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. 1990 Jun;57(6):1233–1243. doi: 10.1016/S0006-3495(90)82642-4

Ca2+ release by inositol-trisphosphorothioate in isolated triads of rabbit skeletal muscle.

C Valdivia 1, H H Valdivia 1, B V Potter 1, R Coronado 1
PMCID: PMC1280833  PMID: 2168221

Abstract

The effectiveness of the nonmetabolizable second messenger analogue DL-myo-inositol 1,4,5-trisphosphorothioate (IPS3) described by Cooke, A. M., R. Gigg, and B. V. L. Potter, (1987b. Jour. Chem. Soc. Chem. Commun. 1525-1526.) was examined in triads purified from rabbit skeletal muscle. A Ca2+ electrode uptake-release assay was used to determine the size and sensitivity of the IPS3-releasable pool of Ca2+ in isolated triads. Uptake was initiated by 1 mM MgATP, pCa 5.8, pH 7.5 Release was initiated when the free Ca2+ had lowered to pCa approximately 7. We found that 5-25 microM myo-inositol 1,4,5-trisphosphate (IP3), and separately IPS3, consistently released 5-20% of the Ca2+ pool actively loaded into triads. Single channel recording was used to determine if ryanodine receptor Ca2+ release channels were affected by IPS3 at the same myoplasmic Ca2+ and IPS3 concentrations. Open probability of ryanodine receptor Ca2+ release channels was monitored in triads fused to bilayers over long periods (200 s) in the absence and following addition of 30 microM IPS3 to the same channel. At myoplasmic pCa approximately 7, IPS3 had no effect in the absence of MgATP (Po = 0.0094 +/- 0.001 in control and Po = 0.01 +/- 0.006 after IPS3) and slightly increased activity in the presence of 1 mM MgATP (Po = 0.024 +/- 0.03 in control and Po = 0.05 +/- 0.03 after IPS3). Equally small effects were observed at higher myoplasmic Ca2+. The onset of channel activation by IPS3 or IP3 was slow, on the time scale 20-60 s. We suggest that in isolated triads of rabbit skeletal muscle, IP3-induced release of stored Ca2+ is probably not mediated by the opening of Ca2+ release channels.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Block B. A., Imagawa T., Campbell K. P., Franzini-Armstrong C. Structural evidence for direct interaction between the molecular components of the transverse tubule/sarcoplasmic reticulum junction in skeletal muscle. J Cell Biol. 1988 Dec;107(6 Pt 2):2587–2600. doi: 10.1083/jcb.107.6.2587. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Caswell A. H., Lau Y. H., Garcia M., Brunschwig J. P. Recognition and junction formation by isolated transverse tubules and terminal cisternae of skeletal muscle. J Biol Chem. 1979 Jan 10;254(1):202–208. [PubMed] [Google Scholar]
  3. Chadwick C. C., Inui M., Fleischer S. Identification and purification of a transverse tubule coupling protein which binds to the ryanodine receptor of terminal cisternae at the triad junction in skeletal muscle. J Biol Chem. 1988 Aug 5;263(22):10872–10877. [PubMed] [Google Scholar]
  4. Coronado R., Smith J. S. Monovalent ion current through single calcium channels of skeletal muscle transverse tubules. Biophys J. 1987 Mar;51(3):497–502. doi: 10.1016/S0006-3495(87)83371-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Donaldson S. K., Goldberg N. D., Walseth T. F., Huetteman D. A. Inositol trisphosphate stimulates calcium release from peeled skeletal muscle fibers. Biochim Biophys Acta. 1987 Jan 19;927(1):92–99. doi: 10.1016/0167-4889(87)90070-x. [DOI] [PubMed] [Google Scholar]
  6. Ehrlich B. E., Watras J. Inositol 1,4,5-trisphosphate activates a channel from smooth muscle sarcoplasmic reticulum. Nature. 1988 Dec 8;336(6199):583–586. doi: 10.1038/336583a0. [DOI] [PubMed] [Google Scholar]
