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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
. 1991 Feb 1;88(3):727–731. doi: 10.1073/pnas.88.3.727

Calcium channels from Cyprinus carpio skeletal muscle.

M Grabner 1, K Friedrich 1, H G Knaus 1, J Striessnig 1, F Scheffauer 1, R Staudinger 1, W J Koch 1, A Schwartz 1, H Glossmann 1
PMCID: PMC50886  PMID: 1846962

Abstract

The complete amino acid sequence of the L-type calcium channel alpha 1 subunit from the carp (Cyprinus carpio) white skeletal muscle was deduced by cDNA cloning and sequence analysis. The open reading frame encodes 1852 amino acids (Mr 210,060). A 155-amino acid COOH-terminal sequence (after the fourth internal repeat) is evolutionarily preserved (90% homology) and may represent an important functional domain of L-type calcium channels. The photolabeled, membrane-bound, and purified carp alpha 1 subunits have masses of 211 and 190 kDa. The purified channel could not be phosphorylated by cAMP-dependent protein kinase. Two glycoproteins (alpha 2 subunits) are associated with the alpha 1 subunit and change their apparent masses from 235 and 220 kDa to 159 kDa upon reduction of disulfide bonds. Nucleic acid hybridization with alpha 2 cDNA revealed an 8.0-kilobase transcript in carp skeletal muscle. Evidence for a copurification of subunits similar in size to mammalian beta or gamma subunits was not obtained.

