The Ryanodine Receptor Family of Intracellular Calcium Release Channels

Advances in Pharmacology

Volumn 33, Issue C, 1995, Pages 67-90

  Sorrentino, Vincenzo ^a  

^a UNIVERSITY OF SIENA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CALCIUM CHANNEL; CALMODULIN BINDING PROTEIN; ION CHANNEL; MUSCLE PROTEIN; RYANODINE RECEPTOR;

ANIMAL; CHEMICAL STRUCTURE; CLASSIFICATION; METABOLISM; PHYSIOLOGY; REVIEW; TISSUE DISTRIBUTION;

ANIMALS; CALCIUM; CALCIUM CHANNELS; CALMODULIN-BINDING PROTEINS; ION CHANNELS; MOLECULAR STRUCTURE; MUSCLE PROTEINS; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL; TISSUE DISTRIBUTION;

EID: 0029438246     PISSN: 10543589     EISSN: 15578925     Source Type: Book Series    
DOI: 10.1016/S1054-3589(08)60666-3     Document Type: Article

References (130)

1. Airey, J.A., Baring, M.D., Beck, C.F., Chelliah, Y., Deerinck, T.J., Ellisman, M.H., Houenou, L.J., McKemy, D.D., Sutko, J.L., Talvenheimo, J., Failure to make normal a ryanodine receptor is an early event associated with the crooked neck dwarf (cn) mutation in chicken. Dev. Dyn. 197 (1993), 169–188.
2. Airey, J.A., Beck, C.F., Murakami, K., Tanksley, S.J., Deerinck, T.J., Ellisman, M.H., Sutko, J.L., Identification and localization of two triad junctional foot protein isoforms in mature avian fast twitch skeletal muscle. J. Biol. Chem. 265 (1990), 14187–14194.
3. Airey, J.A., Deerinck, T.J., Ellisman, M.H., Houenou, L.J., Ivanenko, A., Kenyon, J.L., McKemy, D.D., Sutko, J.L., Crooked neck dwarf (cn) mutant chicken skeletal muscle cells in low density primary cultures fail to express normal a. ryanodine receptor and exhibit a partial mutant phenotype. Dev. Dyn. 197 (1993), 189–202.
4. Ailey, J.A., Grinsell, M.M., Jones, L.R., Sutko, J.I., Witcher, D., Three ryanodine receptor isoforms exist in avian striated muscles. Biochemistry 32 (1993), 5739–5745.
5. 2+ release channel complex. J. Biol. Chem. 264 (1989), 1329–1335.
6. Berridge, M.J., Inositol triphosphate and calcium signalling. Nature 361 (1993), 315–325.
7. Berridge, M.J., A tale of two messengers. Nature 365 (1993), 388–389.
8. Bezprozvanny, I., Watras, J., Ehrlich, B.E., Bell-shaped calcium-response curves of lns(l,4,5)P3-and calcium-gated channels from endoplasmic reticulum of cerebellum. Nature 351 (1991), 751–754.
9. Blondel, O., Takeda, J., Janssen, H., Seino, S., Bell, G.I., Sequence and functional characterization of a third inositol trisphosphate receptor subtype, IP3R-3, expressed in pancreatic islets, kidney, gastrointestinal tract, and other tissues. J. Biol. Chem. 268 (1993), 11356–11363.
10. 2+ release. Current Biology 4 (1994), 169–176.
11. Brillantes, A.B., Ondrias, K., Scott, A., Kobrinsky, E., Ondriasova, E., Moschella, M.C., Jayaraman, T., Landers, M., Ehrlich, B.E., Marks, A.R., Stabilization of calcium release channel (ryanodine receptor) function by FK-506-binding protein. Cell 77 (1994), 513–523.
12. K.P., Campbell, C.M., Knudson, T., Imagawa, A.T., Leung, J.L., Sutko, S.D., Kahl, C.R., Raab, L., Madson, Identification and characterization of the high affinity [3, H]ryanodine receptor of the junctional sarcoplasmic reticulum Ca, 2+, release channel, J. Biol. Chem., (1987), 262, 6460-6463
13. Cavanna, J.S., Greenfield, A.J., Johnson, K.J., Marks, A.R., Nadal-Ginard, B., Brown, S.D.M., Establishment of the mouse chromosome 7 region with homology to the myotonic dystrophy region of human chromosome 19q. Genomics 7 (1990), 12–18.
