Evidence for an Intracellular Ryanodine- and Caffeine-Sensitive Calcium Ion-Conducting Channel in Excitable Tissues

  • G. Meissner
  • A. Herrmann-Frank
  • F. A. Lai
  • L. Xu
Conference paper
Part of the NATO ASI Series book series (volume 48)

Abstract

In skeletal and cardiac muscle, an action potential triggers the release of calcium ions from the intracellular membrane compartment, sarcoplasmic reticulum (SR), via a ligand-gated, high-conductance “Ca2+ release” channel. This channel has been identified as the receptor for the plant alkaloid ryanodine and also shown to be morphologically identical with the large protein structures (“feet”) that span the gap between junctional SR and the muscle surface membrane and T-tubule. The detergent-solubilized Ca2+ release channel has been purified from skeletal and cardiac muscle as a tetrameric 30 S protein complex and reconstituted into planar lipid bilayers. The skeletal and cardiac channels conduct monovalent cations in addition to Ca2+, are activated by Ca2+, and modulated by ATP, Mg2+, calmodulin, and the two Ca2+ releasing drugs caffeine and ryanodine. Ruthenium red, a polyvalent cation, inhibits the channels at micromolar concentrations. Recently, our laboratory has also obtained evidence for the presence of a 30 S mono- and divalent cation-conducting channel complex in canine and porcine aorta and rat and bovine brain. A similar high molecular weight Ca2+ release channel complex may be present therefore, in most, if not all, mammalian excitable tissues.

