Advertisement

Ryanodine-Sensitive Calcium Release Channels

  • Daniela Rossi
  • Virginia Barone
  • Ilenia Simeoni
  • Vincenzo Sorrentino

Abstract

Variations in the intracellular calcium concentration [Ca2+] i play an important role in a variety of intracellular processes, including secretion, contraction and cell proliferation (Berridge, 1993). Increases in [Ca2+] i can be exerted by an influx of ions from the extracellular medium and/or by a release of Ca2+ from intracellular stores. Two classes of intracellular channels that play a key role in regulating Ca2+ release from intracellular stores have been so far identified: the inositol 1,4,5-trisphosphate (InsP3) receptors and the Ryanodine Receptors (RyRs) (Berridge, 1993; Sorrentino and Volpe, 1993). InsP3 receptors are described in Parys et al. (this book). This chapter will focus on the second class of intracellular Ca2+ release channels: the Ryanodine Receptors.

Keywords

Skeletal Muscle Sarcoplasmic Reticulum Release Channel Ryanodine Receptor Granular Cell Layer 
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. Airey, J.A., Beck, C.F., Murakami, K., Tanksley, S.J., Deerinck, T.J., Ellisman, M.H. and Sutko, J.L., 1990, Identification and localization of two triad junctional foot protein isoforms in mature avian fast twitch skeletal muscle, J. Biol. Chem. 265, 14187–14194.PubMedGoogle Scholar
  2. Balschun, D., Wolfer, D.R, Bertocchini, F., Barone, V., Conti, A., Zuschratter, W., Missiaen, L., Lipp, H.R, Frey, U. and Sorrentino, V., 1999, Deletion of the ryanodine receptor type 3 (RyR3) impairs forms of synaptic plasticity and spatial learning, EMBO J. 18, 5264–5273.PubMedCrossRefGoogle Scholar
  3. Barone, V., Bertocchini, R, Bottinelli, R., Protasi, E, Allen, P.D., Franzini Armstrong, C, Reggiani, C. and Sorrentino, V., 1998, Contractile impairment and structural alterations of skeletal muscles from knockout mice lacking type 1 and type 3 ryanodine receptors, FEBS Lett. 422, 160–164.PubMedCrossRefGoogle Scholar
  4. Berridge, J.B., 1993, Inositol trisphosphte and calcium signalling. Nature, 361, 315–325.PubMedCrossRefGoogle Scholar
  5. Bertocchini, F., Ovitt, C.E., Conti, A., Barone, V., Schöler, H.R., Bottinelli, R., Reggiani, C. and Sorrentino, V., 1997, Requirement for the ryanodine receptor type 3 for efficient contraction in neonatal skeletal muscle, EMBO J. 16, 6956–6963.PubMedCrossRefGoogle Scholar
  6. Buck, E.D., Nguyen, H., Pessah, I. and Allen, P.D., 1997, Dyspedic mouse skeletal muscle expresses major elements of the triadic junction but lacks detectable ryanodine receptor protein and function, J. Cell Biol. 272, 7360–7367.Google Scholar
  7. Chen, S.R.W., Zhang, L. and MacLennan, D.H., 1992, Characterization of a Ca2+ binding and regulatory site in the Ca2+ release channel (ryanodine receptor) of rabbit skeletal muscle sarcoplasmic reticulum, J. Biol. Chem. 267, 23318–23326.PubMedGoogle Scholar
  8. Chen, S.R.W., Ebisawa, K., Li, X. and Zhang, L., 1998, Molecular identification of the ryanodine receptor Ca2+ sensor, J. Biol. Chem. 273, 14675–14678.PubMedCrossRefGoogle Scholar
  9. Conklin, M.W., Barone, V., Sorrentino, V. and Coronado, R, 1999, Contribution of ryanodine receptor type 3 to Ca2+ sparks in embryonic mouse skeletal muscle, Biophys. J. 77(3), 1394–1403.PubMedCrossRefGoogle Scholar
  10. Conti, A., Gorza, L. and Sorrentino, V., 1996, Differential distribution of ryanodine receptor type 3 (RyR3) gene product in mammalian skeletal muscles, Biochem. J. 316, 19–23.PubMedGoogle Scholar