14. 2+. Biochem. J. 275 (1991), 697–701.
15. 2+ release from caffeine-sensitive stores in adrenal chromaffin cells. J. Biol. Chem. 268 (1993), 27076–27083.
16. 2+ mobilization by ryanodine receptors is due to all-or-none release from functionally discrete intracellular stores. Biochem. J. 301 (1994), 879–883.
17. 2+ release channel (ryanodine receptor) resulting from partial digestion of rabbit skeletal muscle sarcoplasmic reticulum. J. Biol. Chem. 268 (1993), 22642–22649.
18. 2+ release channel (ryanodine receptor) of rabbit skeletal muscle sarcoplasmic reticulum. J. Biol. Chem. 267 (1992), 23318–23326.
19. 2+ release channel (ryanodine receptor) of rabbit skeletal muscle sarcoplasmic reticulum. J. Biol. Chem. 268 (1993), 13414–13421.
20. Clapper, D.L., Walseth, T.F., Dargie, P.J., Lee, H.C., Pyridine nucleotide metabolites stimulate calcium release from sea urchin egg microsomes desensitized to inositol trisphosphate. J. Biol. Chem. 262 (1987), 9561–9568.
21. Coronado, R., Morrissette, J., Sukhareva, M., Vaugham, D.M., Structure and function of ryanodine receptors. Am. J. Physiol. 266 (1994), C1485–C1504.
22. Danoff, S.K., Ferris, C.D., Donath, C., Fischer, G.A., Munemitsu, S., Ullrich, A., Synder, S.H., Ross, C.A., Inositol 1,4,5-triphosphate receptors: Distinct neuronal and non-neuronal forms derived by alternative splicing differ in phosphorylation. Proc. Natl. Acad. Sci. USA 88 (1991), 2951–2955.
23. 2+ -release channels. Trends Pharmacol. Sci. 15 (1994), 145–149.
24. Fabiato, A., Appraisal of the physiological relevance of two hypotheses for the mechanism of calcium release from the mammalian cardiac sarcoplasmic reticulum: calcium induced release versus charge-coupled release. Mol. Cell. Biochem. 89 (1989), 135–140.
25. Ferris, C.D., Snyder, S.H., Inositol 1,4,5+trisphosphate-activated calcium channels. Annu. Rev. Physiol. 54 (1992), 469–488.
26. Fleischer, S., Inui, M., Biochemistry and biophysics of exitation-contraction cou pling. Annu. Rev. Biophys. Biophys. Chem. 18 (1989), 333–364.
27. 2+ release channels with ryanodine in junctional terminal cisternae of sarcoplasmic reticulum of fast skeletal muscle. Proc. Natl. Acad. Sci. USA 82 (1985), 7256–7259.
28. Flucher, B.E., Andrews, S.B., Fleischer, S., Marks, A.R., Caswell, A., Powell, J.A., Triad formation: Organization and function of the sarcoplasmic reticulum calcium release channel and triadin in normal and dysgenic muscle in vitro. J. Cell Biol. 123 (1993), 1161–1174.
29. Franzini-Amstrong, C., Jorgensen, A.O., Structure and development of E-C coupling units in skeletal muscle. Annu. Rev. Physiol. 56 (1994), 509–534.
30. 2+ release channels are diffentially expressed in rabbit brain. J. Neurosci. 14 (1994), 4794–4805.
31. Furuichi, T., Shiota, C., Mikoshiba, K., Distribution of inositol 1,4,5-trisphosphate receptor mRNA in mouse tissues. FEBS Lett. 267 (1990), 85–88.
32. Furuichi, T., Yoshikawa, S., Miyawaki, A., Wada, K., Maeda, N., Mikoshiba, K., Primary structure and functional expression of the inositol 1,4,5-trisphosphate-binding protein P400. Nature 342 (1989), 32–38.
33. 2+ release in sea urchin egg homogenates: Modulation by cyclic ADP-ribose. Science 13 (1991), 1143–1145.
34. Galione, A., McDougall, A., Busa, W.B., Willmot, N., Gillot, I., Whitaker, M., Redundant mechanisms of calcium-induced calcium release underlying calcium waves during fertilization of sea urchin eggs. Science 261 (1993), 348–352.