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

  1. Ahlijanian M. K., Westenbroek R. E., Catterall W. A. Subunit structure and localization of dihydropyridine-sensitive calcium channels in mammalian brain, spinal cord, and retina. Neuron. 1990 Jun;4(6):819–832. doi: 10.1016/0896-6273(90)90135-3. [DOI] [PubMed] [Google Scholar]
  2. Akster H. A. Morphometry of muscle fibre types in the carp (Cyprinus carpio L.). Relationships between structural and contractile characteristics. Cell Tissue Res. 1985;241(1):193–201. doi: 10.1007/BF00214641. [DOI] [PubMed] [Google Scholar]
  3. Aviv H., Leder P. Purification of biologically active globin messenger RNA by chromatography on oligothymidylic acid-cellulose. Proc Natl Acad Sci U S A. 1972 Jun;69(6):1408–1412. doi: 10.1073/pnas.69.6.1408. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bosse E., Regulla S., Biel M., Ruth P., Meyer H. E., Flockerzi V., Hofmann F. The cDNA and deduced amino acid sequence of the gamma subunit of the L-type calcium channel from rabbit skeletal muscle. FEBS Lett. 1990 Jul 2;267(1):153–156. doi: 10.1016/0014-5793(90)80312-7. [DOI] [PubMed] [Google Scholar]
  5. Campbell K. P., Leung A. T., Sharp A. H. The biochemistry and molecular biology of the dihydropyridine-sensitive calcium channel. Trends Neurosci. 1988 Oct;11(10):425–430. doi: 10.1016/0166-2236(88)90193-2. [DOI] [PubMed] [Google Scholar]
  6. Chang F. C., Hosey M. M. Dihydropyridine and phenylalkylamine receptors associated with cardiac and skeletal muscle calcium channels are structurally different. J Biol Chem. 1988 Dec 15;263(35):18929–18937. [PubMed] [Google Scholar]
  7. 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]
  8. Chou P. Y., Fasman G. D. Empirical predictions of protein conformation. Annu Rev Biochem. 1978;47:251–276. doi: 10.1146/annurev.bi.47.070178.001343. [DOI] [PubMed] [Google Scholar]
  9. De Jongh K. S., Merrick D. K., Catterall W. A. Subunits of purified calcium channels: a 212-kDa form of alpha 1 and partial amino acid sequence of a phosphorylation site of an independent beta subunit. Proc Natl Acad Sci U S A. 1989 Nov;86(21):8585–8589. doi: 10.1073/pnas.86.21.8585. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Ellis S. B., Williams M. E., Ways N. R., Brenner R., Sharp A. H., Leung A. T., Campbell K. P., McKenna E., Koch W. J., Hui A. Sequence and expression of mRNAs encoding the alpha 1 and alpha 2 subunits of a DHP-sensitive calcium channel. Science. 1988 Sep 23;241(4873):1661–1664. doi: 10.1126/science.2458626. [DOI] [PubMed] [Google Scholar]
  11. Feinberg A. P., Vogelstein B. "A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity". Addendum. Anal Biochem. 1984 Feb;137(1):266–267. doi: 10.1016/0003-2697(84)90381-6. [DOI] [PubMed] [Google Scholar]
  12. Ferry D. R., Glossmann H. Identification of putative calcium channels in skeletal muscle microsomes. FEBS Lett. 1982 Nov 8;148(2):331–337. doi: 10.1016/0014-5793(82)80835-1. [DOI] [PubMed] [Google Scholar]
  13. Flockerzi V., Oeken H. J., Hofmann F., Pelzer D., Cavalié A., Trautwein W. Purified dihydropyridine-binding site from skeletal muscle t-tubules is a functional calcium channel. Nature. 1986 Sep 4;323(6083):66–68. doi: 10.1038/323066a0. [DOI] [PubMed] [Google Scholar]
  14. Fosset M., Jaimovich E., Delpont E., Lazdunski M. [3H]nitrendipine receptors in skeletal muscle. J Biol Chem. 1983 May 25;258(10):6086–6092. [PubMed] [Google Scholar]
  15. Glossmann H., Ferry D. R., Boschek C. B. Purification of the putative calcium channel from skeletal muscle with the aid of [3H]-nimodipine binding. Naunyn Schmiedebergs Arch Pharmacol. 1983 Jun;323(1):1–11. doi: 10.1007/BF00498821. [DOI] [PubMed] [Google Scholar]
  16. Hawkes R. Identification of concanavalin A-binding proteins after sodium dodecyl sulfate--gel electrophoresis and protein blotting. Anal Biochem. 1982 Jun;123(1):143–146. doi: 10.1016/0003-2697(82)90634-0. [DOI] [PubMed] [Google Scholar]
  17. Hosey M. M., Lazdunski M. Calcium channels: molecular pharmacology, structure and regulation. J Membr Biol. 1988 Sep;104(2):81–105. doi: 10.1007/BF01870922. [DOI] [PubMed] [Google Scholar]
  18. Hubbard S. C., Ivatt R. J. Synthesis and processing of asparagine-linked oligosaccharides. Annu Rev Biochem. 1981;50:555–583. doi: 10.1146/annurev.bi.50.070181.003011. [DOI] [PubMed] [Google Scholar]
  19. Hymel L., Striessnig J., Glossmann H., Schindler H. Purified skeletal muscle 1,4-dihydropyridine receptor forms phosphorylation-dependent oligomeric calcium channels in planar bilayers. Proc Natl Acad Sci U S A. 1988 Jun;85(12):4290–4294. doi: 10.1073/pnas.85.12.4290. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Jay S. D., Ellis S. B., McCue A. F., Williams M. E., Vedvick T. S., Harpold M. M., Campbell K. P. Primary structure of the gamma subunit of the DHP-sensitive calcium channel from skeletal muscle. Science. 1990 Apr 27;248(4954):490–492. doi: 10.1126/science.2158672. [DOI] [PubMed] [Google Scholar]
  21. Kishimoto A., Nishiyama K., Nakanishi H., Uratsuji Y., Nomura H., Takeyama Y., Nishizuka Y. Studies on the phosphorylation of myelin basic protein by protein kinase C and adenosine 3':5'-monophosphate-dependent protein kinase. J Biol Chem. 1985 Oct 15;260(23):12492–12499. [PubMed] [Google Scholar]
  22. Knaus H. G., Scheffauer F., Romanin C., Schindler H. G., Glossmann H. Heparin binds with high affinity to voltage-dependent L-type Ca2+ channels. Evidence for an agonistic action. J Biol Chem. 1990 Jul 5;265(19):11156–11166. [PubMed] [Google Scholar]
