Characterization of high-affinity ryanodine-binding sites of rat liver endoplasmic reticulum. Differences between liver and skeletal muscle (original) (raw)

Abstract

In this study, the binding of [3H]ryanodine to liver microsomal subfractions was investigated. The specific binding of [3H]ryanodine, as determined both by vacuum filtration and by ultracentrifugation, is to a single class of high-affinity binding sites with a Kd of 10 +/- 2.5 nM and density of 500 +/- 100 and 1200 +/- 200 fmol/mg of protein by the filtration and centrifugation methods respectively. [3H]Ryanodine binding reached equilibrium in about 1 min and 2 min at 36 degrees C and 24 degrees C respectively, and the half-time of dissociation at 37 degrees C was approx. 15 s. The binding of [3H]ryanodine is Ca(2+)-independent: it is slightly stimulated by NaCl, Mg2+, ATP and InsP3 but strongly inhibited by caffeine, diltiazem and sodium dantrolene. Thus the binding of ryanodine to endoplasmic reticulum membranes shares some of the characteristics of its binding to the sarcoplasmic reticulum but also differs from it in several important properties, such as its Ca(2+)-independence, its rapid association and dissociation, and its inhibition by caffeine. The structural similarities between the skeletal muscle and liver binding sites were further explored by employing in vitro DNA amplification techniques, using the known sequence of the skeletal muscle receptor as reference point. The data obtained with this method indicate that the liver does not process mRNA for the skeletal muscle ryanodine receptor.

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  1. Ashley R. H. Activation and conductance properties of ryanodine-sensitive calcium channels from brain microsomal membranes incorporated into planar lipid bilayers. J Membr Biol. 1989 Oct;111(2):179–189. doi: 10.1007/BF01871781. [DOI] [PubMed] [Google Scholar]
  2. Berridge M. J., Irvine R. F. Inositol phosphates and cell signalling. Nature. 1989 Sep 21;341(6239):197–205. doi: 10.1038/341197a0. [DOI] [PubMed] [Google Scholar]
  3. Campbell K. P., Shamoo A. E. Chloride-induced release of actively loaded calcium from light and heavy sarcoplasmic reticulum vesicles. J Membr Biol. 1980;54(1):73–80. doi: 10.1007/BF01875378. [DOI] [PubMed] [Google Scholar]
  4. Danko S., Kim D. H., Sreter F. A., Ikemoto N. Inhibitors of Ca2+ release from the isolated sarcoplasmic reticulum. II. The effects of dantrolene on Ca2+ release induced by caffeine, Ca2+ and depolarization. Biochim Biophys Acta. 1985 Jun 11;816(1):18–24. doi: 10.1016/0005-2736(85)90388-8. [DOI] [PubMed] [Google Scholar]
  5. Dawson A. P., Hills G., Comerford J. G. The mechanism of action of GTP on Ca2+ efflux from rat liver microsomal vesicles. Biochem J. 1987 May 15;244(1):87–92. doi: 10.1042/bj2440087. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Depierre J. W., Dallner G. Structural aspects of the membrane of the endoplasmic reticulum. Biochim Biophys Acta. 1975 Dec 29;415(4):411–472. doi: 10.1016/0304-4157(75)90006-4. [DOI] [PubMed] [Google Scholar]
  7. Fleischer S., Inui M. Biochemistry and biophysics of excitation-contraction coupling. Annu Rev Biophys Biophys Chem. 1989;18:333–364. doi: 10.1146/annurev.bb.18.060189.002001. [DOI] [PubMed] [Google Scholar]