Keywords

Sucrose Cage Sedimentation Polypeptide Caffeine 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Anderson K, Lai FA, Liu QY, Rousseau E, Erickson HP, Meissner G (1989) Structural and functional characterization of the purified cardiac ryanodine receptor–Ca’“ release channel complex. J Biol Chem 264: 1329–1335.PubMedGoogle Scholar
  2. Donaldson SK, Goldberg ND, Walseth TF, Huetteman DA (1988) Voltage dependence of inositol 1,4,5-trisphosphate-induced Ca2+ release in peeled skeletal muscle fibers. Proc Natl Acad Sci, USA 85: 5749–5753.Google Scholar
  3. Endo M (1977) Calcium release from the sarcoplasmic reticulum. Physiol Rev 57: 71–108.PubMedGoogle Scholar
  4. Ehrlich BE, Watras J (1988) Inositol 1,4,5-trisphosphate activates a channel from smooth muscle sarcoplasmic reticulum. Nature 336: 583–586.PubMedCrossRefGoogle Scholar
  5. Fabiato A (1983) Calcium-induced release of calcium from the cardiac sarcoplasmic reticulum. Am J Physiol 245: C1 - C14.PubMedGoogle Scholar
  6. Furuichi T, Yoshikawa S, Miyawaki A, Wada K, Maeda N, Mikoshiba K (1989) Primary structure and functional expression of the inositol 1,4,5-trisphosphate-binding protein P400. Nature 342: 32–38.PubMedCrossRefGoogle Scholar
  7. Herrmann-Frank A, Darling E Meissner G (1990) Single channel measurements of the Ca’“-gated ryanodine-sensitive Ca2+ release channel of vascular smooth muscle. Biophys J 57: 156a.Google Scholar
  8. Lai FA, Erickson HP, Rousseau E, Liu QY, Meissner G (1988) Purification and reconstitution of the calcium release channel from skeletal muscle. Nature 331: 315–319.PubMedCrossRefGoogle Scholar
  9. Lai FA, Meissner (1989) The muscle ryanodine receptor and its intrinsic Ca’’ channel activity. J Bioenerg Biomembr 21: 227–246.Google Scholar
  10. Lai FA, Misra M, Xu L, Smith HA, Meissner G (1989) The ryanodine receptor-Ca2+ release channel complex of skeletal muscle sarcoplasmic reticulum. Evidence for a cooperatively coupled, negatively charged homotetramer. J Biol Chem 264: 16776–16785.Google Scholar
  11. Lai FA, Xu L, Meissner G (1990) Identification of a ryanodine receptor in rat and bovine brain. Biophys J 57: 529a.Google Scholar
  12. Liu QY, Lai FA, Rousseau E, Jones RV, Meissner G (1989) Multiple conductance states of the purified calcium release channel complex from skeletal sarcoplasmic reticulum. Biophys J 55: 415–424.PubMedCrossRefGoogle Scholar
  13. Meissner G (1986) Evidence of a role for calmodulin in the regulation of calcium release from skeletal muscle sarcoplasmic reticulum. Biochemistry 25: 244–251.PubMedCrossRefGoogle Scholar
  14. Meissner G, Darling E, Eveleth J (1986) Kinetics of r.p+id C“ release by sarcoplasmic reticulum. Effects of Ca’’ Mg and adenine nucleotides. Biochemistry 25: 236–244.Google Scholar
  15. Meissner G, Henderson JS (1987) Rapid calcium release from cardiac muscle arcoplasmic reticulum ve icles is dependent on Ca’’ and is modulated by Mg’+, adenine nucleotide and calmodulin. J Biol Chem 262: 3065–3073.PubMedGoogle Scholar
  16. Peachey LD, Franzini-Armstrong C (1983) Structure and function of membrane systems of skeletal muscle cells. In Skeletal Muscle ( Peachey LD, Adrian RH, Geiger SR, eds) Handbook of Physiology. American Physiological Society, Bethesda, MD pp 23–71.Google Scholar
  17. Rios E, Pizarro G (1988) Voltage sensors and calcium channels of excitation-contraction coupling. NIPS 3: 223–227.Google Scholar
  18. Rousseau E, Smith, JS Henderson JS, Meissner G (1986) Single channel and Ca2 flux measurements of the cardiac sarcoplasmic reticulum calcium channel. Biophys J 50: 1009–1014.PubMedCrossRefGoogle Scholar
  19. Rousseau E, LaDine J, Liu QY, Meissner G (1988) Activation of the Ca2+ release channel of skeletal muscle sarcoplasmic reticulum by caffeine and related compounds. Arch Biochem Biophys 267: 75–86.PubMedCrossRefGoogle Scholar
  20. Rousseau E, Meissner G (1989) Single cardiac sarcoplasmic reticulum Ca + release channel: activation by caffeine. Am J Physiol 256: H328 - H333.PubMedGoogle Scholar
  21. Smith JS, Coronado R, Meissner G (1986) Single channel measurements of the calcium release channel from skeletal muscle sarcoplasmic Keticulum. Activation by Ca2+ and ATP and modulation by Mg +. J Gen Physiol 88: 573–588.PubMedCrossRefGoogle Scholar
  22. Smith JS, Rousseau E, Meissner G (1989) Calmodulin modulation of single sarcoplasmic reticulum Ca2+-release channels from cardiac and skeletal muscle. Circ Research 64: 352–359.Google Scholar
  23. Takeshima H, Nishimura S, Matsumoto T, Ishida H, Kangawa K, Minamino N, Matsuo H, Ueda M, Hanaoka M, Hirose T, Numa S (1989) Primary structure and expression from complementary DNA of skeletal muscle ryanodine receptor. Nature 339: 439–445.PubMedCrossRefGoogle Scholar
  24. Thayer SA, Hirning LD, Miller RJ (1988) The role of caffeine-sensitive calcium stores in the regulation of the intracellular free calcium concentration in rat sympathetic neurons in vitro. Mol. Pharmacol. 34: 664–673.Google Scholar
  25. Van Breemen C, Saida K (1989) Cellular mechanisms regulating [Ca +]i in smooth muscle. Annu Rev Physiol 51: 315–329.PubMedCrossRefGoogle Scholar
  26. Walker JW, Somlyo AV, Goldman YE, Somlyo AP, Trentham DR (1987) Kinetics of smooth and skeletal muscle activation by laser pulse photolysis of caged inositol 1,4,5-trisphosphate. Nature 327: 249–252.PubMedCrossRefGoogle Scholar
  27. Zorzato F, Fujii J, Otsu K, Phillips M, Green NM, Lai FA, Meissner G, MacLennan DH (1990) Molecular cloning of cDNA encoding human and rabbit forms of the Ca2+ release channel (ryanodine receptor) of skeletal muscle sarcoplasmic reticulum. J Biol Chem 265: 2244–2256.PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1990

Authors and Affiliations

  • G. Meissner
    • 1
    • 2
  • A. Herrmann-Frank
    • 1
    • 2
  • F. A. Lai
    • 1
    • 2
  • L. Xu
    • 1
    • 2
  1. 1.Department of BiochemistryUniversity of North CarolinaChapel HillUSA
  2. 2.Department of PhysiologyUniversity of North CarolinaChapel HillUSA

Personalised recommendations