  11. Currie, K.R, Swann, K., Galione, A. and Scott, R.H.,1992, Activation of Ca (2+)-dependent currents in cultured rat dorsal root ganglion neurones by a sperm factor and cyclic ADP-ribose, Mol Biol Cell 3, 1415–1425.PubMedGoogle Scholar
  12. Dargie, P.J., Agre, M.C. and Lee, H.C.,1990, Comparison of Ca2+ mobilizing activities of cyclic ADP-ribose and inositol trisphosphate, Cell Regul 1, 279–290.PubMedGoogle Scholar
  13. Du, G.G. and MacLennan, D.H., 1999, Ca2+ inactivation sites are located in the COOH-terminal quarter of recombinant rabbit skeletal muscle Ca2+ release channels (ryanodine receptors), J. Biol Chem. 274, 26120–26126.PubMedCrossRefGoogle Scholar
  14. Fabiato, A., 1983, Calcium-induced release of calcium from the cardiac sarcoplasmic reticulum, Am. J. Physiol 245, C1–C14.PubMedGoogle Scholar
  15. Fabiato, A., 1985, Simulated calcium current can both cause calcium loading in and trigger calcium release from the sarcoplasmic reticulum of a skinned canine cardiac Purkinje cell, J. Gen. Physiol. 85, 291–320.PubMedCrossRefGoogle Scholar
  16. Flucher, B.E., Conti, A., Takeshima, H. and Sorrentino, V., 1999, Type 3 and Type 1 ryanodine receptors are localized in triads of the same mammalian skeletal muscle fibers, J. Cell Biol. 146, 621–629.PubMedCrossRefGoogle Scholar
  17. Franzini-Armstrong, C. and Protasi, F., 1997, Ryanodine receptors of striated muscles: A complex channel capable of multiple interactions, Physiol. Rev. 11, 699–729.Google Scholar
  18. Fruen, B.R., Mickelson, J.R., Shomer, N.H., Velez, P. and Louis, C.F., 1994, Cyclic ADP-ribose does not affect cardiac or skeletal muscle ryanodine receptors, FEBS Lett. 352, 123–126.PubMedCrossRefGoogle Scholar
  19. Furuichi, T, Furutama, D., Hakamata, Y., Nakai, J., Takeshima, H. and Mikoshiba, K., 1994, Multiple types of ryanodine receptor/Ca2+ release channels are differentially expressed in rabbit brain, J. Neuroscl 14, 4794–4805.Google Scholar
  20. Futatsugi, A., Kuwajima, G. and Mikoshiba, K., 1995, Tissue-specific and development-ally regulated alternative splicing in mouse skeletal muscle ryanodine receptor mRNA, Biochem J. 305, 373–378.PubMedGoogle Scholar
  21. Galione, A., Lee, H.C. and Busa, W.,1991, Ca2+-induced Ca2+ release in sea urchin egg homogenates: Modulation by cyclic ADP-ribose, Science 253, 1143–1146.PubMedCrossRefGoogle Scholar
  22. Giannini, G., Clementi, E., Ceci, R., Marziali, G. and Sorrentino, V.,1992, Expression of a ryanodine receptor-Ca2+ channel that is regulated by TGF-β, Science 257, 91–94.PubMedCrossRefGoogle Scholar
  23. Giannini, G., Conti, A., Mammarella, S., Scrobogna, M. and Sorrentino, V., 1995, The ryanodine receptor/Calcium release channel genes are widely and differentially expressed in murine brain and peripheral tissues, J. Cell Biol 128, 893–904.PubMedCrossRefGoogle Scholar
  24. Hakamata, Y., Nakai, J., Takeshima, H. and Imoto, K., 1992, Primary structure and distribution of a novel ryanodine receptor/calcium release channel from rabbit brain, FEBS Lett. 312, 229–235.PubMedCrossRefGoogle Scholar
  25. Ikemoto, T., Iino, M. and Endo, M., 1995, Enhancing effect of calmodulin on Ca2+-induced-Ca2+ release in the sarcoplasimc reticulum of skeletal muscle fibers, J. Physiol 487, 573–582.PubMedGoogle Scholar
  26. Ikemoto, T, Komazaki, S., Takeshima, H., Nishi, M., Noda, T, Iino, M. and Endo, M., 1997, Functional and morphological features of skeletal muscle from mutant mice lacking both type 1 and type 3 ryanodine receptors, J. Physiol. 501, 305–312.PubMedCrossRefGoogle Scholar
