Skip to main content
NCBI home page
Biophysical Journal logoLink to Biophysical Journal
. 1998 Apr;74(4):1795–1807. doi: 10.1016/S0006-3495(98)77890-7

Effect of luminal calcium on Ca2+ release channel activity of sarcoplasmic reticulum in situ.

N Kurebayashi 1, Y Ogawa 1
PMCID: PMC1299524  PMID: 9545042

Abstract

Ca2+ influx into empty SR in the absence of Ca2+ pump activity was determined in skinned frog skeletal muscle fibers and compared with Ca2+ efflux from loaded SR (i.e., Ca2+ release) to deepen our understanding of the properties of the Ca2+ release channel (CRC). Calcium content in SR increased approximately in a first-order kinetics and finally reached the equilibrium level determined by cytoplasmic Ca2+ ([Ca2+]c). Because AMP caused an increase in the rate of Ca2+ influx, and procaine, Mg2+, and high concentrations of Ca2+ caused a characteristic decrease, the major Ca2+ influx pathway was concluded to be the CRC, as is true of Ca2+ release. The apparent rate constant (k(app)) of Ca2+ efflux did not significantly change when the loading level was decreased to one-third. At a given [Ca2+]c, the same equilibrium level of calcium in SR was attained with a similar k(app) by both Ca2+ influx and Ca2+ efflux. The relationship between [Ca2+]c and calcium in SR indicated the Ca2+ binding sites in SR. These results, together with the anticipated effects of these Ca2+ buffer sites on kinetics, are consistent with the idea that luminal Ca2+ inhibits the CRC.

Full Text

The Full Text of this article is available as a PDF (179.5 KB).

