Abstract
The Ca2+-gated Ca2+ release channel of aortic sarcoplasmic reticulum (SR) was partially purified and reconstituted into planar lipid bilayers. Canine and porcine aorta microsomal protein fractions were solubilized in the detergent 3-[(3-cholamidopropyl)dimethylammonio]-1-propane sulphonate (CHAPS) in the presence and absence of 3[H]-ryanodine and centrifuged through linear sucrose gradients. A single 3[H]-ryanodine receptor peak with an apparent sedimentation coefficient of 30 s was obtained. Upon reconstitution into planar lipid bilayers, the unlabelled 30 s protein fraction induced the formation of a Ca2+- and monovalent-ion-conducting channel (110 pS in 100 mM Ca2+, 360 pS in 250 mM K+). The channel was activated by micromolar Ca2+, modulated by millimolar adenosine triphosphate, Mg2+ and the Ca2+-releasing drug caffeine, and inhibited by micromolar ruthenium red. Micro- to millimolar concentrations of the plant alkaloid ryanodine induced a permanently closed state of the channel. Our results suggest that smooth muscle SR contains a Ca2+-gated Ca2+ release pathway, with properties similar to those observed for the skeletal and cardiac ryanodine receptor/Ca2+ release channel complexes.
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References
Anderson K, Lai FA, Liu Q-Y, Rousseau E, Erickson HP, Meissner G (1989) Structural and functional characterization of the purified cardiac ryanodine receptor-Ca2+ release channel complex. J Biol Chem 264:1329–1335
Breemen C van, Saida K (1989) Cellular mechanisms regulating [Ca2+]i smooth muscle. Annu Rev Physiol 51:315–329
Breemen C van, Saida K, Yamamoto H, Hwang K, Twort C (1988) Vascular smooth muscle sarcoplasmic reticulum. Function and mechanisms of Ca2+ release. Ann NY Acad Sci 522:60–73
Chadwick CC, Saito A, Fleischer S (1990) Isolation of the inositol trisphosphate receptor from smooth muscle. Proc Natl Acad Sci USA 87:2132–2136
Ehrlich B, Watras J (1988) Inositol 1,4,5-trisphosphate activates a channel from smooth muscle sarcoplasmic reticulum. Nature 336:583–586
Endo M (1985) Calcium release from sarcoplasmic reticulum. In: Bronner F (ed) Current topics in membranes and transport, vol 25. Academic, New York, p 181
Fabiato A (1988) Computer programs for calculating total from specified free or free from specified total ionic concentrations in aqueous solutions containing multiple metals and ligands. Methods Enzymol 157:378–417
Ferris CD, Huganir RE, Snyder SE (1989) Calcium flux mediated by purified inositol 1,4,5-trisphosphate receptor in reconstituted lipid vesicles is allosteric regulated by adenine nucleotides. Proc Natl Acad Sci USA 87:2147–2151
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
Hai C-M, Murphy A (1989) Ca2+, crossbridge phosphorylation, and contraction. Annu Rev Physiol 51:285–298
Herrmann-Frank A, Darling E, Meissner G (1990) Single channel measurements of the Ca2+-gated ryanodine-sensitive Ca2+ release channel of vascular smooth muscle (abstract). Biophys J 57:156
Hymel E, Inui M, Fleischer S, Schindler H (1988) Purified ryanodine receptor of skeletal muscle sarcoplasmic reticulum forms Ca2+-activated oligomeric Ca2+ channels in planar bilayers. Proc Natl Acad Sci USA 85:441–445
Iino M (1987) Calcium dependent inositol trisphosphate-induced calcium release in the guinea-pig Taenia caeci. Biochem Biophys Res Commun 142:47–52
Iino M, Kobayashi T, Endo M (1988) Use of ryanodine for functional removal of the calcium store in smooth muscle cells of the guinea-pig. Biochem Biophys Res Commun 152:417–422
