Abstract
Microinjection of inositol 1,4,5-trisphosphate (InsP 3 into intact skeletal muscle fibers isolated from frogs (Rana temporaria) increased resting cytosolic Ca2+ concentration ([Ca2+]i) as measured by double-barreled Ca2+-selective microelectrodes. In contrast, microinjection of inositol 1-phosphate, inositol 1,4-biphosphate, and inositol 1,4,5,6-tetrakisphosphate did not induce changes in [Ca2+]i. Incubation in low-Ca2+ solution, or in the presence of L-type Ca2+ channel blockers did not affect InsP 3Vinduced release of cytosolic Ca2+. Neither ruthenium red, a blocker of ryanodine receptor Ca2+-release channels, nor cytosolic Mg2+, a known inhibitor of the Ca2+-induced Ca2+-release process, modified the InsP 3induced release of cytosolic Ca2+. However, heparin, a blocker of InsP 3 receptors, inhibited InsP 3-induced release of cytosolic Ca2+. Also, pretreatment with dantrolene or azumulene, two inhibitors of cytosolic Ca2+ release, reduced [Ca2+]i, and prevented InsP 3 from inducing release of cytosolic Ca2+. Incubation in caffeine or lengthening of the muscle increased [Ca2+]i and enhanced the ability of InsP 3 to induce release of cytosolic Ca2+. These results indicate that InsP 3, at physiological concentrations, induces Ca2+ release in intact muscle fibers, and suggest that the InsP 3-induced Ca2+ release is regulated by [Ca2+]i. A Ca2+-dependent effect of InsP 3 on cytosolic Ca2+ release could be of importance under physiological or pathophysiological conditions associated with alterations in cytosolic Ca2+ homeostasis.
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References
Alamo L, Lopez JR, Caputo C (1985) The increase in muscle metabolic rate associated with stretching in skeletal muscle might be related to an increment in free [Ca2+]i. Biophys J 47: 378a
Allen P, López JR, Sanchez V, Ryan JF, Sreter FA (1992) EU-4093 decreases cytosolic [Ca2+] in skeletal muscle from control and malignant hyperthermia-susceptible swine. Anesthesiology 76:132–138
Alvarez Leffmans FJ, Gamino SM, Giraldez F, Gonzalez-Serratos H (1986) Cytosolic free magnesium in frog skeletal muscle fibres measured with ion selective microelectrodes. J Physiol (Lond) 378:461–483
Berridge MJ (1993) Inositol trisphosphate and calcium signaling. Nature 361:315–325
Berridge MJ, Irvine RF (1989) Inositol phosphates and cell signaling. Nature 341:197–205
Bootman MD, Missiaen L, Parys JB, De Smedt H, Casteels R (1995) Control of inositol 1,4,5-trisphosphate-induced Ca2+ release by cytosolic Ca2+. Biochem J 306:445–451
Cleworth NF, Edman KA (1972) Changes in sarcomere length during isometric tension development in frog skeletal muscle. J Physiol (Lond) 227:1–17
Combettes L, Champeil P (1994) Calcium and inositol 1,4,5-trisphosphate-induced Ca2+ release. Science 265: 813–815
Combettes L, Hannaert-Merah Z, Coquil JF, Rosseau C, Claret M, Swillens S, Champeil P (1994) Rapid filtration studies of the effect of cytosolic Ca2+ on inositol 1,4,5-trisphosphate-induced 45Ca2+ release from cerebellar microsomes. J Biol Chem 269:17561–17571
Ehrlich BE, Watras J (1988) Inositol 1,4,5-trisphosphate activates a channel from smooth muscle sarcoplasmic reticulum. Nature 336:583–586
Endo M (1975) Conditions required for calcium-induced release of calcium from the sarcoplasmic reticulum. Proc Jpn Acad 51:479–484
Finch EA, Turner TJ, Goldin SM (1991) Calcium as a coagonist of inositol 1,4,5-trisphosphate-induced calcium release. Science 252:443–446
Ford LE, Podolsky RJ (1972) Cytosolic calcium movement in skinned muscle fibres. J Physiol (Lond) 223:21–33
Foster PS, Genisi E, Claudianos C, Hopkinson K, Denborough M (1989) Inositol 1,4,5-trisphosphate phosphatase deficiency and malignant hyperthermia in swine Lancet 2:124–127
Hannon JD, Lee N, Yandong C, Blinks J (1992) Inositol trisphosphate (InsP 3) causes contraction in skeletal muscle only under artificial conditions: evidence that Ca2+ release can result from depolarization of T-tubules. J Muscle Res Cell Motil 13:447–456
Hidalgo C, Jaimovich E (1989) Inositol trisphosphate and excitation contraction coupling in skeletal muscle. J Bioenerg Biomembr 21:267–281
Jean T, Klee CB (1986) Calcium modulation of inositol 1,4,5 trisphosphate-induced calcium release from neuroblastoma × glioma hybrid (NG 108-15) microsomes. J Biol Chem 261:16414–16420
Joseph SK, Rice HL (1989) The relation between inositol trisphosphate receptor density and calcium release in brain microsomes. Mol Pharmacol 35:355–359
Jovanovic A, López JR, Terzic A (1996) Cytosolic Ca2+ domain-dependent protective action of adenosine in cardiomyocytes. Eur J Pharmacol 298:63–69