  8. Fleischer S., Ogunbunmi E. M., Dixon M. C., Fleer E. A. Localization of Ca2+ release channels with ryanodine in junctional terminal cisternae of sarcoplasmic reticulum of fast skeletal muscle. Proc Natl Acad Sci U S A. 1985 Nov;82(21):7256–7259. doi: 10.1073/pnas.82.21.7256. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Fleschner C. R., Kraus-Friedmann N. The effect of Mg2+ on hepatic microsomal Ca2+ and Sr2+ transport. Eur J Biochem. 1986 Jan 15;154(2):313–320. doi: 10.1111/j.1432-1033.1986.tb09399.x. [DOI] [PubMed] [Google Scholar]
  10. Foster P. S., Denborough M. A. Effect of diltiazem and dantrolene on the contractility of isolated malignant hyperpyrexia-susceptible porcine skeletal muscle. Br J Anaesth. 1989 May;62(5):566–572. doi: 10.1093/bja/62.5.566. [DOI] [PubMed] [Google Scholar]
  11. Foster P. S., Hopkinson K. C., Denborough M. A. Effect of diltiazem, verapamil and dantrolene on the contractility of isolated malignant hyperpyrexia-susceptible human skeletal muscle. Clin Exp Pharmacol Physiol. 1989 Oct;16(10):799–805. doi: 10.1111/j.1440-1681.1989.tb01518.x. [DOI] [PubMed] [Google Scholar]
  12. Gibbs R. A., Nguyen P. N., McBride L. J., Koepf S. M., Caskey C. T. Identification of mutations leading to the Lesch-Nyhan syndrome by automated direct DNA sequencing of in vitro amplified cDNA. Proc Natl Acad Sci U S A. 1989 Mar;86(6):1919–1923. doi: 10.1073/pnas.86.6.1919. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hymel L., Inui M., Fleischer S., Schindler H. Purified ryanodine receptor of skeletal muscle sarcoplasmic reticulum forms Ca2+-activated oligomeric Ca2+ channels in planar bilayers. Proc Natl Acad Sci U S A. 1988 Jan;85(2):441–445. doi: 10.1073/pnas.85.2.441. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Inui M., Saito A., Fleischer S. Purification of the ryanodine receptor and identity with feet structures of junctional terminal cisternae of sarcoplasmic reticulum from fast skeletal muscle. J Biol Chem. 1987 Feb 5;262(4):1740–1747. [PubMed] [Google Scholar]
  15. Kimura S., Higham S., Robison B. C., Kraus-Friedmann N. Mechanism of action of GTP in the induction of Ca2+ release from hepatic microsomes. J Biochem. 1990 Apr;107(4):550–553. doi: 10.1093/oxfordjournals.jbchem.a123084. [DOI] [PubMed] [Google Scholar]
  16. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  17. 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]
  18. Lai F. A., Meissner G. The muscle ryanodine receptor and its intrinsic Ca2+ channel activity. J Bioenerg Biomembr. 1989 Apr;21(2):227–246. doi: 10.1007/BF00812070. [DOI] [PubMed] [Google Scholar]
  19. Lai F. A., Misra M., Xu L., Smith H. A., Meissner G. The ryanodine receptor-Ca2+ release channel complex of skeletal muscle sarcoplasmic reticulum. Evidence for a cooperatively coupled, negatively charged homotetramer. J Biol Chem. 1989 Oct 5;264(28):16776–16785. [PubMed] [Google Scholar]
  20. Lattanzio F. A., Jr, Schlatterer R. G., Nicar M., Campbell K. P., Sutko J. L. The effects of ryanodine on passive calcium fluxes across sarcoplasmic reticulum membranes. J Biol Chem. 1987 Feb 25;262(6):2711–2718. [PubMed] [Google Scholar]
  21. Meissner G. Ryanodine activation and inhibition of the Ca2+ release channel of sarcoplasmic reticulum. J Biol Chem. 1986 May 15;261(14):6300–6306. [PubMed] [Google Scholar]
