Skip to main content
Springer Nature Link
Log in

Structure of a putative sodium channel from the sea anemoneAiptasia pallida

  • Original Articles
  • Published:
Invertebrate Neuroscience

Abstract

A cDNA encoding a full length putative sodium channel has been cloned from the sea anemoneAiptasia pallida. The deduced protein, named AiNal, has a predicted molecular weight of 205 000 Da. It shows high structural similarity to other sodium channels from both invertebrates and vertebrates, and its structure is consistent with the four domain, six transmembrane segment motif of all known voltage-gated sodium channels. In the region purported to constitute the tetrodotoxin (TTX) receptor of sodium channels, AiNal differs from the TTX-sensitive motif, suggesting that currents carried by this channel would be insensitive to TTX. The presence of a conventional sodium channel protein in anemones indicates, for the first time, that neurons in sea anemones are likely to be capable of producing fast, overshooting action, potentials.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Anderson, P. A. V. (1985) Physiology of a bidirectional, excitatory, chemical synapse.J. Neurophysiol.,53, 821–835.

    PubMed  CAS  Google Scholar 

  • Anderson, P. A. V. (1987) Properties and pharmacology of a TTX-insensitive Na+ current in neurones of the jellyfish Cyanea capillata.J. Exp. Biol.,133, 231–248.

    Google Scholar 

  • Anderson, P. A. V. (1990) Ionic currents in the scyphozoa. InEvolution of the First Nervous Systems, ed. Peter A. V. Anderson, pp. 267–280. New York: Plenum Press.

    Google Scholar 

  • Anderson, P. A. V. and Schwah, W. E. (1984) An epithelial cell-free preparation of the motor nerve net of Cyanea (Coelenterata: Scyphozoa).Biol. Bull.,166, 396–408.

    Article  Google Scholar 

  • Anderson, P. A. V., Holman, M. A. and Greenberg, R. M. (1993) Deduced amino acid sequence of a putative sodium channel from the scyphozoan jellyfish Cyanea capillata.Proc. Natl. Acad. Sci. USA,90, 7419–7423.

    Article  PubMed  CAS  Google Scholar 

  • Bennett, E., Urcan, M. S., Tinkle, S. S., Koszowski, A. G. and Levinson, S. R. (1997) Contribution of sialic acid to the voltage-dependence of sodium channel gating.J. Gen. Physiol.,109, 327–343.

    Article  PubMed  CAS  Google Scholar 

  • Blair, K. L. and Anderson, P. A. V. (1993) Properties of voltage-activated ionic currents in cells from the brains of the triclad flatwormBdelloura candida.J. Exp. Biol.,185, 267–286.

    Google Scholar 

  • Blin, N. and Stafford, D. W. (1976) A general method for isolation of high molecular weight DNA from eukaryotes.Nucl. Acids Res.,3, 2303–2308.

    PubMed  CAS  Google Scholar 

  • Brusca, R. C. and Brusca, G. J. (1990).Invertebrates Sunderland, Mass: Sinauer Assoc.

    Google Scholar 

  • Byerly, L., and Moody, W. J. (1984) Intracellular calcium ions and calcium currents in perfused neurones of the snail,Lymnaea stagnalis, J. Physiol. (Lond.),352, 637–652.

    CAS  Google Scholar 

  • Catterall, W. A. (1995) Structure and function of voltage-gated ion channels.Ann. Rev. Biochem.,64, 493–531.

    Article  PubMed  CAS  Google Scholar 

  • Chandy, K. G. and Gutman, G. A. (1995) Voltage-gated potassium channel genes. In:Ligand and Voltage-Gated Ion Channels, ed. R. A. North, pp. 1–71.Handbook of Receptors and Channels. Boca Raton: CRC Press.

    Google Scholar 

  • Cho, K., and McFarlane, I. D. (1996) The anthozoan neuropeptide Antho-RWamide I modulates Ca2+ current in sea anemone myoepithelial cells.Neurosci Letts.209, 53–56.

    Article  CAS  Google Scholar 

  • Conner, J. A., and Stevens, C. F. (1971) Prediction of repetitive firing behaviour from voltage clamp data on an isolated neurone soma.J. Physiol. (Lond.),213, 1–19.

    Google Scholar 

  • Feng, G., Deák, P., Chopra, M. and Hall, L. M. (1995) Cloning and functional analysis of TipE, a novel membrane protein that enhancesDrosophila para sodium channel function.Cell,82, 1001–1011.

    Article  PubMed  CAS  Google Scholar 

  • Frohman, M. A. (1990) RACE: Rapid amplification of cDNA ends. InPCR Protocols, ed. M. A. Innis, D. H. Gelfand, J. J. Sninsky and T. J. White, pp. 28–38. San Diego: Academic Press.

    Google Scholar 

  • Goldin, A. L. (1995) Voltage-gated sodium channels. InLigand and Voltage-Gated Ion Channels, ed. R. A. North, pp. 73–112.Handbook of Receptors and Channels, Boca Raton: CRC Press.

    Google Scholar 

  • Hille, B. (1968) Pharmacological modifications of the sodium channels of frog nerve.J. Gen. Physiol.,51, 199–219.