  7. Fabiato A., Fabiato F. Effects of pH on the myofilaments and the sarcoplasmic reticulum of skinned cells from cardiace and skeletal muscles. J Physiol. 1978 Mar;276:233–255. doi: 10.1113/jphysiol.1978.sp012231. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. 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. 1989 Nov 2;342(6245):32–38. doi: 10.1038/342032a0. [DOI] [PubMed] [Google Scholar]
  9. Hamblin M. R., Flora J. S., Potter B. V. myo-Inositol phosphorothioates, phosphatase-resistant analogues of myo-inositol phosphates. Synthesis of DL-myo-inositol 1,4-bisphosphate and DL-myo-inositol 1,4-bisphosphorothioate. Biochem J. 1987 Sep 15;246(3):771–774. doi: 10.1042/bj2460771. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Hasselbach W., Oetliker H. Energetics and electrogenicity of the sarcoplasmic reticulum calcium pump. Annu Rev Physiol. 1983;45:325–339. doi: 10.1146/annurev.ph.45.030183.001545. [DOI] [PubMed] [Google Scholar]
  11. Hidalgo C., Carrasco M. A., Magendzo K., Jaimovich E. Phosphorylation of phosphatidylinositol by transverse tubule vesicles and its possible role in excitation-contraction coupling. FEBS Lett. 1986 Jun 23;202(1):69–73. doi: 10.1016/0014-5793(86)80651-2. [DOI] [PubMed] [Google Scholar]
  12. Ikemoto N., Antoniu B., Kim D. H. Rapid calcium release from the isolated sarcoplasmic reticulum is triggered via the attached transverse tubular system. J Biol Chem. 1984 Nov 10;259(21):13151–13158. [PubMed] [Google Scholar]
  13. Imagawa T., Smith J. S., Coronado R., Campbell K. P. Purified ryanodine receptor from skeletal muscle sarcoplasmic reticulum is the Ca2+-permeable pore of the calcium release channel. J Biol Chem. 1987 Dec 5;262(34):16636–16643. [PubMed] [Google Scholar]
  14. Lai F. A., Erickson H. P., Rousseau E., Liu Q. Y., Meissner G. Purification and reconstitution of the calcium release channel from skeletal muscle. Nature. 1988 Jan 28;331(6154):315–319. doi: 10.1038/331315a0. [DOI] [PubMed] [Google Scholar]
  15. Lea T. J., Griffiths P. J., Tregear R. T., Ashley C. C. An examination of the ability of inositol 1,4,5-trisphosphate to induce calcium release and tension development in skinned skeletal muscle fibres of frog and crustacea. FEBS Lett. 1986 Oct 20;207(1):153–161. doi: 10.1016/0014-5793(86)80031-x. [DOI] [PubMed] [Google Scholar]
  16. Ma J., Coronado R. Heterogeneity of conductance states in calcium channels of skeletal muscle. Biophys J. 1988 Mar;53(3):387–395. doi: 10.1016/S0006-3495(88)83115-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Ma J., Fill M., Knudson C. M., Campbell K. P., Coronado R. Ryanodine receptor of skeletal muscle is a gap junction-type channel. Science. 1988 Oct 7;242(4875):99–102. doi: 10.1126/science.2459777. [DOI] [PubMed] [Google Scholar]
  18. Martonosi A. N. Mechanisms of Ca2+ release from sarcoplasmic reticulum of skeletal muscle. Physiol Rev. 1984 Oct;64(4):1240–1320. doi: 10.1152/physrev.1984.64.4.1240. [DOI] [PubMed] [Google Scholar]
  19. Meissner G. Evidence of a role for calmodulin in the regulation of calcium release from skeletal muscle sarcoplasmic reticulum. Biochemistry. 1986 Jan 14;25(1):244–251. doi: 10.1021/bi00349a034. [DOI] [PubMed] [Google Scholar]
  20. Mikos G. J., Snow T. R. Failure of inositol 1,4,5-trisphosphate to elicit or potentiate Ca2+ release from isolated skeletal muscle sarcoplasmic reticulum. Biochim Biophys Acta. 1987 Feb 18;927(2):256–260. doi: 10.1016/0167-4889(87)90142-x. [DOI] [PubMed] [Google Scholar]