35. 2+ in sea urchin eggs by stimulating cyclic ADP-ribose synthesis. Nature 365 (1993), 456–459.
36. 2+ channel that is regulated by TGF–α. Science 257 (1992), 91–94.
37. Giannini, G., Conti, A., Mammarella, S., Scrobogna, M., Sorrentino, V., The ryanodine receptor/Calcium channel genes are widely and differentially expressed in murine brain and peripheral tissues. J. Cell Biol. 128 (1995), 893–906.
38. 2+ release. J. Biol. Chem. 267 (1992), 20850–20856.
39. Gillard, E.F., Otsu, K., Fujii, J., Duff, C., Leon, S.D., Khanna, V.K., Britt, B.A., Worton, R.G., MacLennan, D.H., Polymorphisms and deduced amino acid substitutions in the coding sequence of the ryanodine receptor (RyRl) gene in individuals with malignant hyperthermia. Genomics 13 (1992), 1247–1254.
40. Gillard, E.F., Otsu, K., Fujii, J., Kahna, V.K., Leon, S.D., Derdemezi, J., Britt, B.A., Duff, C.L., Worton, R.G., MacLennan, D.H., A substitution of cysteine for arginine 614 in the ryanodine receptor is potentially caustive of human malignant hyperthermia. Genomics 11 (1991), 751–755.
41. Click, D.L., Hellmich, M.R., Beushausen, S., Tempst, P., Bayley, H., Strumwasser, F., Primary structure of a molluscan egg-specific NADase a second-messenger enzyme. Cell Regul. 2 (1991), 211–218.
42. Gorza, L., Vettore, S., Volpe, P., Sorrentino, V., Samuel, J.-L., Anger, M., and Lompre, A. M. Cardiac myocytes differ in mRNA composition for sarcoplasmic reticulum calcium channels and calcium pumps. Ann. N. Y. Acad. Set., in press.
43. 2+ release in heart. Science, 260, 1993, 807.
44. Hakamata, Y., Nakai, J., Takeshima, H., lmoto, K., Primary structure and distribution of a novel ryanodine receptor/calcium release channel from rabbit brain. FEBS Lett. 312 (1992), 229–235.
45. 2+ -release channels: Identification and expression patterns of the inositol 1,4,5-triphos-phate and the ryanodine receptor genes. Development 166 (1992), 967–975.
46. Hellmich, M.R., Stumwasser, F., Purification and characterization of a molluscan egg specific NADase, a second-messenger enzyme. Cell Regul. 2 (1991), 193–202.
47. Howard, M., Grimaldi, J.C., Bazan, J.F., Lund, F.E., Santos-Agrumedo, L., Parkhouse, R.M.E., Walseth, T.F., Lee, H.C., Formation and hydrolysis of cyclic ADP-Ribose catalyzed by Lymphocyte antigen CD38. Science 262 (1993), 1056–1059.
48. Inui, M., Saito, A., Fleischer, S., Isolation of the ryanodine receptor from cardiac sarcoplasmic reticulum and identity with the feet structures. J. Biol. Chem. 262 (1987), 15637–15642.
49. Inui, M., Saito, A., Fleischer, S., Purification of the ryanodine receptor and identity with the feet structures of the terminal cisternae of sarcoplasmic reticulum from fast skeletal muscle. Biol. Chem. 262 (1987), 1740–1747.
50. Jayaraman, T., Brillantes, A.M., Timerman, A.P., Fleischer, S., Erdjument-Bromage, H., Tempst, P., Marks, A.R., FK506 binding protein associated with the calcium release channel (ryanodine receptor). J. Biol. Chem. 267 (1992), 9474–9477.
51. 2+ -release channel/ryanodine receptor is localized in junctional and corbular sarcoplasmic reticulum in cardiac muscle. J. Cell Biol. 120 (1993), 969–980.
52. Junker, J., Sommer, J.R., Sar, M., Meissner, G., Extended Junctional Sarcoplasmic reticulum of avian cardiac muscle contains functional ryanodine receptors. J. Biol. Chem. 269 (1994), 1627–1634.
53. Kaisho, T., Ishikawa, J., Oritani, K., Inazawa, J., Tomizawa, H., Muraoka, O., Ochi, T., Hirano, T., BST-1, a surface molecule of bone marrow stromal cell lines that facilitates pre-B-cell growth. Proc. Natl. Acad. Sci. USA 91 (1994), 5325–5328.