Selected References

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

  1. Baylor S. M., Chandler W. K., Marshall M. W. Sarcoplasmic reticulum calcium release in frog skeletal muscle fibres estimated from Arsenazo III calcium transients. J Physiol. 1983 Nov;344:625–666. doi: 10.1113/jphysiol.1983.sp014959. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Chen S. R., Zhang L., MacLennan D. H. Asymmetrical blockade of the Ca2+ release channel (ryanodine receptor) by 12-kDa FK506 binding protein. Proc Natl Acad Sci U S A. 1994 Dec 6;91(25):11953–11957. doi: 10.1073/pnas.91.25.11953. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Donoso P., Prieto H., Hidalgo C. Luminal calcium regulates calcium release in triads isolated from frog and rabbit skeletal muscle. Biophys J. 1995 Feb;68(2):507–515. doi: 10.1016/S0006-3495(95)80212-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Fill M., Coronado R., Mickelson J. R., Vilven J., Ma J. J., Jacobson B. A., Louis C. F. Abnormal ryanodine receptor channels in malignant hyperthermia. Biophys J. 1990 Mar;57(3):471–475. doi: 10.1016/S0006-3495(90)82563-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Harafuji H., Ogawa Y. Re-examination of the apparent binding constant of ethylene glycol bis(beta-aminoethyl ether)-N,N,N',N'-tetraacetic acid with calcium around neutral pH. J Biochem. 1980 May;87(5):1305–1312. doi: 10.1093/oxfordjournals.jbchem.a132868. [DOI] [PubMed] [Google Scholar]
  6. Ikemoto N., Antoniu B., Kang J. J., Mészáros L. G., Ronjat M. Intravesicular calcium transient during calcium release from sarcoplasmic reticulum. Biochemistry. 1991 May 28;30(21):5230–5237. doi: 10.1021/bi00235a017. [DOI] [PubMed] [Google Scholar]
  7. Ikemoto N., Bhatnager G. M., Gergely J. Fractionation of solubilized sarcoplasmic reticulum. Biochem Biophys Res Commun. 1971 Sep 17;44(6):1510–1517. doi: 10.1016/s0006-291x(71)80257-7. [DOI] [PubMed] [Google Scholar]
  8. Ikemoto N., Nagy B., Bhatnagar G. M., Gergely J. Studies on a metal-binding protein of the sarcoplasmic reticulum. J Biol Chem. 1974 Apr 25;249(8):2357–2365. [PubMed] [Google Scholar]
  9. Ikemoto N., Ronjat M., Mészáros L. G., Koshita M. Postulated role of calsequestrin in the regulation of calcium release from sarcoplasmic reticulum. Biochemistry. 1989 Aug 8;28(16):6764–6771. doi: 10.1021/bi00442a033. [DOI] [PubMed] [Google Scholar]
  10. Ikemoto N. Transport and inhibitory Ca2+ binding sites on the ATPase enzyme isolated from the sarcoplasmic reticulum. J Biol Chem. 1975 Sep 25;250(18):7219–7224. [PubMed] [Google Scholar]
  11. Kawasaki T., Kasai M. Regulation of calcium channel in sarcoplasmic reticulum by calsequestrin. Biochem Biophys Res Commun. 1994 Mar 30;199(3):1120–1127. doi: 10.1006/bbrc.1994.1347. [DOI] [PubMed] [Google Scholar]
  12. Kurebayashi N., Ogawa Y. Characterization of increased Ca2+ efflux by quercetin from the sarcoplasmic reticulum in frog skinned skeletal muscle fibres. J Muscle Res Cell Motil. 1986 Apr;7(2):142–150. doi: 10.1007/BF01753415. [DOI] [PubMed] [Google Scholar]
  13. Kurebayashi N., Ogawa Y. Discrimination of Ca(2+)-ATPase activity of the sarcoplasmic reticulum from actomyosin-type ATPase activity of myofibrils in skinned mammalian skeletal muscle fibres: distinct effects of cyclopiazonic acid on the two ATPase activities. J Muscle Res Cell Motil. 1991 Aug;12(4):355–365. doi: 10.1007/BF01738590. [DOI] [PubMed] [Google Scholar]
  14. Ma J., Bhat M. B., Zhao J. Rectification of skeletal muscle ryanodine receptor mediated by FK506 binding protein. Biophys J. 1995 Dec;69(6):2398–2404. doi: 10.1016/S0006-3495(95)80109-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. 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]
  16. MacLennan D. H., Wong P. T. Isolation of a calcium-sequestering protein from sarcoplasmic reticulum. Proc Natl Acad Sci U S A. 1971 Jun;68(6):1231–1235. doi: 10.1073/pnas.68.6.1231. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Meissner G., Darling E., Eveleth J. Kinetics of rapid Ca2+ release by sarcoplasmic reticulum. Effects of Ca2+, Mg2+, and adenine nucleotides. Biochemistry. 1986 Jan 14;25(1):236–244. doi: 10.1021/bi00349a033. [DOI] [PubMed] [Google Scholar]
  18. Meissner G., Rios E., Tripathy A., Pasek D. A. Regulation of skeletal muscle Ca2+ release channel (ryanodine receptor) by Ca2+ and monovalent cations and anions. J Biol Chem. 1997 Jan 17;272(3):1628–1638. doi: 10.1074/jbc.272.3.1628. [DOI] [PubMed] [Google Scholar]
  19. Miyamoto H., Kasai M. Asymmetric distribution of calcium binding sites of sarcoplasmic reticulum fragments. J Biochem. 1979 Mar;85(3):765–773. [PubMed] [Google Scholar]
  20. Murayama T., Kurebayashi N., Ogawa Y. Stimulation by polyols of the two ryanodine receptor isoforms of frog skeletal muscle. J Muscle Res Cell Motil. 1998 Jan;19(1):15–24. doi: 10.1023/a:1005344108908. [DOI] [PubMed] [Google Scholar]
  21. Murayama T., Ogawa Y. Similar Ca2+ dependences of [3H]ryanodine binding to alpha- and beta-ryanodine receptors purified from bullfrog skeletal muscle in an isotonic medium. FEBS Lett. 1996 Feb 19;380(3):267–271. doi: 10.1016/0014-5793(96)00053-1. [DOI] [PubMed] [Google Scholar]
  22. Ogawa Y., Harafuji H. Effect of temperature on [3H]ryanodine binding to sarcoplasmic reticulum from bullfrog skeletal muscle. J Biochem. 1990 Jun;107(6):887–893. doi: 10.1093/oxfordjournals.jbchem.a123143. [DOI] [PubMed] [Google Scholar]
  23. Ogawa Y. Some properties of fragmented frog sarcoplasmic reticulum with particular reference to its response to caffeine. J Biochem. 1970 May;67(5):667–683. doi: 10.1093/oxfordjournals.jbchem.a129295. [DOI] [PubMed] [Google Scholar]
  24. Owen V. J., Lamb G. D., Stephenson D. G., Fryer M. W. Relationship between depolarization-induced force responses and Ca2+ content in skeletal muscle fibres of rat and toad. J Physiol. 1997 Feb 1;498(Pt 3):571–586. doi: 10.1113/jphysiol.1997.sp021884. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Pape P. C., Jong D. S., Chandler W. K. Calcium release and its voltage dependence in frog cut muscle fibers equilibrated with 20 mM EGTA. J Gen Physiol. 1995 Aug;106(2):259–336. doi: 10.1085/jgp.106.2.259. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Philipson K. D., Bers D. M., Nishimoto A. Y. The role of phospholipids in the Ca2+ binding of isolated cardiac sarcolemma. J Mol Cell Cardiol. 1980 Nov;12(11):1159–1173. doi: 10.1016/0022-2828(80)90063-2. [DOI] [PubMed] [Google Scholar]
  27. Shirokova N., García J., Pizarro G., Ríos E. Ca2+ release from the sarcoplasmic reticulum compared in amphibian and mammalian skeletal muscle. J Gen Physiol. 1996 Jan;107(1):1–18. doi: 10.1085/jgp.107.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Sitsapesan R., Williams A. J. The gating of the sheep skeletal sarcoplasmic reticulum Ca(2+)-release channel is regulated by luminal Ca2+. J Membr Biol. 1995 Jul;146(2):133–144. doi: 10.1007/BF00238004. [DOI] [PubMed] [Google Scholar]
  29. 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]
  30. 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]
  31. Somlyo A. V., Gonzalez-Serratos H. G., Shuman H., McClellan G., Somlyo A. P. Calcium release and ionic changes in the sarcoplasmic reticulum of tetanized muscle: an electron-probe study. J Cell Biol. 1981 Sep;90(3):577–594. doi: 10.1083/jcb.90.3.577. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Tinker A., Williams A. J. Divalent cation conduction in the ryanodine receptor channel of sheep cardiac muscle sarcoplasmic reticulum. J Gen Physiol. 1992 Sep;100(3):479–493. doi: 10.1085/jgp.100.3.479. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Tripathy A., Meissner G. Sarcoplasmic reticulum lumenal Ca2+ has access to cytosolic activation and inactivation sites of skeletal muscle Ca2+ release channel. Biophys J. 1996 Jun;70(6):2600–2615. doi: 10.1016/S0006-3495(96)79831-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Volpe P., Simon B. J. The bulk of Ca2+ released to the myoplasm is free in the sarcoplasmic reticulum and does not unbind from calsequestrin. FEBS Lett. 1991 Jan 28;278(2):274–278. doi: 10.1016/0014-5793(91)80134-o. [DOI] [PubMed] [Google Scholar]

Articles from Biophysical Journal are provided here courtesy of The Biophysical Society

RESOURCES