  22. Michalak M., Dupraz P., Shoshan-Barmatz V. Ryanodine binding to sarcoplasmic reticulum membrane; comparison between cardiac and skeletal muscle. Biochim Biophys Acta. 1988 Apr 22;939(3):587–594. doi: 10.1016/0005-2736(88)90106-x. [DOI] [PubMed] [Google Scholar]
  23. Moldéus P., Högberg J., Orrenius S. Isolation and use of liver cells. Methods Enzymol. 1978;52:60–71. doi: 10.1016/s0076-6879(78)52006-5. [DOI] [PubMed] [Google Scholar]
  24. Ohnishi S. T., Taylor S., Gronert G. A. Calcium-induced Ca2+ release from sarcoplasmic reticulum of pigs susceptible to malignant hyperthermia. The effects of halothane and dantrolene. FEBS Lett. 1983 Sep 5;161(1):103–107. doi: 10.1016/0014-5793(83)80739-x. [DOI] [PubMed] [Google Scholar]
  25. Otsu K., Willard H. F., Khanna V. K., Zorzato F., Green N. M., MacLennan D. H. Molecular cloning of cDNA encoding the Ca2+ release channel (ryanodine receptor) of rabbit cardiac muscle sarcoplasmic reticulum. J Biol Chem. 1990 Aug 15;265(23):13472–13483. [PubMed] [Google Scholar]
  26. Pessah I. N., Francini A. O., Scales D. J., Waterhouse A. L., Casida J. E. Calcium-ryanodine receptor complex. Solubilization and partial characterization from skeletal muscle junctional sarcoplasmic reticulum vesicles. J Biol Chem. 1986 Jul 5;261(19):8643–8648. [PubMed] [Google Scholar]
  27. Pessah I. N., Stambuk R. A., Casida J. E. Ca2+-activated ryanodine binding: mechanisms of sensitivity and intensity modulation by Mg2+, caffeine, and adenine nucleotides. Mol Pharmacol. 1987 Mar;31(3):232–238. [PubMed] [Google Scholar]
  28. Saito A., Seiler S., Chu A., Fleischer S. Preparation and morphology of sarcoplasmic reticulum terminal cisternae from rabbit skeletal muscle. J Cell Biol. 1984 Sep;99(3):875–885. doi: 10.1083/jcb.99.3.875. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Shoshan-Barmatz V. High affinity ryanodine binding sites in rat liver endoplasmic reticulum. FEBS Lett. 1990 Apr 24;263(2):317–320. doi: 10.1016/0014-5793(90)81403-b. [DOI] [PubMed] [Google Scholar]
  30. Shoshan-Barmatz V., Zarka A. Trypsin destruction of the high affinity ryanodine binding sites of the junctional sarcoplasmic reticulum. J Biol Chem. 1988 Nov 15;263(32):16772–16779. [PubMed] [Google Scholar]
  31. Shoshan-Barmatz V., Zhang G. H., Garretson L., Kraus-Friedmann N. Distinct ryanodine- and inositol 1,4,5-trisphosphate-binding sites in hepatic microsomes. Biochem J. 1990 Jun 15;268(3):699–705. doi: 10.1042/bj2680699. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. 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]
  33. Smith P. K., Krohn R. I., Hermanson G. T., Mallia A. K., Gartner F. H., Provenzano M. D., Fujimoto E. K., Goeke N. M., Olson B. J., Klenk D. C. Measurement of protein using bicinchoninic acid. Anal Biochem. 1985 Oct;150(1):76–85. doi: 10.1016/0003-2697(85)90442-7. [DOI] [PubMed] [Google Scholar]
  34. 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]
  35. Webb W. W., Anders M. W. Coupling of ATP synthesis to reversal of rat liver microsomal Ca2+-ATPase. Biochemistry. 1985 Dec 17;24(26):7741–7745. doi: 10.1021/bi00347a036. [DOI] [PubMed] [Google Scholar]
  36. Zhang G. H., Yamaguchi M., Kimura S., Higham S., Kraus-Friedmann N. Effects of heavy metal on rat liver microsomal Ca2(+)-ATPase and Ca2+ sequestering. Relation to SH groups. J Biol Chem. 1990 Feb 5;265(4):2184–2189. [PubMed] [Google Scholar]