54. Kim, H., Jacobson, E.L., Jacobson, M.K., Synthesis and degradation of cyclic ADP-ribose by NAD glycohydrolases. Science 261 (1993), 1330–1333.
55. Y.K., Kim, H.H., Valdivia, E.B., Maryon, P., Anderson, R., Coronado, High molecular weight proteins in the nematode C. elegans bind [3, H]ryanodine and form a large conductance channel, Biophysics, (1992), 63, 1379-1384
56. Kuwajiima, G., Futatsugi, A., Niinobe, M., Nakanishi, S., Mikoshiba, K., Two types of ryanodine receptors in mouse brain: Skeletal muscle type exclusively in purkinje cells and cardiac muscle type in various neurons. Neuron 9 (1992), 1133–1142.
57. 2+ channel within the ryanodine receptor complex from cardiac sarcoplasmic reticulum. Biochem. Biophys. Res. Commun. 151 (1988), 441–449.
58. Lai, F., Erickson, H., Rousseau, E., Liu, Q., Meissner, G., Purification and reconstitution of the calcium release channel from skeletal muscle. Nature (London) 331 (1988), 315–319.
59. 2+ release channel complex of skeletal muscle sarcoplasmic reticulum. Evidence for a cooperatively coupled, negatively charged homotetramer. J. Biol. Chem. 264 (1989), 16776–16785.
60. 2+ -release channel isoform in mammalian brain. Biocbem. J. 288 (1992), 553–564.
61. Lee, H.C., Specific binding of cyclic ADP-ribose to calcium-storing microsomes from sea urchin eggs. J. Biol. Chem. 266 (1991), 2276–2281.
62. Lee, H.C., Potentiation of calcium- and caffeine-induced calcium release by cyclic ADP-ribose. J. Biol. Chem. 268 (1993), 293–299.
63. Lee, H.C., Aarhus, R., Wide distribution of an enzyme that catalyzes the hydrolysis of cyclic ADP-ribose. Biochim. Biophys. Acta 1164 (1993), 68–74.
64. Lee, H.C., Aarhus, R., Warlseth, T.F., Calcium mobilization by dual receptors during fertilization of sea urchin eggs. Science 261 (1993), 352–355.
65. +2 mobilizing activity. J. Biol. Chem. 264 (1989), 1608–1615.
66. Lesh, R.E., Marks, A.R., Somlyo, A.V., Fleischer, S., Somlyo, A.P., Antiryanodine receptor antibody binding sites in vascular and endocardial endothelium. Cir. Res. 72 (1993), 481–488.
67. Lodish, H.F., Multi-spanning membrane proteins: How accurate are the models?. Trends Bio. Sci. 13 (1988), 332–334.
68. Lu, X., Xu, L., Meissner, G., Activation of the skeletal muscle calcium release channel by a cytoplasmic loop of the dihydropyridine receptor. J. Biol. Chem. 269 (1994), 6511–6516.
69. MacLennan, D.H., Duff, C., Zorzato, F., Fujii, J., Phillips, M., Korneluk, R.G., Frodis, W., Britt, B.A., Worton, R.G., Ryanodine receptor gene is candidate for predisposition to malignant hyperthermia. Nature 343 (1990), 559–564.
70. MacLennan, D.H., Phillips, M.S., Malignant hyperthermia. Science 256 (1992), 789–794.
71. Maeda, N., Kawasaki, T., Nakade, S., Yokota, N., Taguchi, T., Kasai, M., Mikoshiba, K., Structural and functional characterization of inositol 1,4,5–trisphosphate receptor channel from mouse cerebellum. J. Biol. Chem. 266 (1991), 1109–1116.
72. Malavasi, F., Funaro, A., Roggero, S., Horenstein, A., Calosso, L., Mehta, K., Human CD38: A glycoprotein search of a function. Immunol. Today 15 (1994), 95–97.
73. Marks, A.R., Tempst, P., Hwang, K.S., Taubman, M.B., Inui, M., Chadwick, C., Fleischer, S., Nadal-Ginard, B., Molecular cloning and characterization of the ryanodine receptor/junctional channel complex cDNA from skeletal muscle sarcoplasmic reticulum. Proc. Nat. Acad. Sci. USA 86 (1989), 8683–8687.
