Skip to main content
PMC home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1993 Aug 1;90(15):7419–7423. doi: 10.1073/pnas.90.15.7419

Deduced amino acid sequence of a putative sodium channel from the scyphozoan jellyfish Cyanea capillata.

P A Anderson 1, M A Holman 1, R M Greenberg 1
PMCID: PMC47149  PMID: 8394021

Abstract

Members of the phylum Cnidaria are the lowest extant organisms to possess a nervous system and are the first that are known to contain cells that produce action potentials carried exclusively by Na+ ions. They thus occupy an important position in the evolution of Na+ channels. A cDNA encoding a 198-kDa protein with high sequence identity to known Na+ channels was isolated from the scyphozoan jellyfish Cyanea capillata. The similarity between this and other Na+ channels is greatest in the transmembrane segments and the putative pore region and less so in the cytoplasmic loops that link the four domains of the protein. Phylogenetic analysis of the deduced protein reveals that it is closely related to known Na+ channels, particularly those of squid and Drosophila, and more distantly separated from Ca2+ channels. Scrutiny of the Cyanea channel in regions corresponding to those purported to form the tetrodotoxin receptor and selectivity filter of Na+ channels in higher animals reveals several anomalies that suggest that current models of the location of the tetrodotoxin binding site and Na+ channel selectivity filter are incomplete.