  27. Ikemoto, T, Takeshima, H., Iino, M. and Endo, M., 1998, Effect of calmodulin on Ca2+ induced Ca2+ release of skeletal muscle from mutant mice expressing either ryanodine receptor type 1 or type 3, Pflügers Arch. — Eur. J. Physiol 437, 43–48.CrossRefGoogle Scholar
  28. Koshiyama, H., Lee, H.C. and Tashjian, A.H., 1991, Novel mechanism of intracellular calcium release in pituitary cells, J. Biol. Chem. 266, 16985–16988.PubMedGoogle Scholar
  29. Lai, F.A., Liu, Q.-L., Xu, L., El-Hashem, A., Kramarcy, N.R., Sealock, R. and Meissner, G., 1992, Amphibian ryanodine receptor isoforms are related to those of mammalian skeletal or cardiac muscle, Am. J. Physiol. 263, C365–C372.PubMedGoogle Scholar
  30. Ledbetter, M.W., Preiner, J.K., Louis, C.F. and Mickelson, J.R., 1994, Tissue distribution of ryanodine receptor isoforms and alleles determined by reverse transcription polymerase chain reaction, J. Biol. Chem. 269, 31544–31551.PubMedGoogle Scholar
  31. Lee, H.C., 1997, Mechanisms of calcium signaling by cyclic ADP-ribose and NAADP, Physiol. Rev. 77, 1133–1164.PubMedGoogle Scholar
  32. Lee, H.C., Aarhus, R., Graeff, R., Gurnack, M.E. and Walseth, T.F.,1994, Cyclic ADP ribose activation of the ryanodine receptor is mediated by calmodulin, Nature 370, 307–309.PubMedCrossRefGoogle Scholar
  33. Ma, J. and Zhao, J.Y., 1994, Highly cooperative and hysteretic response of the skeletal muscle ryanodine receptor to changes in proton concentrations, Biophys. J. 67, 626–633.PubMedCrossRefGoogle Scholar
  34. Marziali, G., Rossi, D., Giannini, G., Charlesworth, A. and Sorrentino, V., 1996, cDNA cloning reveals a tissue specific expression of alternatively spliced transcripts of the ryanodine receptor type 3 (RyR3) calcium release channel, FEBS Lett. 394, 76–82.PubMedCrossRefGoogle Scholar
  35. McPherson, P.S. and Campbell, K.P., 1993, The ryanodine receptor/Ca2+ release channel, J. Biol Chem. 268, 13765–13768.PubMedGoogle Scholar
  36. Meszaros, L.G., Bak, J. and Chu, A.,1993, Cyclic ADP-ribose as an endogenous regulator of the non-skeletal type ryanodine receptor Ca2+ channel, Nature 364, 76–79.PubMedCrossRefGoogle Scholar
  37. Nabauer, 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, 800–803.PubMedCrossRefGoogle Scholar
  38. Nakai, J., Imagawa, T., Hakamata, Y., Shigekawa, M., Takeshima, H. and Numa, S., 1990, Primary structure and functional expression from cDNA of the cardiac ryanodine receptor/calcium release channel, FEBS Lett. 271, 169–177.PubMedCrossRefGoogle Scholar
  39. Nakai, J., Dirksen, R.T., Nguyen, H.T., Pessah, I.N., Beam, K.G. and Allen, P.D.,1996, Enhanced dihydropyridine receptor channel activity in the presence of ryanodine receptor, Nature 380, 72–75.PubMedCrossRefGoogle Scholar
  40. Olivares, E.B., Tanksley, S.J., Airey, J.A., Beck, C.F., Ouyang, Y., Deerinck, T.J., Ellisman, M.H. and Sutko, J.L., 1991, Multiple foot protein isoforms in amphibian, avian and piscine skeletal muscles, Biophys. J. 59, 1153–1163PubMedCrossRefGoogle Scholar
  41. 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, 13472–13483.PubMedGoogle Scholar
  42. Ottini, L., Marziali, G., Conti, A., Charlesworth, A. and Sorrentino, V., 1996, α and β isoforms of ryanodine receptors from chicken skeletal muscle are the homologues of mammalian RyR1 and RyR3, Biochem. J. 315, 207–215.PubMedGoogle Scholar
  43. Oyamada, H., Murayama, T., Takagi, T., Iino, M., Iwabe, N., Miyata, T., Ogawa, Y. and Endo, M., 1994, Primary structures and distribution of ryanodine-binding protein isoforms of the bullfrog skeletal muscle, J. Biol. Chem. 269, 17206–17214.PubMedGoogle Scholar