74. Maranto, A.R., Primary structure, ligand binding, and localization of the human type 3 inositol 1,4,5-trisphosphate receptor expressed in intestinal epithelium. J. Biol. Chem. 269 (1993), 1222–1230.
75. Mattei, M.G., Giannini, G., Moscatelli, F., Sorrentino, V., Chromosomal localization of murine ryanodine receptor genes RYR1, RYR2, and RYR3 by situ hybridization. Genomics 22 (1994), 202–204.
76. McCarthy, T., Healy, J.M.S., Heffron, J.J.A., Lehane, M., Deufel, T., Lehmann-Horn, F., Farral, M., Johnson, K., Localization of the malignant hyperthermia susceptibility locus to human chromosome 19ql2–13.2. Nature (London) 343 (1990), 562–564.
77. McPherson, P., Kim, Y.K., Valdivia, H., Knudson, M., Takekura, H., Franzini-Amstrong, C., Coronado, R., Campbell, K., The brain ryanodine receptor: A caffeine-sensitive calcium release channel. Neuron 7 (1991), 17–25.
78. 2+ release channel. J. Biol. Chem. 268 (1993), 19785–19790.
79. 2+ release channel. J. Biol. Chem. 268 (1993), 13765–13768.
80. 2+ release in sarcoplasmic reticulum. J. Biol. Chem. 259 (1984), 2365–2374.
81. Meissner, G., Evidence of role for calmodulin in the regulation of calcium release from skeletal muscle sarcoplasmic reticulum. Biochemistry 25 (1986), 244–251.
82. 2+ channel. Nature 364 (1993), 76–79.
83. Mignery, G.A., Newton, B.T.A.C.L. III, Sudhof, T.C., Structure and expression of the rat inositol 1,4,5-trisphosphate receptor. J. Biol. Chem. 265 (1990), 12679–12685.
84. Mikoshiba, K., Inositol 1,4,5-trisphosphate receptor. Trends Pharmacol. Sci. 14 (1993), 86–89.
85. 2+ release in rabbit skeletal muscle sarcoplasmic reticulum. FEBS Lett. 330 (1993), 270–274.
86. Nakagawa, T., Okano, H., Furuichi, T., Aruga, J., Mikoshiba, K., The subtypes of the mouse inositol 1,4,5-trisphosphate receptor are expressed in a tissue-specific and developmentally specific manner. Proc. Natl. Acad. Sci. USA 88 (1991), 6244–6248.
87. Nakai, J., Imagawa, T., Hakamata, Y., Shigekawa, M., Takeshima, H., Numa, S., Primary structure and functional expression from cDNA of the cardiac ryanodine receptor/calcium release channel. FEBS Lett. 271 (1990), 169–177.
88. O'Brien, J., Meissner, G., Block, B.A., The fastest contracting muscles of nonmam-malian vertebrates express only one isoform of the ryanodine receptor. Biophys. J. 65 (1993), 2418–2427.
89. Olivares, E.B., Tanksley, S.J., Airey, J.A., Beck, C.F., Ouyang, Y., Deerinck, T.J., Ellisman, M.H., Sutko, J.L., Nonmammalian vertebrate skeletal muscles express two triad junctional foot protein isoforms. Biophys. J. 59 (1991), 1153–1163.
90. Otsu, K., Fujii, J., Periasamy, M., Difilippantonio, M., Uppender, M., Ward, D.C., MacLennan, D.H., Chromosome mapping of five human cardiac and skeletal muscle sarcoplasmic reticulum protein genes. Genomics 17 (1993), 507–509.
91. 2+ release channel(ryanodine receptor) of rabbit cardiac muscle sarcoplasmic reticulum. J. Biol. Chem. 265 (1990), 13472–13483.
92. Oyamada, H., Murayama, T., Takagi, T., lino, M., Iwabe, N., Miyata, T., Ogawa, Y., Endo, M., primary structure and distribution of ryanodine-binding protein isoforms of the bullfrog skeletal muscle. Biol. Chem. 269 (1994), 17206–17214.
93. Percival, A.L., Williams, A.J., Kenyon, J.L., Grinsell, M.M., Airey, J.A., Sutko, J.L., Chicken skeletal muscle ryanodine receptor isoforms/ion channel properties. Biophys. J. 67 (1994), 1839–1850.