Full text

PDF
7419

Images in this article

7421Fig. 1
on p.7421
7422Fig. 2
on p.7422
7422Fig. 3
on p.7422

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Auld V. J., Goldin A. L., Krafte D. S., Catterall W. A., Lester H. A., Davidson N., Dunn R. J. A neutral amino acid change in segment IIS4 dramatically alters the gating properties of the voltage-dependent sodium channel. Proc Natl Acad Sci U S A. 1990 Jan;87(1):323–327. doi: 10.1073/pnas.87.1.323. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Backx P. H., Yue D. T., Lawrence J. H., Marban E., Tomaselli G. F. Molecular localization of an ion-binding site within the pore of mammalian sodium channels. Science. 1992 Jul 10;257(5067):248–251. doi: 10.1126/science.1321496. [DOI] [PubMed] [Google Scholar]
  3. Chirgwin J. M., Przybyla A. E., MacDonald R. J., Rutter W. J. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry. 1979 Nov 27;18(24):5294–5299. doi: 10.1021/bi00591a005. [DOI] [PubMed] [Google Scholar]
  4. Grabner M., Friedrich K., Knaus H. G., Striessnig J., Scheffauer F., Staudinger R., Koch W. J., Schwartz A., Glossmann H. Calcium channels from Cyprinus carpio skeletal muscle. Proc Natl Acad Sci U S A. 1991 Feb 1;88(3):727–731. doi: 10.1073/pnas.88.3.727. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Han J. H., Rutter W. J. Lambda gt22, an improved lambda vector for the directional cloning of full-length cDNA. Nucleic Acids Res. 1987 Aug 11;15(15):6304–6304. doi: 10.1093/nar/15.15.6304. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Heinemann S. H., Terlau H., Stühmer W., Imoto K., Numa S. Calcium channel characteristics conferred on the sodium channel by single mutations. Nature. 1992 Apr 2;356(6368):441–443. doi: 10.1038/356441a0. [DOI] [PubMed] [Google Scholar]
  7. Higgins D. G., Bleasby A. J., Fuchs R. CLUSTAL V: improved software for multiple sequence alignment. Comput Appl Biosci. 1992 Apr;8(2):189–191. doi: 10.1093/bioinformatics/8.2.189. [DOI] [PubMed] [Google Scholar]
  8. Kao C. Y. Structure-activity relations of tetrodotoxin, saxitoxin, and analogues. Ann N Y Acad Sci. 1986;479:52–67. doi: 10.1111/j.1749-6632.1986.tb15561.x. [DOI] [PubMed] [Google Scholar]
  9. Kozak M. Compilation and analysis of sequences upstream from the translational start site in eukaryotic mRNAs. Nucleic Acids Res. 1984 Jan 25;12(2):857–872. doi: 10.1093/nar/12.2.857. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Lipman D. J., Pearson W. R. Rapid and sensitive protein similarity searches. Science. 1985 Mar 22;227(4693):1435–1441. doi: 10.1126/science.2983426. [DOI] [PubMed] [Google Scholar]
  11. Lopez G. A., Jan Y. N., Jan L. Y. Hydrophobic substitution mutations in the S4 sequence alter voltage-dependent gating in Shaker K+ channels. Neuron. 1991 Aug;7(2):327–336. doi: 10.1016/0896-6273(91)90271-z. [DOI] [PubMed] [Google Scholar]
  12. Meech R. W., Mackie G. O. Ionic currents in giant motor axons of the jellyfish, Aglantha digitale. J Neurophysiol. 1993 Mar;69(3):884–893. doi: 10.1152/jn.1993.69.3.884. [DOI] [PubMed] [Google Scholar]
  13. Mikami A., Imoto K., Tanabe T., Niidome T., Mori Y., Takeshima H., Narumiya S., Numa S. Primary structure and functional expression of the cardiac dihydropyridine-sensitive calcium channel. Nature. 1989 Jul 20;340(6230):230–233. doi: 10.1038/340230a0. [DOI] [PubMed] [Google Scholar]
  14. Noda M., Ikeda T., Kayano T., Suzuki H., Takeshima H., Kurasaki M., Takahashi H., Numa S. Existence of distinct sodium channel messenger RNAs in rat brain. Nature. 1986 Mar 13;320(6058):188–192. doi: 10.1038/320188a0. [DOI] [PubMed] [Google Scholar]
  15. Noda M., Shimizu S., Tanabe T., Takai T., Kayano T., Ikeda T., Takahashi H., Nakayama H., Kanaoka Y., Minamino N. Primary structure of Electrophorus electricus sodium channel deduced from cDNA sequence. Nature. 1984 Nov 8;312(5990):121–127. doi: 10.1038/312121a0. [DOI] [PubMed] [Google Scholar]
  16. Noda M., Suzuki H., Numa S., Stühmer W. A single point mutation confers tetrodotoxin and saxitoxin insensitivity on the sodium channel II. FEBS Lett. 1989 Dec 18;259(1):213–216. doi: 10.1016/0014-5793(89)81531-5. [DOI] [PubMed] [Google Scholar]
  17. Rogart R. B., Cribbs L. L., Muglia L. K., Kephart D. D., Kaiser M. W. Molecular cloning of a putative tetrodotoxin-resistant rat heart Na+ channel isoform. Proc Natl Acad Sci U S A. 1989 Oct;86(20):8170–8174. doi: 10.1073/pnas.86.20.8170. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Satin J., Kyle J. W., Chen M., Bell P., Cribbs L. L., Fozzard H. A., Rogart R. B. A mutant of TTX-resistant cardiac sodium channels with TTX-sensitive properties. Science. 1992 May 22;256(5060):1202–1205. doi: 10.1126/science.256.5060.1202. [DOI] [PubMed] [Google Scholar]
  19. Sato C., Matsumoto G. Primary structure of squid sodium channel deduced from the complementary DNA sequence. Biochem Biophys Res Commun. 1992 Jul 15;186(1):61–68. doi: 10.1016/s0006-291x(05)80775-2. [DOI] [PubMed] [Google Scholar]
  20. Strong M., Chandy K. G., Gutman G. A. Molecular evolution of voltage-sensitive ion channel genes: on the origins of electrical excitability. Mol Biol Evol. 1993 Jan;10(1):221–242. doi: 10.1093/oxfordjournals.molbev.a039986. [DOI] [PubMed] [Google Scholar]
  21. Stühmer W., Conti F., Suzuki H., Wang X. D., Noda M., Yahagi N., Kubo H., Numa S. Structural parts involved in activation and inactivation of the sodium channel. Nature. 1989 Jun 22;339(6226):597–603. doi: 10.1038/339597a0. [DOI] [PubMed] [Google Scholar]
  22. Tanabe T., Takeshima H., Mikami A., Flockerzi V., Takahashi H., Kangawa K., Kojima M., Matsuo H., Hirose T., Numa S. Primary structure of the receptor for calcium channel blockers from skeletal muscle. Nature. 1987 Jul 23;328(6128):313–318. doi: 10.1038/328313a0. [DOI] [PubMed] [Google Scholar]
  23. Terlau H., Heinemann S. H., Stühmer W., Pusch M., Conti F., Imoto K., Numa S. Mapping the site of block by tetrodotoxin and saxitoxin of sodium channel II. FEBS Lett. 1991 Nov 18;293(1-2):93–96. doi: 10.1016/0014-5793(91)81159-6. [DOI] [PubMed] [Google Scholar]
  24. West J. W., Patton D. E., Scheuer T., Wang Y., Goldin A. L., Catterall W. A. A cluster of hydrophobic amino acid residues required for fast Na(+)-channel inactivation. Proc Natl Acad Sci U S A. 1992 Nov 15;89(22):10910–10914. doi: 10.1073/pnas.89.22.10910. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES