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. 1989 Mar;86(6):2079–2082. doi: 10.1073/pnas.86.6.2079

Two sodium-channel genes in Drosophila: implications for channel diversity.

M Ramaswami 1, M A Tanouye 1
PMCID: PMC286851  PMID: 2538830

Abstract

We describe two Drosophila melanogaster transcription units that are highly homologous to a rat Na+-channel cDNA. They appear to encode the major subunits of two distinct Na+-channel proteins. One of these maps to the second chromosome and is identical to a Na+-channel gene whose partial sequence has been previously reported [Salkoff, L., Butler, A., Wei, A., Scavarda, N., Giffen, K., Ifune, K., Goodman, R. & Mandel, G. (1987) Science 237, 744-749]. The other transcription unit maps to position 14C/D, on the X chromosome, close to the paralyzed (para) gene. Mutations in para affect membrane excitability in Drosophila neurons [Ganetzky, B. & Wu, C.F. (1986) Annu. Rev. Genet. 20, 13-44]. Sequence comparisons suggest that two Na+-channel genes arose early in evolution, before the divergence of vertebrate and invertebrate lines.

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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., Marshall J., Dunn J. M., Catterall W. A., Lester H. A., Davidson N., Dunn R. J. A rat brain Na+ channel alpha subunit with novel gating properties. Neuron. 1988 Aug;1(6):449–461. doi: 10.1016/0896-6273(88)90176-6. [DOI] [PubMed] [Google Scholar]
  2. Baumann A., Krah-Jentgens I., Müller R., Müller-Holtkamp F., Seidel R., Kecskemethy N., Casal J., Ferrus A., Pongs O. Molecular organization of the maternal effect region of the Shaker complex of Drosophila: characterization of an I(A) channel transcript with homology to vertebrate Na channel. EMBO J. 1987 Nov;6(11):3419–3429. doi: 10.1002/j.1460-2075.1987.tb02665.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Catterall W. A. Molecular properties of voltage-sensitive sodium channels. Annu Rev Biochem. 1986;55:953–985. doi: 10.1146/annurev.bi.55.070186.004513. [DOI] [PubMed] [Google Scholar]
  4. Feinberg A. P., Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem. 1983 Jul 1;132(1):6–13. doi: 10.1016/0003-2697(83)90418-9. [DOI] [PubMed] [Google Scholar]
  5. Ganetzky B. Genetic studies of membrane excitability in Drosophila: lethal interaction between two temperature-sensitive paralytic mutations. Genetics. 1984 Dec;108(4):897–911. doi: 10.1093/genetics/108.4.897. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Ganetzky B. Neurogenetic analysis of Drosophila mutations affecting sodium channels: synergistic effects on viability and nerve conduction in double mutants involving tip-E. J Neurogenet. 1986 Jan;3(1):19–31. doi: 10.3109/01677068609106892. [DOI] [PubMed] [Google Scholar]
  7. Ganetzky B., Wu C. F. Neurogenetics of membrane excitability in Drosophila. Annu Rev Genet. 1986;20:13–44. doi: 10.1146/annurev.ge.20.120186.000305. [DOI] [PubMed] [Google Scholar]
  8. Haimovich B., Schotland D. L., Fieles W. E., Barchi R. L. Localization of sodium channel subtypes in adult rat skeletal muscle using channel-specific monoclonal antibodies. J Neurosci. 1987 Sep;7(9):2957–2966. doi: 10.1523/JNEUROSCI.07-09-02957.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Jaimovich E., Ildefonse M., Barhanin J., Rougier O., Lazdunski M. Centruroides toxin, a selective blocker of surface Na+ channels in skeletal muscle: voltage-clamp analysis and biochemical characterization of the receptor. Proc Natl Acad Sci U S A. 1982 Jun;79(12):3896–3900. doi: 10.1073/pnas.79.12.3896. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Kamb A., Iverson L. E., Tanouye M. A. Molecular characterization of Shaker, a Drosophila gene that encodes a potassium channel. Cell. 1987 Jul 31;50(3):405–413. doi: 10.1016/0092-8674(87)90494-6. [DOI] [PubMed] [Google Scholar]
  11. Kamb A., Tseng-Crank J., Tanouye M. A. Multiple products of the Drosophila Shaker gene may contribute to potassium channel diversity. Neuron. 1988 Jul;1(5):421–430. doi: 10.1016/0896-6273(88)90192-4. [DOI] [PubMed] [Google Scholar]
  12. Llinás R., Sugimori M. Electrophysiological properties of in vitro Purkinje cell somata in mammalian cerebellar slices. J Physiol. 1980 Aug;305:171–195. doi: 10.1113/jphysiol.1980.sp013357. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Messing J. New M13 vectors for cloning. Methods Enzymol. 1983;101:20–78. doi: 10.1016/0076-6879(83)01005-8. [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. Papazian D. M., Schwarz T. L., Tempel B. L., Jan Y. N., Jan L. Y. Cloning of genomic and complementary DNA from Shaker, a putative potassium channel gene from Drosophila. Science. 1987 Aug 14;237(4816):749–753. doi: 10.1126/science.2441470. [DOI] [PubMed] [Google Scholar]
  17. Pardue M. L., Gall J. G. Nucleic acid hybridization to the DNA of cytological preparations. Methods Cell Biol. 1975;10:1–16. doi: 10.1016/s0091-679x(08)60727-x. [DOI] [PubMed] [Google Scholar]
  18. Rudy B. Diversity and ubiquity of K channels. Neuroscience. 1988 Jun;25(3):729–749. doi: 10.1016/0306-4522(88)90033-4. [DOI] [PubMed] [Google Scholar]
  19. Salkoff L., Butler A., Scavarda N., Wei A. Nucleotide sequence of the putative sodium channel gene from Drosophila: the four homologous domains. Nucleic Acids Res. 1987 Oct 26;15(20):8569–8572. doi: 10.1093/nar/15.20.8569. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Salkoff L., Butler A., Wei A., Scavarda N., Giffen K., Ifune C., Goodman R., Mandel G. Genomic organization and deduced amino acid sequence of a putative sodium channel gene in Drosophila. Science. 1987 Aug 14;237(4816):744–749. doi: 10.1126/science.2441469. [DOI] [PubMed] [Google Scholar]
  21. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Schwarz T. L., Tempel B. L., Papazian D. M., Jan Y. N., Jan L. Y. Multiple potassium-channel components are produced by alternative splicing at the Shaker locus in Drosophila. Nature. 1988 Jan 14;331(6152):137–142. doi: 10.1038/331137a0. [DOI] [PubMed] [Google Scholar]
  23. Siddiqi O., Benzer S. Neurophysiological defects in temperature-sensitive paralytic mutants of Drosophila melanogaster. Proc Natl Acad Sci U S A. 1976 Sep;73(9):3253–3257. doi: 10.1073/pnas.73.9.3253. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Suzuki D. T., Grigliatti T., Williamson R. Temperature-sensitive mutations in Drosophila melanogaster. VII. A mutation (para-ts) causing reversible adult paralysis. Proc Natl Acad Sci U S A. 1971 May;68(5):890–893. doi: 10.1073/pnas.68.5.890. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Suzuki N., Wu C. F. Altered sensitivity to sodium channel-specific neurotoxins in cultured neurons from temperature-sensitive paralytic mutants of Drosophila. J Neurogenet. 1984 Sep;1(3):225–238. doi: 10.3109/01677068409107088. [DOI] [PubMed] [Google Scholar]
  26. 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]
  27. Tanouye M. A., Kamb C. A., Iverson L. E., Salkoff L. Genetics and molecular biology of ionic channels in Drosophila. Annu Rev Neurosci. 1986;9:255–276. doi: 10.1146/annurev.ne.09.030186.001351. [DOI] [PubMed] [Google Scholar]
  28. Tempel B. L., Papazian D. M., Schwarz T. L., Jan Y. N., Jan L. Y. Sequence of a probable potassium channel component encoded at Shaker locus of Drosophila. Science. 1987 Aug 14;237(4816):770–775. doi: 10.1126/science.2441471. [DOI] [PubMed] [Google Scholar]
  29. Wu C. F., Ganetzky B. Genetic alteration of nerve membrane excitability in temperature-sensitive paralytic mutants of Drosophila melanogaster. Nature. 1980 Aug 21;286(5775):814–816. doi: 10.1038/286814a0. [DOI] [PubMed] [Google Scholar]
  30. Zwiebel L. J., Cohn V. H., Wright D. R., Moore G. P. Evolution of single-copy DNA and the ADH gene in seven drosophilids. J Mol Evol. 1982;19(1):62–71. doi: 10.1007/BF02100224. [DOI] [PubMed] [Google Scholar]

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