Advertisement

Purification and Reconstitution of the Ryanodine- and Caffeine-Sensitive Ca2+ Release Channel Complex from Muscle Sarcoplasmic Reticulum

  • Gerhard Meissner
  • F. Anthony Lai
  • Kristin Anderson
  • Le Xu
  • Qi-Yi Liu
  • Annegret Herrmann-Frank
  • Eric Rousseau
  • Rodney V. Jones
  • Hee-Bong Lee
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 304)

Abstract

Studies in our laboratory are directed towards obtaining a better understanding of the process of excitation-contraction coupling in muscle, primarily using purified membrane and protein preparations. In excitable tissues, release of Ca2+ ions can be triggered by a change in surface membrane potential (Ebashi, 1976), or it can occur via a chain of voltage-independent steps that involve agonist-induced formation of inositol 1,4,5-trisphosphate (IP3) and its subsequent binding and activation of an intracellular membrane receptor/channel complex, the IP3 receptor (Van Breemen and Saida, 1989). The voltage-dependent mechanism, commonly referred to as excitation -contraction (E-C) coupling, has been most extensively studied in skeletal and cardiac muscle. In striated muscle, rapid release of Ca2+ ions from the intracellular membrane compartment, sarcoplasmic reticulum (SR), is triggered by a surface membrane action potential that is thought to be communicated to the SR at specialized areas where the SR comes in close contact with tubular infoldings of the surface membrane (T-tubule). Spanning the gap between the two membrane systems are protein bridges (Peachey and Armstrong, 1983) which have been variously termed “feet” (Franzini-Armstrong, 1970), “bridges” (Somlyo, 1979), “pillars” (Eisenberg and Eisenberg, 1982), or “spanning” proteins (Caswell and Brandt, 1989), and are now believed to be identical with the ryanodine receptor or SR Ca2+ release channel complex (Fleischer and Inui, 1989; Lai and Meissner, 1989).

Keywords

Sarcoplasmic Reticulum Release Channel Ryanodine Receptor Channel Complex Planar Lipid Bilayer 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Anderson, K., Lai, F. A., Liu, Q. Y., Rousseau, E., Erickson, H. P., and Meissner, G., Structural and functional characterization of the purified cardiac ryanodine receptor-Ca2+ release channel complex, 1989, J. Biol. Chem., 264: 1329.PubMedGoogle Scholar
  2. Caswell, A. H. and Brandt, N. R., 1989, Triadic proteins of skeletal muscle, J. Bioenerg. Biomembr., 21: 149.PubMedCrossRefGoogle Scholar
  3. Ebashi, S., 1976, Excitation-contraction coupling, Ann. Rev. Physiol, 38: 293.CrossRefGoogle Scholar
  4. Eisenberg, B. R. and Eisenberg, R. S., 1982, The T-SR junction in contracting single muscle fibers, J. Gen. Physiol., 79: 1.PubMedCrossRefGoogle Scholar
  5. Endo, M., 1977, Calcium release from the sarcoplasmic reticulum, Physiol. Rev., 57: 71.PubMedGoogle Scholar
  6. Fabiato, A., 1983, Calcium-induced release of calcium from the cardiac sarcoplasmic reticulum, Am. J. Physiol., 245: C1.Google Scholar
  7. Fleischer, S. and Inui, M., 1989, Biochemistry and biophysics of excitation-contraction coupling, Ann. Rev. Biophys. Chem., 18: 333.CrossRefGoogle Scholar
  8. Franzini-Armstrong, C., 1980, Structure of sarcoplasmic reticulum, Fed. Proc, 39: 2403.PubMedGoogle Scholar
  9. Herrmann-Frank, A., Darling, E., and Meissner, G., 1990, Single channel measurements of the Ca2+-gated ryanodine-sensitive Ca2+ release channel of vascular smooth muscle, Biophys. J., 57: 156a.Google Scholar
  10. Imagawa, T., Smith, J. S., Coronado, R., and Campbell, K. P., 1987, Purified ryanodine receptor from skeletal muscle sarcoplasmic reticulum is the Ca2+-permeable pore of the calcium release channel, J. Biol. Chem., 262: 16636.PubMedGoogle Scholar
  11. Inui, M., Saito, A., and Fleischer, S., 1987, Isolation of the ryanodine receptor from cardiac sarcoplasmic reticulum and identity with the feet structures, J. Biol Chem., 262: 15637.PubMedGoogle Scholar
  12. Lai, F. A., Erickson, H. P., Rousseau, E., Liu, Q. Y., and Meissner, G., 1988, Purification and reconstitution of the calcium release channel from skeletal muscle, Nature, 331: 315.PubMedCrossRefGoogle Scholar
  13. Lai, F. A. and Meissner, G., 1989, The muscle ryanodine receptor and its intrinsic Ca2+ channel activity, J. Bioenerg. Biomembr., 21: 227.PubMedCrossRefGoogle Scholar
  14. Lai, F. A., Misra, M., Xu, L., Smith, H. A., and 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.PubMedGoogle Scholar
  15. Lai, F. A., Xu, L., and Meissner, G., 1990, Identification of a ryanodine receptor in rat and bovine brain, Biophys. J., 57: 529a.Google Scholar
  16. Liu, Q. Y., Lai, F. A., Rousseau, E., Jones, R. V., and Meissner, G., 1989, Multiple conductance states of the purified calcium release channel complex from skeletal sarcoplasmic reticulum, Biophys. J., 55: 415.PubMedCrossRefGoogle Scholar
  17. Meissner, G., 1975, Isolation and characterization of two types of sarcoplasmic reticulum vesicles, Biochim. Biophys. Acta, 389: 51.PubMedCrossRefGoogle Scholar
  18. Meissner, G., 1984, Adenine nucleotide stimulation of Ca2+-induced Ca2+ release in sarcoplasmic reticulum, J. Biol. Chem., 259: 1365.Google Scholar
  19. Meissner, G., 1986a, Evidence of a role for calmodulin in the regulation of calcium release from skeletal muscle sarcoplasmic reticulum, Biochemistry, 25: 244.PubMedCrossRefGoogle Scholar
  20. Meissner, G., 1986b, Ryanodine activation and inhibition of the Ca2+ release channel of sarcoplasmic reticulum, J. Biol. Chem., 261: 6300.PubMedGoogle Scholar
  21. Meissner, G., Darling, E., and Eveleth, J., 1986, Kinetics of rapid Ca2+ release by sarcoplasmic reticulum. Effects of Ca2+, Mg2+, and adenine nucleotides, Biochemistry, 25: 236.PubMedCrossRefGoogle Scholar
  22. Meissner, G. and Henderson, J. S., 1987, Rapid calcium release from cardiac sarcoplasmic reticulum vesicles is dependent on Ca2+ and is modulated by Mg2+, adenine nucleotide, and calmodulin, J. Biol. Chem., 262: 3065.PubMedGoogle Scholar
  23. Näbauer, M., Callewaert, G., Cleemann, L., and Morad, M., 1989, Regulation of calcium release is gated by calcium current, not gating charge, in cardiac myocytes, Science, 244: 800.PubMedCrossRefGoogle Scholar
  24. Otsu, K., Willard, H. F., Khanna, V. K., Zorzato, F., Green, N. M., and MacLennan, D. H., 1990, Molecular cloning of cDNA encoding the Ca2+ release channel (ryanodine receptor) of rabbit cardiac muscle sarcoplasmic reticulum, J. Biol. Chem., 265: 13472.PubMedGoogle Scholar
  25. Palade, P., Dettbarn, C., Brunder, D., Stein, P., and Hals, G., 1989, Pharmacology of calcium release from sarcoplasmic reticulum, J. Bioenerg. Biomembr., 21: 295.PubMedCrossRefGoogle Scholar