    Article  PubMed  CAS  Google Scholar 

  • Holman, M., and Anderson, P. A. V. (1991) Voltage-activated ionic currents in myoepithelial cells from the sea anemoneCalliactis tricolor.J. Exp. Biol.,161, 333–346.

    CAS  Google Scholar 

  • Jakubcsak, R. S., Keith, C. H. and Porter, J. W. (1988) The neuropharmacology of photoreceptive pathway in corals.Soc. Neurosci. Abstr.,18, 375.

    Google Scholar 

  • Jeziorski, M. C., Greenberg, R. M. and Anderson, P. A. V. (1997) Cloning of a putative voltage-gated sodium channel from the turbellarian flatwormBdelloura candida.Parasitology,115, 289–96.

    Article  PubMed  CAS  Google Scholar 

  • Jeziorski, M. C., Greenberg, R. M., Clark, K. S. and Anderson, P. A. V. (1998) Cloning and functional expression of a voltage-gated calcium channel α1 subunit from jellyfish.J. Biol. Chem.,273, 22792–22799.

    Article  PubMed  CAS  Google Scholar 

  • Krishtal, O. A., Pidoplichko, V. I. and Shakhovalov, Y. A. (1981) Conductance of the calcium channel in the membrane of snail neurones.J. Physiol. (Lond.),310, 423–434.

    CAS  Google Scholar 

  • Kumar, S., Tamura, K. and Nei, M. (1993) MEGA: Molecular Evolutionary Genetics Analysis, version 1.0. The Pennsylvania University, University Park, PA 16802.

    Google Scholar 

  • Lipkind, G. M. and Fozzard, H. A. (1994) A structural model of the tetrodotoxin and saxitoxin binding site of the Na+ channel.Biophysical J.,66, 1–13.

    CAS  Google Scholar 

  • Mackie, G. O. (1965) Conduction in the nerve-free epithelia of siphonophores.Am. Zool.,5, 439–453.

    PubMed  CAS  Google Scholar 

  • Mackie, G. O. (1976) Propagated spikes in a coelenterate glandular epithelium.J. Gen. Physiol.,68, 313–325.

    Article  PubMed  CAS  Google Scholar 

  • Mackie, G. O. and Meech, R. W. (1985) Separate sodium and calcium spikes in the same axon.Nature,313, 791–793.

    Article  PubMed  CAS  Google Scholar 

  • Mackie, G. O. and Passano, L. M. (1968) Epithelial conduction in hydromedusae.J. Gen. Physiol.,52, 600–621.

    Article  PubMed  CAS  Google Scholar 

  • McFarlane, I. D. (1969) Two slow conduction systems in the sea anemoneCalliactis parasitica.J. Exp. Biol.,51, 377–385.

    PubMed  CAS  Google Scholar 

  • McFarlane, I. D. (1973) Spontaneous contractions and nerve net activity in the sea anemoneCalliactis parasitica.Mar. Behav. Physiol.,2, 97–113.

    Article  Google Scholar 

  • McFarlane, I. D. (1974) Excitatory and inhibitory control of inherent contractions in the sea anemoneCalliactis parasitica.J. Exp. Biol.,60, 397–422.

    PubMed  CAS  Google Scholar 

  • McFarlane, I. D. (1975) Control of mouth opening and pharynx protrusion during feeding in the sea anemoneCalliactis parasitica.J. Exp. Biol.,63, 615–626.

    PubMed  CAS  Google Scholar 

  • McFarlane, I. D., Graff, D. and Grimmelikhuijzen, C. J. P. (1987) Excitatory actions of Antho-RFamide, an anthozoan neuropeptide, on muscles and conducting systems in the sea anemoneCalliactis parasitica.J. Exp. Biol.,133, 157–168.

    CAS  Google Scholar 

  • Meech, R. W., and Mackie, G. O. (1993a) Ionic currents in giant motor axons of the jellyfishAglantha digitale.J. Neurophysiol.,69, 884–893.

    PubMed  CAS  Google Scholar 

  • Meech, R. W., and Mackie, G. O. (1993b) Potassium channel family in giant motor axons ofAglantha digitale.J. Neurophysiol.,69, 894–901.

    PubMed  CAS  Google Scholar 

  • Patton, D. E., West, J. W., Catterall, W. A. and Goldin, A. L. (1992) Amino acid residues required for fast Na+-channel inactivation: Charge neutralizations and deletions in the III–IV linker.Proc. Natl. Acad. Sci. USA,89, 10905–10909.

    Article  PubMed  CAS  Google Scholar 

  • Przysiezniak, J., and Spencer, A. N. (1992) Voltage-activated calcium currents in identified neurons from a hydrozoan jellyfish,Polyorchis pennicilatus.J. Neurosci.,12, 2065–2078.

    PubMed  CAS  Google Scholar 

  • Przysiezniak, J., and Spencer, A. N. (1994) Voltage-activated potassium currents in isolated motor neurons from the jellyfishPolyorchis pennicilatus.J. Neurophysiol.,72, 1010–1019.

    PubMed  CAS  Google Scholar 

  • Saitou, N. and Nei, M. (1987) The neighbour-joining method: a new method for reconstructing phylogenetic trees.Mol. Biol. Evol.,4, 406–425.

    PubMed  CAS  Google Scholar 

  • Sambrook, J., Fritsch, E. F. and Maniatis, T. (1989).Molecular Cloning: A Laboratory Manual, Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press.

    Google Scholar 

  • Saripalli, L. D., and Westfall, J. A. (1996). Classification of nerve cells dissociated from tentacles of the sea anemoneCalliactis parasitica.Biol. Bull.,190, 111–124.

    Article  Google Scholar 

  • Satin, J., Kyle, J. W., Chen, M., Bell, P., Cribbs, L. L., Fozzard, H. A. and Rogart, R. B. (1992) A mutant of TTX-resistant cardiac sodium channels with TTX-sensitive properties.Science,256, 1202–1205.

    Article  PubMed  CAS  Google Scholar 

  • Schetz, J. A., and Anderson, P. A. V. (1995) Glycosylation patterns of membrane proteins of the jellyfishCyanea capillata.Cell Tiss. Res.,279, 315–321.

    Article  CAS  Google Scholar 

  • Schrager, P., and Profera, C. (1973) Inhibition of the receptor for tetrodotoxin in nerve membranes by modifying carbonyl groups.Biochim. Biophys. Acta.,318, 141–146.

    Article  Google Scholar 

  • Schwartz, L. M., and Stuhmer, W. (1984) Voltage-dependent sodium chaanels in an invertebrate striated muscle.Science,225, 523–525.

    Article  PubMed  CAS  Google Scholar 

  • Spafford, J. D., Grigoriev, N. and Spencer, A. N. (1996). Pharmacological properties of voltage-gated Na+ currents in motor neurones from a hydrozoan jellyfishPolyorchis pennicilatus.J. Exp. Biol.,199, 941–948.

    PubMed  CAS  Google Scholar 

  • Stea, A., Soong, T. W. and Snutch, T. P. (1995) Voltage-gated calcium channels. InLigand and Voltage-Gated Ion Channels, ed. R. A. North, pp. 113–151.Handbook of Receptors and Channels, Boca Raton: CRC Press.

    Google Scholar 

  • Terlau, H., Heinemann, S. H., Stühmer, Pusch, M., Conti, F., Imoto, K. and Numa, S. (1991) Mapping the site of block by tetrodotoxin and saxitoxin of sodium channel II.FEBS,293 93–96.

    Article  CAS  Google Scholar 

  • Thompson, J. D., Higgins, D. G. and Gibson, T. J. (1994). CLUSTALW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice.Nucl. Acids Res.,22, 4673–4680.

    Article  PubMed  CAS  Google Scholar 

  • Warmke, J. W., Reenan, R. A. G., Wang, P., Qian, S., Arena, J. P., Wang, J., Wunderler, D., Liu, K., Kaczorowski, G. J., Van der Ploeg, L. H. T., Ganetsky, B. and Cohen, C. J. (1997) Functional expression ofDrosophila para sodium channels; modulation by the membrane protein TipE and toxin pharmacology.J. Gen. Physiol.,110, 119–133.

    Article  PubMed  CAS  Google Scholar 

  • West, J. W., Patton, D. E., Scheuer, T., Wang, Y., Goldin, A. L. and Catterall, W. A. (1992) A cluster of hydrophobic amino acid residues required for fast Na+ channel inactivation.Proc. Natl. Acad. Sci. USA,89, 10910–10914.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Whitney Laboratory, University of Florida, 9505 Ocean Shore Blvd., 32086, St. Augustine, Fl, USA

    Gena B. White, Arnold Pfahnl, Steven Haddock & Susanna Lamers

  2. Department of Physiology, University of Florida, 9505 Ocean Shore Blvd., 32086, St. Augustine, Fl, USA

    Peter A. V. Anderson

  3. Department of Neuroscience, University of Florida, 9505 Ocean Shore Blvd., 32086, St. Augustine, Fl, USA

    Robert M. Greenberg & Peter A. V. Anderson

Authors
  1. Gena B. White
    View author publications

    You can also search for this author inPubMed Google Scholar

  2. Arnold Pfahnl
    View author publications

    You can also search for this author inPubMed Google Scholar

  3. Steven Haddock
    View author publications

    You can also search for this author inPubMed Google Scholar

  4. Susanna Lamers
    View author publications

    You can also search for this author inPubMed Google Scholar

  5. Robert M. Greenberg
    View author publications

    You can also search for this author inPubMed Google Scholar

  6. Peter A. V. Anderson
    View author publications

    You can also search for this author inPubMed Google Scholar

Corresponding author

Correspondence to Peter A. V. Anderson.

Rights and permissions

Reprints and permissions

About this article

Cite this article

White, G.B., Pfahnl, A., Haddock, S. et al. Structure of a putative sodium channel from the sea anemoneAiptasia pallida . Invertebrate Neuroscience 3, 317–326 (1998). https://doi.org/10.1007/BF02577691

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02577691

Key Words