (1992) Receptors for N-acetylated sugars may stimulate adenylate cyclase to sensitize and tune mechanoreceptors involved in triggering nematocyst discharge. Exp Cell Res 198:8–16

    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, Roberts J (1995) Chemoreceptor-mediated polymerization and depolymerization of actin in hair bundles of sea anemones. Cell Motility Cytoskeleton 30:208–220

    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 (1998) Frequency specificity of vibration dependent discharge of nematocysts in sea anemones. J Exp Zool 281:582–593

    Article  PubMed  CAS  Google Scholar 

  • Watson GM, Pham L, Graugnard EM, Mire P (2008) Cadherin 23-like polypeptide in hair bundle mechanoreceptors of sea anemones. J Comp Physiol Ser A 194:811–820

    Article  CAS  Google Scholar 

  • Watson GM, Mire P, Kinler KM (2009) Mechanosensitivity in the model sea anemone Nematostella vectensis. Mar Biol 156:2129–2137

    Article  Google Scholar 

Download references

Acknowledgments

We appreciate the financial support from the US National Science Foundation, IOB0542574 and the diligence of the two anonymous reviewers.

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Authors and Affiliations

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

    Janna L. Mahoney, Erin M. Graugnard, Patricia Mire & Glen M. Watson

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  1. Janna L. Mahoney
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  2. Erin M. Graugnard
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  3. Patricia Mire
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  4. Glen M. Watson
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Correspondence to Glen M. Watson.

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Mahoney, J.L., Graugnard, E.M., Mire, P. et al. Evidence for involvement of TRPA1 in the detection of vibrations by hair bundle mechanoreceptors in sea anemones. J Comp Physiol A 197, 729–742 (2011). https://doi.org/10.1007/s00359-011-0636-7

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  • DOI: https://doi.org/10.1007/s00359-011-0636-7

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