  23. Knudson C. M., Chaudhari N., Sharp A. H., Powell J. A., Beam K. G., Campbell K. P. Specific absence of the alpha 1 subunit of the dihydropyridine receptor in mice with muscular dysgenesis. J Biol Chem. 1989 Jan 25;264(3):1345–1348. [PubMed] [Google Scholar]
  24. Kozak M. The scanning model for translation: an update. J Cell Biol. 1989 Feb;108(2):229–241. doi: 10.1083/jcb.108.2.229. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Krebs E. G., Beavo J. A. Phosphorylation-dephosphorylation of enzymes. Annu Rev Biochem. 1979;48:923–959. doi: 10.1146/annurev.bi.48.070179.004423. [DOI] [PubMed] [Google Scholar]
  26. Kyte J., Doolittle R. F. A simple method for displaying the hydropathic character of a protein. J Mol Biol. 1982 May 5;157(1):105–132. doi: 10.1016/0022-2836(82)90515-0. [DOI] [PubMed] [Google Scholar]
  27. Lehrach H., Diamond D., Wozney J. M., Boedtker H. RNA molecular weight determinations by gel electrophoresis under denaturing conditions, a critical reexamination. Biochemistry. 1977 Oct 18;16(21):4743–4751. doi: 10.1021/bi00640a033. [DOI] [PubMed] [Google Scholar]
  28. Messing J., Crea R., Seeburg P. H. A system for shotgun DNA sequencing. Nucleic Acids Res. 1981 Jan 24;9(2):309–321. doi: 10.1093/nar/9.2.309. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. 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]
  30. Neumcke B. Diversity of sodium channels in adult and cultured cells, in oocytes and in lipid bilayers. Rev Physiol Biochem Pharmacol. 1990;115:1–49. [PubMed] [Google Scholar]
  31. Nunoki K., Florio V., Catterall W. A. Activation of purified calcium channels by stoichiometric protein phosphorylation. Proc Natl Acad Sci U S A. 1989 Sep;86(17):6816–6820. doi: 10.1073/pnas.86.17.6816. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Perez-Reyes E., Kim H. S., Lacerda A. E., Horne W., Wei X. Y., Rampe D., Campbell K. P., Brown A. M., Birnbaumer L. Induction of calcium currents by the expression of the alpha 1-subunit of the dihydropyridine receptor from skeletal muscle. Nature. 1989 Jul 20;340(6230):233–236. doi: 10.1038/340233a0. [DOI] [PubMed] [Google Scholar]
  33. Powers D. A. Fish as model systems. Science. 1989 Oct 20;246(4928):352–358. doi: 10.1126/science.2678474. [DOI] [PubMed] [Google Scholar]
  34. Proudfoot N. J., Brownlee G. G. 3' non-coding region sequences in eukaryotic messenger RNA. Nature. 1976 Sep 16;263(5574):211–214. doi: 10.1038/263211a0. [DOI] [PubMed] [Google Scholar]
  35. Reichlin M. Use of glutaraldehyde as a coupling agent for proteins and peptides. Methods Enzymol. 1980;70(A):159–165. doi: 10.1016/s0076-6879(80)70047-2. [DOI] [PubMed] [Google Scholar]
  36. Ruth P., Röhrkasten A., Biel M., Bosse E., Regulla S., Meyer H. E., Flockerzi V., Hofmann F. Primary structure of the beta subunit of the DHP-sensitive calcium channel from skeletal muscle. Science. 1989 Sep 8;245(4922):1115–1118. doi: 10.1126/science.2549640. [DOI] [PubMed] [Google Scholar]
  37. Röhrkasten A., Meyer H. E., Nastainczyk W., Sieber M., Hofmann F. cAMP-dependent protein kinase rapidly phosphorylates serine- 687 of the skeletal muscle receptor for calcium channel blockers. J Biol Chem. 1988 Oct 25;263(30):15325–15329. [PubMed] [Google Scholar]
  38. 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]
  39. Striessnig J., Goll A., Moosburger K., Glossmann H. Purified calcium channels have three allosterically coupled drug receptors. FEBS Lett. 1986 Mar 3;197(1-2):204–210. doi: 10.1016/0014-5793(86)80327-1. [DOI] [PubMed] [Google Scholar]
  40. Striessnig J., Scheffauer F., Mitterdorfer J., Schirmer M., Glossmann H. Identification of the benzothiazepine-binding polypeptide of skeletal muscle calcium channels with (+)-cis-azidodiltiazem and anti-ligand antibodies. J Biol Chem. 1990 Jan 5;265(1):363–370. [PubMed] [Google Scholar]
  41. Takahashi M., Seagar M. J., Jones J. F., Reber B. F., Catterall W. A. Subunit structure of dihydropyridine-sensitive calcium channels from skeletal muscle. Proc Natl Acad Sci U S A. 1987 Aug;84(15):5478–5482. doi: 10.1073/pnas.84.15.5478. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Tanabe T., Beam K. G., Adams B. A., Niidome T., Numa S. Regions of the skeletal muscle dihydropyridine receptor critical for excitation-contraction coupling. Nature. 1990 Aug 9;346(6284):567–569. doi: 10.1038/346567a0. [DOI] [PubMed] [Google Scholar]
  43. Tanabe T., Beam K. G., Powell J. A., Numa S. Restoration of excitation-contraction coupling and slow calcium current in dysgenic muscle by dihydropyridine receptor complementary DNA. Nature. 1988 Nov 10;336(6195):134–139. doi: 10.1038/336134a0. [DOI] [PubMed] [Google Scholar]
  44. Tanabe T., Mikami A., Numa S., Beam K. G. Cardiac-type excitation-contraction coupling in dysgenic skeletal muscle injected with cardiac dihydropyridine receptor cDNA. Nature. 1990 Mar 29;344(6265):451–453. doi: 10.1038/344451a0. [DOI] [PubMed] [Google Scholar]
  45. 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]
  46. Vaghy P. L., Striessnig J., Miwa K., Knaus H. G., Itagaki K., McKenna E., Glossmann H., Schwartz A. Identification of a novel 1,4-dihydropyridine- and phenylalkylamine-binding polypeptide in calcium channel preparations. J Biol Chem. 1987 Oct 15;262(29):14337–14342. [PubMed] [Google Scholar]

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