94. Pessah, I., Francini, A., Scales, D., Waterhouse, A., Casida, J., Calcium-ryanodine receptor complex. Solubilization and partial characterization from skeletal muscle junc tional sarcoplasmic reticulum vesicles. J. Biol. Chem. 261 (1986), 8643–8648.
95. Quane, K.A., Healy, J.M.S., Keating, K.E., Manning, B.M., Couch, F.J., Palmucci, L.M., Doriguzzi, C., Fagerlund, T.H., Berg, K., Ording, H., Bendixen, D., Mortier, W., Linz, U., Muller, C.R., McCarthy, T.V., Mutations in the ryanodine receptor gene in central core disease and malignant hyperthermia. Nature 5 (1993), 51–54.
96. Ross, C.A., Danoff, S.K., Schell, M.J., Snyder, S.H., Ullrich, A., Three additional inositol 1,4,5–trisphosphate receptors: Molecular cloning and differential localization in brain and peripheral tissues. Proc. Nat. Acad. Sci. USA 89 (1992), 4265–4269.
97. 2+. -release channel: Activation by caffeine. Am. J. Physiol. 256 (1989), H328–H333.
98. 2+-mobilizing activity. J. Biol. Chem. 264 (1989), 11725–11731.
99. 2+-dependent ryanodine binding site: soluble preparation from rabbit cardiac sarcoplasmic reticulum. Biochim. Biophys. Acta 861 (1986), 399–405.
100. 2+ release channel (ryanodine receptor) has functional properties distinct from the mammalian channel proteins. J. Biol. Chem. 267 (1992), 15893–15901.
101. 2+ release channels in rat brain. J. Neurosci. 13 (1993), 3051–3063.
102. Smith, J., Coronado, R., Meissner, G., Sarcoplasmic reticulum contains adenine nucleotide-activated channels. Nature (London) 316 (1985), 446–449.
103. Smith, J.S., Imagawa, T., Ma, J., Fill, M., Campbell, K.P., Coronado, R., Purified ryanodine receptor from rabbit skeletal muscle is the calcium-release channel of sarcoplasmic reticulum. J. Gen. Physiol. 92 (1988), 1–26.
104. Sorrentino, V., Giannini, G., Malzac, P., Mattei, M.G., Localization of a novel ryanodine receptor gene (RYR3) to human chromosome 15ql4-ql5 by in situ hybridization. Genomics 18 (1993), 163–165.
105. Sorrentino, V., Volpe, P., Ryanodine receptors: how many, where and why?. Trends Pharmacol. Sci. 14 (1993), 98–105.
106. States, D.J., Walseth, T.F., Lee, H.C., Similarities in amino acid sequences of Aplysia ADP-ribosyl cyclase and human lymphocyte antigen CD38. Trends Biochem. Sci., 17, 1992, 495.
107. Strand, M., Louis, C., Mickleson, J., Phosphorilation of the porcine skeletal and cardiac muscles sarcoplasmic reticulum ryanodine receptor. Biochim. Biophys. Acta. 1175 (1993), 319–326.
108. 3 receptor. EMBO J. 10 (1991), 3199–3206.
109. Suko, J., Maurer-Fogy, I., Plank, B., Bertel, O., Wyskovsky, W., Hohenegger, M., Hellmann, G., Phosphorylation of serine 2843 in ryanodine receptor-calcium release channel of skeletal muscle by cAMP-, cGMP- and CaM-dependent protein kinase. Biochim. Biophys. Acta 1175 (1993), 193–206.
110. Takasawa, S., Nata, K., Yonekura, H., Okamoto, H., Cyclic ADP-ribose in insulin secretion from pancreatic cells. Science 259 (1993), 370–373.
111. Takasawa, S., Tohgo, A., Noguchi, N., Koguma, T., Nata, K., Sugimoto, T., Yonekura, H., Okamoto, H., Synthesis and hydrolysis of cyclic ADP-ribose by human leukocyte antigen CD38 and inhibition of the hydrolysis by ATP. J. Biol. Chem. 268 (1993), 26052–26054.