  26. Peachey, L. D. and Franzini-Armstrong, C., 1983, Structure and function of membrane systems of skeletal muscle cells, in: “Skeletal Muscle”, Handbook of Physiology, Sect. 10, L. D. Peachey, R. H. Adrian, S. R. Geiger eds., American Physiological Society, Bethesda, p. 23.Google Scholar
  27. Penner, R., Neher, E., Takeshima, H., Nishimura, S., and Numa, S., 1989, Functional expression of the calcium release channel from skeletal muscle ryanodine receptor cDNA, FEBS Lett., 259: 217.PubMedCrossRefGoogle Scholar
  28. Rios, E. and Pizarro, G., 1988, Voltage sensors and calcium channels of excitation-contraction coupling, News Physiol. Sci., 3: 223.Google Scholar
  29. Rousseau, E., Smith, J. S., Henderson, J. S., and Meissner, G., 1986, Single channel and 45Ca2+ flux measurements of the cardiac sarcoplasmic reticulum calcium channel, Biophys. J., 50: 1009.PubMedCrossRefGoogle Scholar
  30. Rousseau, E., LaDine, J., Liu, Q. Y., and Meissner, G., 1988, Activation of the Ca2+ release channel of skeletal muscle sarcoplasmic reticulum by caffeine and related compounds, Arch. Biochem. Biophys., 267: 75.PubMedCrossRefGoogle Scholar
  31. Rousseau, E. and Meissner, G., 1989, Single cardiac sarcoplasmic reticulum Ca2+-release channel: activation by caffeine, Am. J. Physiol, 256: H328.Google Scholar
  32. Saito, A., Inui, M., Wall, J. S., and Fleischer, S., 1989, Mass measurement of the feet structures/calcium release channel of sarcoplasmic reticulum by scanning transmission electron microscopy (STEM), Biophys. J., 55: 206a.Google Scholar
  33. Schneider, M. F., 1981 Membrane charge movement and depolarization-contraction coupling, Ann. Rev. Physiol., 43: 507.CrossRefGoogle Scholar
  34. Smith, J. S., Coronado, R., and Meissner, G., 1986a, Single-channel calcium and barium currents of large and small conductance from sarcoplasmic reticulum, Biophys. J., 50: 921.PubMedCrossRefGoogle Scholar
  35. Smith, J. S., Coronado, R., and Meissner, G., 1986b, Single measurements of the calcium release channel from skeletal muscle sarcoplasmic reticulum, activation by Ca2+ and ATP and modulation by Mg2+, J. Gen. Physiol, 88: 573.PubMedCrossRefGoogle Scholar
  36. Smith, J. S., Imagawa, T., Ma, J., Fill, M., Campbell, K. P., and Coronado, R., 1988, Purified ryanodine receptor from rabbit skeletal muscle is the calcium-release channel of sarcoplasmic reticulum, J. Gen. Physiol, 92: 1.PubMedCrossRefGoogle Scholar
  37. Smith, J. S., Rousseau, E., and Meissner, G., 1989, Calmodulin modulation of single sarcoplasmic reticulum Ca2+-release channels from cardiac and skeletal muscle, Circ. Res., 64: 352.PubMedGoogle Scholar
  38. Somlyo, A. V., 1979, Bridging structures spanning the junctional gap at the triad of skeletal muscle, J. Cell Biol, 80: 743PubMedCrossRefGoogle Scholar
  39. Stephenson, E. W., 1981, Activation of fast skeletal muscle: Contributions of studies on skinned fibers, Am. J. Physiol., 240: C1.Google Scholar
  40. Takeshima, H., Nishimura, S., Matsumoto, T., Ishida, H., Kangawa, K., Minamino, N., Matsuo, H., Ueda, M., Hanaoka, M., Hirose, T., and Numa, S., 1989, Primary structure and expression from complementary DNA of skeletal muscle ryanodine receptor, Nature, 339: 439.PubMedCrossRefGoogle Scholar
  41. Tanabe, T., Beam, K. G., Powell, J. A., and Numa, S., 1988, Restoration of excitation-contraction coupling and slow calcium current in dysgenic muscle by dihydropyridine receptor complementary DNA, Nature, 336: 134.PubMedCrossRefGoogle Scholar
  42. Tanabe, T., Mikami, A., Numa, S., and Beam, K. G., 1990, Cardiac-type excitation-contraction coupling in dysgenic skeletal muscle injected with cardiac dihydropyridine receptor cDNA, Nature, 344: 451.PubMedCrossRefGoogle Scholar
  43. Van Breemen, C., and Saida, K., 1989, Cellular mechanisms regulating [Ca2+] in smooth muscle, Ann. Rev. Physiol., 51: 315.CrossRefGoogle Scholar
  44. Wagenknecht, T., Grassucci, R., Frank, J., Saito, A., Inui, M., and Fleischer, S., 1989, Three-dimensional architecture of the calcium channel/foot structure of the sarcoplasmic reticulum, Nature, 338: 167.PubMedCrossRefGoogle Scholar
  45. Zaidi, N. F., Lagenaur, C. F., Hilker, R. J., Xiong, H., Abramson, J. J., and Salama, G., 1989, Disulfide linkage of biotin identifies a 106-kDa Ca2+ release channel in sarcoplasmic reticulum, J. Biol. Chem., 264: 21737.PubMedGoogle Scholar
  46. Zorzato, F., Fujii, J., Otsu, K., Phillips, M., Green, N. M., Lai, F. A., Meissner, G., and MacLennan, D. H., 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.PubMedGoogle Scholar

Copyright information

© Plenum Press, New York 1991

Authors and Affiliations

  • Gerhard Meissner
    • 1
  • F. Anthony Lai
    • 1
  • Kristin Anderson
    • 1
  • Le Xu
    • 1
  • Qi-Yi Liu
    • 1
  • Annegret Herrmann-Frank
    • 1
  • Eric Rousseau
    • 1
  • Rodney V. Jones
    • 1
  • Hee-Bong Lee
    • 1
  1. 1.Department of Biochemistry and BiophysicsUniversity of North CarolinaChapel HillUSA

Personalised recommendations