  44. Percival, A., Airey, J.A., Grinsell, M.M., Kenyon, J.L., Williams, A.J. and Sutko, J.L., 1994, Chicken skeletal muscle ryanodine receptor isoforms: Ion channel properties, Biophys. J. 67, 1834–1850.PubMedCrossRefGoogle Scholar
  45. Powell, J.A., Petherbridge, L. and Flucher, B.E., 1996, Formation of triads without the dihydropyridine receptor alpha subunits in cell lines from dysgenic skeletal muscle, J. Cell Biol 134, 375–387.PubMedCrossRefGoogle Scholar
  46. Protasi, F., Franzini-Armstrong, C. and Allen, P.D., 1998, Role of ryanodine receptors in assembly of calcium release units in skeletal muscle, J. Cell Biol. 140, 831–842.PubMedCrossRefGoogle Scholar
  47. Radermacher, M., Rao, V., Grassucci, R., Frank, J., Timerman, A.R, Fleischer, S. and Wagenknecht, T., 1994, Cryo-electron microscopy and three-dimensional reconstruction of the calcium release channel/ryanodine receptor from skeletal muscle, J. Cell Biol. 127, 411–423.PubMedCrossRefGoogle Scholar
  48. Rusinko, N. and Lee, H.C., 1989, Widespread occurrence in animal tissues of an enzyme catalyzing the conversion of NAD+ into a cyclic metabolite with intracellular Ca2+ mobilizing activity, J. Biol Chem. 64, 11725–11731.Google Scholar
  49. Serysheva, I., Orlova, E.V., Chiu, W., Sherman, M.B., Hamilton, S.L.H. and van Heel, M., 1995, Electron cryomicroscopy and angular reconstitution used to visualize the skeletal muscle calcium release channel, Nature Struct. Biol 2, 18–24.PubMedCrossRefGoogle Scholar
  50. Sharma, M.R., Penczek, P., Grassucci, R., Xin, H., Fleischer, S. and Wagenknecht, T., 1998, Cryoelectron microscopy and image analysis of the cardiac ryanodine receptor, J. Biol Chem. 273, 18429–18434.PubMedCrossRefGoogle Scholar
  51. Shirokova, M., Shirokov, R., Rossi, D., Gonzales, A., Kirsch, W.G., Garcia, J., Sorrentino, V. and Rios, E., 1999, Spatially segregated control of Ca2+ release in developing skeletal muscle of mice, J. Physiol (Lond.) 521(2), 483–495.CrossRefGoogle Scholar
  52. Sitsapesan, R. and Williams, A.J., 1995, Cyclic ADP-ribose and related compounds activate sheep skeletal sarcoplasmic reticulum Ca2+ release channel, Am. J. Physiol 268, C1235–C1240.PubMedGoogle Scholar
  53. Smith, J.S., Coronado, R. and Meissner, G.,1985, Sarcoplasmic reticulum contains adenine nucleotide-activated calcium channels, Nature 316, 446–449.PubMedCrossRefGoogle Scholar
  54. Sonnleitner, A., Conti, A., Bertocchini, F., Schindler, H. and Sorrentino, V., 1998, Functional properties of the Ryanodine receptor type 3 (RyR3) Ca2+ release channel, EMBO J. 17, 2790–2798.PubMedCrossRefGoogle Scholar
  55. Sorrentino, V. and Volpe, P., 1993, Ryanodine receptors: How many, where and why?, Trends Pharmacol Sci. 14, 98–103.PubMedCrossRefGoogle Scholar
  56. Sorrentino, V. and Reggiani, C, 1999, Expression of the ryanodine receptor type 3 in skeletal muscle. A new partner in excitation-contraction coupling?, Trends Card. Med. 9, 54–61.CrossRefGoogle Scholar
  57. Suko, J., Maurer-Fogy, I., Plank, B., Bertel, O., Wyskovsky, W., Hohenegger, M. and Hellmann, G., 1993, Phosphorilation of serine 2843 in ryanodine receptor-calcium release channel of skeletal muscle by cAMP, cGMP and CAM-dependent protein kinase, Biochim. Biophys. Acta 1175, 193–206.PubMedCrossRefGoogle Scholar
  58. Sutko, J.L. and Airey, J.A., 1996, Ryanodine receptors Ca2+ release channels: Does diversity in form equal diversity in function, Physiol. Rev. 76, 1027–1071.PubMedGoogle Scholar