Lea TJ, Griffiths PJ, Treager RT, Ashley CC (1986) An examination of the ability of inositol 1,4,5-trisphosphate to induce calcium release and tension development in skinned skeletal muscle fibers of frog and Crustacea. FEBS Lett 203:153–161
Lino M, Endo M (1992) Calcium-dependent immediate feedback control of inositol 1,4,5-trisphosphate-induced Ca2+ release. Nature 360:76–78
López JR, Parra L (1991) Inositol 1,4,5-trisphosphate increases myoplasmic [Ca2+]i in isolated muscle fibers. Depolarization enhances its effects. Cell Calcium 12:543–557
López JR, Wanek L, Taylor S (1981) Skeletal muscle: length-dependent effects of potentiating agents. Science 214:79–82
López JR, Allen P, Alamo L, Jone D, Sreter F (1988) Myoplasmic free [Ca2+] during a malignant hyperthermia episode in swine. Muscle Nerve 11:22–88
López JR, Gerardi A, López M, Allen P (1991) Effect of dantrolene on myoplasmic free [Ca2+] measured in vivo in patients susceptible to malignant hyperthermia. Anesthesiology 76:711–719
López JR, Pérez C, Alfonzo M, Cordovez G, Linares N, Allen P (1993) Changes in cytosolic Ca2+ concentration induced by inositol 1,4,5-trisphosphate in human malignant hyperthermia skeletal muscle. Life Sci 12:131–140
López JR, Jovanovic A, Terzic A (1995) Spontaneous calcium waves without contraction in cardiac myocytes. Biochem Biophys Res Commun 214:781–787
López JR, Rojas B, Gonzalez M, Terzic A (1995) Myoplasmic Ca2+ concentration during exertional rhabdomyolysis. Lancet 345:424–425
López JR, Linares N, Cordovez G, Terzic A (1995) Elevated myoplasmic calcium in exercise induced equine rhabdomyolysis. Pflügers Arch 430:293–295
López JR, Pérez C, Linares N, Allen P, Terzic A (1995) Hypersensitive response of malignant hyperthermia-susceptible skeletal muscle to inositol 1,4,5-trisphosphate induced release of calcium. Naunyn Schmiedebergs Arch Pharmacol 352: 442–446
Meissner G (1986) Ryanodine activation and inhibition of the Ca2+ release channel of sarcoplasmic reticulum. J Biol Chem 261:6300–6306
Meyer T, Stryer L (1990) Transient calcium release induced by successive increments of inositol 1,4,5-trisphosphate. Proc Natl Acad Sci USA 87:3841–3845
Miyamoto H, Racker E (1982) Mechanism of calcium release from skeletal muscle sarcoplasmic reticulum. J Memb Biol 66:193–201
Palade P, Dettbarn C, Alderson B, Volpe P (1989) Pharmacologic differentiation between inositol 1,4,5-trisphosphate-induced Ca2+ release and Ca2+ or caffeine-induced Ca2+ release from cytosolic membrane systems. Mol Pharmacol 36:673–680
Pape PC, Konishi M, Baylor S, Somlyo AP (1988) Excitation-contraction coupling in skeletal muscle fibers injected with the InsP 3 blocker heparin. FEBS Lett 253:57–62
Rojas C, Jaimovich E (1990) Calcium release modulated by inositol trisphosphate in ruptured fibers from frog skeletal muscle. Pflügers Archiv 416:296–304
Schneider MF, Chandler WK (1973) Voltage dependent charge movement in skeletal muscle: a possible step in excitation contraction coupling. Nature 242:244–246
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
Suárez Isla B, Alcayaga C, Marengo JJ, Bull R (1991) Activation of inositol trisphosphate-sensitive Ca2+ channels of sarcoplasmic reticulum from frog skeletal muscle. J Physiol (Lond) 441:575–591
Valdivia C, Vaughan D, Potter BV, Coronado R (1992) Fast release of 45Ca2+ induced by inositol 1,4,5-trisphosphate and Ca2+ in the sarcoplasmic reticulum of rabbit skeletal muscle: evidence for two types of Ca2+ release channels. Biophys J 61:1184–1193
Vergara J, Tsien R, Delay M (1985) Inositol 1,4,5-trisphosphate. A possible chemical link in excitation-contraction coupling in muscle. Proc Natl Acad Sci USA 82:6352–6356
Vilven J, Coronado R (1988) Opening of dihydropyridine calcium channels in skeletal muscle membranes by inositol trisphosphate. Nature 336:587–589.
Volpe P, Salviati G, De Virgillo F, Pozzan T (1985) Inositol 1,4,5 trisphosphate induced calcium release from sarcoplasmic reticulum. Nature 316:347–349
Walker JW, Somlyo AV, Goldman YE, Somlyo AP, Trenham DR (1987) Kinetics of smooth and skeletal muscle activation by laser pulse photolysis of caged inositol 1,4,5-trisphosphate. Nature 327:249–252
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López, J.R., Terzic, A. Inositol 1,4,5-trisphosphate-induced Ca2+ release is regulated by cytosolic Ca2+ in intact skeletal muscle. Pflügers Arch. 432, 782–790 (1996). https://doi.org/10.1007/s004240050199
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DOI: https://doi.org/10.1007/s004240050199