  21. Mitchell R. D., Palade P., Fleischer S. Purification of morphologically intact triad structures from skeletal muscle. J Cell Biol. 1983 Apr;96(4):1008–1016. doi: 10.1083/jcb.96.4.1008. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Miyamoto H., Racker E. Mechanism of calcium release from skeletal sarcoplasmic reticulum. J Membr Biol. 1982;66(3):193–201. doi: 10.1007/BF01868494. [DOI] [PubMed] [Google Scholar]
  23. Movsesian M. A., Thomas A. P., Selak M., Williamson J. R. Inositol trisphosphate does not release Ca2+ from permeabilized cardiac myocytes and sarcoplasmic reticulum. FEBS Lett. 1985 Jun 17;185(2):328–332. doi: 10.1016/0014-5793(85)80932-7. [DOI] [PubMed] [Google Scholar]
  24. Nahorski S. R., Potter B. V. Molecular recognition of inositol polyphosphates by intracellular receptors and metabolic enzymes. Trends Pharmacol Sci. 1989 Apr;10(4):139–144. doi: 10.1016/0165-6147(89)90165-x. [DOI] [PubMed] [Google Scholar]
  25. Palade P. Drug-induced Ca2+ release from isolated sarcoplasmic reticulum. III. Block of Ca2+-induced Ca2+ release by organic polyamines. J Biol Chem. 1987 May 5;262(13):6149–6154. [PubMed] [Google Scholar]
  26. Pape P. C., Konishi M., Baylor S. M., Somlyo A. P. Excitation-contraction coupling in skeletal muscle fibers injected with the InsP3 blocker, heparin. FEBS Lett. 1988 Aug 1;235(1-2):57–62. doi: 10.1016/0014-5793(88)81233-x. [DOI] [PubMed] [Google Scholar]
  27. Penner R., Neher E., Takeshima H., Nishimura S., Numa S. Functional expression of the calcium release channel from skeletal muscle ryanodine receptor cDNA. FEBS Lett. 1989 Dec 18;259(1):217–221. doi: 10.1016/0014-5793(89)81532-7. [DOI] [PubMed] [Google Scholar]
  28. Rojas E., Nassar-Gentina V., Luxoro M., Pollard M. E., Carrasco M. A. Inositol 1,4,5-trisphosphate-induced Ca2+ release from the sarcoplasmic reticulum and contraction in crustacean muscle. Can J Physiol Pharmacol. 1987 Apr;65(4):672–680. doi: 10.1139/y87-111. [DOI] [PubMed] [Google Scholar]
  29. Scherer N. M., Ferguson J. E. Inositol 1,4,5-trisphosphate is not effective in releasing calcium from skeletal sarcoplasmic reticulum microsomes. Biochem Biophys Res Commun. 1985 May 16;128(3):1064–1070. doi: 10.1016/0006-291x(85)91048-4. [DOI] [PubMed] [Google Scholar]
  30. Smith J. S., Coronado R., Meissner G. Sarcoplasmic reticulum contains adenine nucleotide-activated calcium channels. Nature. 1985 Aug 1;316(6027):446–449. doi: 10.1038/316446a0. [DOI] [PubMed] [Google Scholar]
  31. Smith J. S., Coronado R., Meissner G. Single channel measurements of the calcium release channel from skeletal muscle sarcoplasmic reticulum. Activation by Ca2+ and ATP and modulation by Mg2+. J Gen Physiol. 1986 Nov;88(5):573–588. doi: 10.1085/jgp.88.5.573. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Smith J. S., Coronado R., Meissner G. Single-channel calcium and barium currents of large and small conductance from sarcoplasmic reticulum. Biophys J. 1986 Nov;50(5):921–928. doi: 10.1016/S0006-3495(86)83533-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. 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. 1988 Jul;92(1):1–26. doi: 10.1085/jgp.92.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Somlyo A. P., Walker J. W., Goldman Y. E., Trentham D. R., Kobayashi S., Kitazawa T., Somlyo A. V. Inositol trisphosphate, calcium and muscle contraction. Philos Trans R Soc Lond B Biol Sci. 1988 Jul 26;320(1199):399–414. doi: 10.1098/rstb.1988.0084. [DOI] [PubMed] [Google Scholar]