Kamm KE, Stull JT (1989) Regulation of smooth muscle contractile elements by second messengers. Annu Rev Physiol 51:299–313
Kanaide H, Shogakiushi Y, Kakamura M (1987) The norepinephrine-sensitive Ca2+ -storage site differs from the caffeine-sensitive site in vascular smooth muscle of the rat aorta. FEBS Lett 214:130–134
Kobayashi S, Kitazawa T, Somlyo AV, Somlyo AP (1989) Cytosolic heparin inhibits muscarinic and α-adrenergic Ca2+ release in smooth muscle. J Biol Chem 264:17997–18004
Lai FA, Meissner G (1989) The muscle ryanodine receptor and its intrinsic Ca2+ channel activity. J Bioenerg Biomembr 21:227–245
Lai FA, Erickson HP, Rouseau E, Eiu Q-Y, Meissner G (1988) Purification and reconstitution of the purified sarcoplasmic reticulum Ca2+ release channel into planar lipid bilayers. Nature 331:315–319
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
Leijten PAA, Breemen C van (1984) The effects of caffeine on the noradrenaline-sensitive calcium store in rabbit aorta. J Physiol (Lond) 357:327–339
Leijten PAA, Breemen C van (1986) The relationship between noradrenaline-induced contraction and 45Ca2+ efflux stimulation in rabbit mesenteric artery. Br J Pharmacol 89:739–749
Liu Q-Y, 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
Rousseau E, Smith JS, Henderson JS, Meissner G (1986) Single channel and 45Ca2+ flux measurements of the cardiac sarcoplasmic reticulum calcium channel. Biophys J 50:1009–1024
Rousseau E, Smith JS, Meissner G (1987) Ryanodine modifies conductance and gating behavior of single Ca2+ release channel. Am J Physiol 253:C364-C368
Smith JS, Coronado R, Meissner G (1986) Single channel measurements of the calcium release channel from skeletal muscle sarcoplasmic reticulum. J Gen Physiol 88:573–588
Smith JS, Imagawa T, Ma J, Fill M, Campbell KP, Coronado R (1988) Purified ryanodine receptor from rabbit skeletal muscle is the calcium release channel of sarcoplasmic reticulum. J Gen Physiol 92:1–26
Somlyo AP (1985) Excitation-contraction coupling and the ultrastructure of smooth muscle. Circ Res 57:497–508
Somlyo AP, Walker JW, Goldman YE, Trentham DR, Kobayashi S, Kitazawa T, Somlyo AV (1988) Inositol trisphosphate, calcium and muscle contraction. Philos Trans R Soc Lond [Biol] 320:399–414
Suarez-Isla BA, Irribarra U, Oberhauser A, Larralde L, Bull R, Hidalgo C, Jainivich E (1988) Inositol (1,4,5)-trisphosphate activates a calcium channel in isolated sarcoplasmic reticulum membranes. Biophys J 54:737–741
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
Valdivia C, Valdivia HV, Potter BVL, Coronado R (1990) Ca2+ release by inositol-trisphosphorothioate in isolated triads of rabbit skeletal muscle. Biophys J 57:1233–1243
Wagenknecht T, Grassucci R, Frank J, Saito A, Inui M, Fleischer S (1989) Three-dimensional architecture of the calcium channel/foot structure of sarcoplasmic reticulum. Nature 338:167–170
Worley PF, Grassucci R, Frank J. Saito A, Inui M, Fleischer S (1987) Characterization of inositol trisphosphate receptor binding in brain. J Biol Chem 262:12132–12136
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
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Herrmann-Frank, A., Darling, E. & Meissner, G. Functional characterization of the Ca2+-gated Ca2+ release channel of vascular smooth muscle sarcoplasmic reticulum. Pflugers Arch. 418, 353–359 (1991). https://doi.org/10.1007/BF00550873
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DOI: https://doi.org/10.1007/BF00550873