  59. Takasawa, S., Natsa, K., Yonekura, H. and Okamoto, H.,1993, Cyclic ADP-ribose in insulin secretion from pancreatic beta cells, Science 259, 370–373.PubMedCrossRefGoogle Scholar
  60. 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, 439–445.PubMedCrossRefGoogle Scholar
  61. Takeshima, H., Iino, M., Takekura, H., Nishi, M., Kuno, J., Minowa, O., Takano, H. and Noda, T.,1994, Excitation-contraction uncoupling and muscular degeneration in mice lacking functional skeletal muscle ryanodine-receptor gene, Nature 369, 556–559.PubMedCrossRefGoogle Scholar
  62. Takeshima, H., Yamazawa, T., Ikemoto, T., Takekura, H., Nishi, M., Noda, T. and Iino, M., 1995, Ca2+-induced Ca2+ release in myocites from dyspedic mice lacking the type-1 ryanodine receptor, EMBO J. 14, 2999–3006.PubMedGoogle Scholar
  63. Takeshima, H., Ikemoto, T., Nishi, M., Nishiyama, N., Shimuta, M., Sugitani, Y, Kuno, J., Saito, I., Saito, H., Endo, M., Iino, M. and Noda, T., 1996, Generation and characterization of mutant mice lacking ryanodine receptor type 3, J. Cell Biol. 271, 19649–19652.Google Scholar
  64. Takeshima, H., Komazaki, S., Hirose, K., Nishi, M., Noda, T. and Iino, M., 1998, Embryonic lethality and abnormal cardiac myocytes in mice lacking ryanodine receptor type 2, EMBO J. 17, 3309–3316.PubMedCrossRefGoogle Scholar
  65. Tarroni, P., Rossi, D., Conti, A. and Sorrentino, V., 1997, Expression of the ryanodine receptor type 3 calcium release channel during development and differentiation of mammalian skeletal muscle cells, J. Biol Chem. 272, 19808–19813.PubMedCrossRefGoogle Scholar
  66. Tripathy, A., Xu, L., Mann, G. and Meissner, G., 1995, Calmodulin activation and inhibition of skeletal muscle Ca2+ release channel (ryanodine receptor), Biophys. J. 69, 106–119.PubMedCrossRefGoogle Scholar
  67. Wagenknecht, T., Radermacher, M, Grassucci, R., Berkowitz, J., Xin, H.B. and Fleisher, S., 1997, Locations of calmodulin and FK506-binding protein on the three-dimensional architecture of the skeletal muscle ryanodine receptor, J. Biol. Chem. 272, 32463–32471.PubMedCrossRefGoogle Scholar
  68. Witcher, D.R., Kovacs, R.J., Schulman, H., Cefali, D.C. and Jones, L.R., 1991, Unique phosphorylation site on the cardiac ryanodine receptor regulates calcium channel activity, J. Biol. Chem. 266, 11144–11152.PubMedGoogle Scholar
  69. Yang, H.C., Reedy, M.M., Bruke, C.L. and Strasburg, G.M.,1994, Calmodulin interaction with the skeletal muscle sarcoplasmic reticulum calcium channel protein, Biochemistry 33, 518–525.PubMedCrossRefGoogle Scholar
  70. Zhang, Y., Chen, H.S., Khanna, V.K., De Leon, S., Phillips, M.S., Schappert, K., Britt, B.A., Brownell, A.K.W. and MacLennan, D.H., 1993, A mutation in the human ryanodine receptor gene associated with central core desease, Nat. Genet. 5, 46–50.PubMedCrossRefGoogle Scholar
  71. Zhao, M., Li, P., Li, X., Zhang, L., Winkfein, R., Wayne Chen, S.R., 1999, Molecular identification of the ryanodine receptor pore-forming segment, J. Biol. Chem. 274, 25971–25974.PubMedCrossRefGoogle Scholar
  72. Zorzato, F., Fujii, J., Otsu, K., Phillips, M., Green, N.M., Lai, RA., 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, 2244–2256.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2000

Authors and Affiliations

  • Daniela Rossi
    • 1
  • Virginia Barone
    • 2
  • Ilenia Simeoni
    • 1
  • Vincenzo Sorrentino
    • 1
    • 2
  1. 1.Section of Molecular Medicine, Department of NeurosciencesUniversity of SienaItaly
  2. 2.DIBITIstituto Scientifico San RaffaeleMilanItaly

Personalised recommendations