  35. Strupish J., Cooke A. M., Potter B. V., Gigg R., Nahorski S. R. Stereospecific mobilization of intracellular Ca2+ by inositol 1,4,5-triphosphate. Comparison with inositol 1,4,5-trisphosphorothioate and inositol 1,3,4-trisphosphate. Biochem J. 1988 Aug 1;253(3):901–905. doi: 10.1042/bj2530901. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Supattapone S., Worley P. F., Baraban J. M., Snyder S. H. Solubilization, purification, and characterization of an inositol trisphosphate receptor. J Biol Chem. 1988 Jan 25;263(3):1530–1534. [PubMed] [Google Scholar]
  37. Suárez-Isla B. A., Irribarra V., Oberhauser A., Larralde L., Bull R., Hidalgo C., Jaimovich E. Inositol (1,4,5)-trisphosphate activates a calcium channel in isolated sarcoplasmic reticulum membranes. Biophys J. 1988 Oct;54(4):737–741. doi: 10.1016/S0006-3495(88)83009-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Takeshima H., Nishimura S., Matsumoto T., Ishida H., Kangawa K., Minamino N., Matsuo H., Ueda M., Hanaoka M., Hirose T. Primary structure and expression from complementary DNA of skeletal muscle ryanodine receptor. Nature. 1989 Jun 8;339(6224):439–445. doi: 10.1038/339439a0. [DOI] [PubMed] [Google Scholar]
  39. Taylor C. W., Berridge M. J., Brown K. D., Cooke A. M., Potter B. V. DL-myo-inositol 1,4,5-trisphosphorothioate mobilizes intracellular calcium in Swiss 3T3 cells and Xenopus oocytes. Biochem Biophys Res Commun. 1988 Jan 29;150(2):626–632. doi: 10.1016/0006-291x(88)90438-x. [DOI] [PubMed] [Google Scholar]
  40. Taylor C. W., Berridge M. J., Cooke A. M., Potter B. V. Inositol 1,4,5-trisphosphorothioate, a stable analogue of inositol trisphosphate which mobilizes intracellular calcium. Biochem J. 1989 May 1;259(3):645–650. doi: 10.1042/bj2590645. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Vergara J., Tsien R. Y., Delay M. Inositol 1,4,5-trisphosphate: a possible chemical link in excitation-contraction coupling in muscle. Proc Natl Acad Sci U S A. 1985 Sep;82(18):6352–6356. doi: 10.1073/pnas.82.18.6352. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Volpe P., Salviati G., Di Virgilio F., Pozzan T. Inositol 1,4,5-trisphosphate induces calcium release from sarcoplasmic reticulum of skeletal muscle. Nature. 1985 Jul 25;316(6026):347–349. doi: 10.1038/316347a0. [DOI] [PubMed] [Google Scholar]
  43. 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. 1989 Mar 9;338(6211):167–170. doi: 10.1038/338167a0. [DOI] [PubMed] [Google Scholar]
  44. Walker J. W., Somlyo A. V., Goldman Y. E., Somlyo A. P., Trentham D. R. Kinetics of smooth and skeletal muscle activation by laser pulse photolysis of caged inositol 1,4,5-trisphosphate. Nature. 1987 May 21;327(6119):249–252. doi: 10.1038/327249a0. [DOI] [PubMed] [Google Scholar]
  45. Watras J., Benevolensky D., Childs C. Calcium release from aortic sarcoplasmic reticulum. J Mol Cell Cardiol. 1989 Feb;21 (Suppl 1):125–130. doi: 10.1016/0022-2828(89)90847-x. [DOI] [PubMed] [Google Scholar]
  46. Willcocks A. L., Potter B. V., Cooke A. M., Nahorski S. R. Myo-inositol(1,4,5)trisphosphorothioate binds to specific [3H]inositol(1,4,5)trisphosphate sites in rat cerebellum and is resistant to 5-phosphatase. Eur J Pharmacol. 1988 Oct 11;155(1-2):181–183. doi: 10.1016/0014-2999(88)90420-7. [DOI] [PubMed] [Google Scholar]
  47. Worley P. F., Baraban J. M., Supattapone S., Wilson V. S., Snyder S. H. Characterization of inositol trisphosphate receptor binding in brain. Regulation by pH and calcium. J Biol Chem. 1987 Sep 5;262(25):12132–12136. [PubMed] [Google Scholar]

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