112. H., Takeshima, M., Nishi, N., Iwabe, T., Miyata, T., Hosoya, L., Masai, Y., Hotta, Isolation and characterization of a gene for a ryanodine receptor/calcium release channel in Drosophila melanogaster, FEBS Lett., (1994), 337, 81-87
113. Takeshima, H., Nishimura, S., Matsumoto, T., Ishida, H., Kangawa, K., Minamino, N., Matsuo, H., Ueda, M., Hanaoka, M., Hirose, T., Numa, S., Primary structure and expression from complementary DNA of skeletal muscle ryanodine receptor. Nature (London), 1989, 439–445.
114. 2+ release. Biochem. J. 291 (1993), 757–763.
115. Valdivia, H.H., Fuentes, O., El-Hayek, R., Morrisette, J., Coronado, R., Activation of the ryanodine receptor Ca2+ release channel of sarcoplasmic reticulum by a novel scorpion venom. J. Biol. Chem. 266 (1991), 19135–19138.
116. 2+ -release channel of skeletal and cardiac muscle. Proc. Nat. Acad. Sci. USA 89 (1992), 12185–12189.
117. Verma, A., Hirsch, D.J., Snyder, S.H., Calcium pools mobilized by calcium or inositol 1,4,5-trisphosphate are differentially localized in rat heart and brain. Mol. Biol. Cell 3 (1992), 621–631.
118. Verma, A., Ross, C.A., Verma, D., Supattapone, S., Snyder, S.H., Rat brain endoplasmic reticulum calcium pools are anatomically and functionally segregated. Cell Regul. 1 (1990), 781–790.
119. Wagenknecht, T., Grassucci, R., Frank, J., Saito, A., Inui, M., Fleischer, S., Three dimensional architecture of the calcium channel/foot structure of sarcoplasmic reticulum. Nature (London) 338 (1989), 167–170.
120. Walseth, T.F., Aarhus, R., Zeleznikar, R.J., Lee, H.C., Determination of endogenous levels of cyclic ADP-ribose in rat tissues. Biochem. Biophys. Acta 1094 (1991), 113–120.
121. Wang, J., Best, P.M., Inactivation of the sarcoplasmic reticulum calcium channel by protein kinase. Nature (London) 359 (1992), 739–741.
122. Waterston, R., Martin, C., Craxton, M., Huynh, C., Coulson, A., Hillier, L., Durbin, R., Green, P., Shownkeen, R., Halloran, N., Metzstein, M., Hawkins, T., Wilson, R., Berks, M., Du, Z., Thomas, K., Thierry-Mieg, J., Sulston, J., A survey of expressed genes in Caenorhabditis elegans. Nature Gen. 1 (1992), 114–123.
123. Witcher, D., Kovacs, R., Schulman, H., Cefali, D., Jones, L., Unique phosphorylation site on the cardiac ryanodine receptor regulates calcium channel activity. J. Biol. Chem. 266 (1991), 11144–11152.
124. 2+ Jcalmodulin-dependent protein kinase is conserved in the brain ryanodine receptor. J. Biol. Chem. 267 (1992), 4963–4967.
125. 2+ release channel with an Azido derivative of Ryanodine. J. Biol. Chem. 269 (1994), 13076–13079.
126. Yamamoto-Hino, M., Sugiyama, T., Hikinchi, K., Mattei, M.G., Hasegawa, K., Sekine, S., Sakurada, K., Miyawakis, A., Furuichi, T., Hasegawa, M., Mikoshiba, K., Cloning and characterization of human type 2 and type 3 inositol 1,4,5-triphosphate receptors. Recept. Channels 2 (1994), 9–22.
127. Yoshida, A., Takahashi, M., Imagawa, T., Shigekawa, M., Takisawa, H., Nakamura, T., Phosphorilation of ryanodine receptors in rat myocytes during beta-adrenergic stimulation. J Biochem. (Tokyo) 111 (1992), 186–190.
128. Zarka, A., Shoshan-Barmatz, V., Characterization and photoaffinity labeling of the ATP binding site of the ryanodine receptor from skeletal muscle. Eur. J. Biochem. 213 (1993), 147–154.
129. Zhang, Y., Chen, H.S., Khanna, V.K., Leon, S.D., Phillips, M.S., Shappert, K., Britt, B.A., Brownell, A.K.W., MacLennan, D.H., A mutation in the human ryanodine receptor gene associated with central core disease. Nature 5 (1993), 46–50.
130. 2+ release channel (ryanodine receptor) of skeletal muscle sarcoplasmic reticulum. J Biol. Chem. 265 (1990), 2244–2256.