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. 1993 Apr;64(4):991–1003. doi: 10.1016/S0006-3495(93)81465-6

Procaine effects on single sarcoplasmic reticulum Ca2+ release channels.

A Zahradníková 1, P Palade 1
PMCID: PMC1262417  PMID: 8388270

Abstract

The effects of the Ca(2+)-induced Ca2+ release blocker procaine on individual sarcoplasmic reticulum Ca2+ release channels have been examined in planar lipid bilayers. Procaine did not reduce the single channel conductance nor appreciably shorten the mean open times of the channel; rather, it increased the longest closed time. These results indicated that procaine interacted selectively with a closed state of the channel rather than with an open state. Gating of the sarcoplasmic reticulum Ca2+ release channel was described by a modified scheme of Ashley and Williams (1990. J. Gen. Physiol. 95:981-1005), including an additional long-lived closed state. Computer simulations determined that procaine was more likely to interact with this long-lived Ca(2+)-bound closed state of the channel rather than with other states of the channel. Simulations with the same model were also able to reproduce a prominent Ca(2+)-sensitive transition between "random" and "bursting" forms of gating of the channel, variations of which may account for "gearshift" behavior reported in studies with this and other single channels.

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Selected References

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  1. Almers W., McCleskey E. W., Palade P. T. A non-selective cation conductance in frog muscle membrane blocked by micromolar external calcium ions. J Physiol. 1984 Aug;353:565–583. doi: 10.1113/jphysiol.1984.sp015351. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Anderson K., Lai F. A., Liu Q. Y., Rousseau E., Erickson H. P., Meissner G. Structural and functional characterization of the purified cardiac ryanodine receptor-Ca2+ release channel complex. J Biol Chem. 1989 Jan 15;264(2):1329–1335. [PubMed] [Google Scholar]
  3. Antoniu B., Kim D. H., Morii M., Ikemoto N. Inhibitors of Ca2+ release from the isolated sarcoplasmic reticulum. I. Ca2+ channel blockers. Biochim Biophys Acta. 1985 Jun 11;816(1):9–17. doi: 10.1016/0005-2736(85)90387-6. [DOI] [PubMed] [Google Scholar]
  4. Ashley R. H., Williams A. J. Divalent cation activation and inhibition of single calcium release channels from sheep cardiac sarcoplasmic reticulum. J Gen Physiol. 1990 May;95(5):981–1005. doi: 10.1085/jgp.95.5.981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Baylor S. M., Hollingworth S., Marshall M. W. Effects of intracellular ruthenium red on excitation-contraction coupling in intact frog skeletal muscle fibres. J Physiol. 1989 Jan;408:617–635. doi: 10.1113/jphysiol.1989.sp017480. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bianchi C. P., Bolton T. C. Action of local anesthetics on coupling systems in muscle. J Pharmacol Exp Ther. 1967 Aug;157(2):388–405. [PubMed] [Google Scholar]
  7. Bianchi C. P. Pharmacological actions on excitation-contraction coupling in striated muscle. Fed Proc. 1968 Jan-Feb;27(1):126–131. [PubMed] [Google Scholar]
  8. 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]
  9. Brunder D. G., Györke S., Dettbarn C., Palade P. Involvement of sarcoplasmic reticulum 'Ca2+ release channels' in excitation-contraction coupling in vertebrate skeletal muscle. J Physiol. 1992 Jan;445:759–778. doi: 10.1113/jphysiol.1992.sp018949. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Bull R., Marengo J. J., Suárez-Isla B. A., Donoso P., Sutko J. L., Hidalgo C. Activation of calcium channels in sarcoplasmic reticulum from frog muscle by nanomolar concentrations of ryanodine. Biophys J. 1989 Oct;56(4):749–756. doi: 10.1016/S0006-3495(89)82722-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Chamberlain B. K., Volpe P., Fleischer S. Inhibition of calcium-induced calcium release from purified cardiac sarcoplasmic reticulum vesicles. J Biol Chem. 1984 Jun 25;259(12):7547–7553. [PubMed] [Google Scholar]
  12. Chapman R. A., Miller D. J. The effects of caffeine on the contraction of the frog heart. J Physiol. 1974 Nov;242(3):589–613. doi: 10.1113/jphysiol.1974.sp010725. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Chay T. R. Kinetic modeling for the channel gating process from single channel patch clamp data. J Theor Biol. 1988 Jun 22;132(4):449–468. doi: 10.1016/s0022-5193(88)80084-5. [DOI] [PubMed] [Google Scholar]
  14. Colombini M. A candidate for the permeability pathway of the outer mitochondrial membrane. Nature. 1979 Jun 14;279(5714):643–645. doi: 10.1038/279643a0. [DOI] [PubMed] [Google Scholar]
  15. 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]
  16. Courtney K. R. Mechanism of frequency-dependent inhibition of sodium currents in frog myelinated nerve by the lidocaine derivative GEA. J Pharmacol Exp Ther. 1975 Nov;195(2):225–236. [PubMed] [Google Scholar]
  17. Donaldson S. K. Peeled mammalian skeletal muscle fibers. Possible stimulation of Ca2+ release via a transverse tubule-sarcoplasmic reticulum mechanism. J Gen Physiol. 1985 Oct;86(4):501–525. doi: 10.1085/jgp.86.4.501. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. FEINSTEIN M. B. INHIBITION OF CAFFEINE RIGOR AND RADIOCALCIUM MOVEMENTS BY LOCAL ANESTHETICS IN FROG SARTORIUS MUSCLE. J Gen Physiol. 1963 Sep;47:151–172. doi: 10.1085/jgp.47.1.151. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Fabiato A., Fabiato F. Calculator programs for computing the composition of the solutions containing multiple metals and ligands used for experiments in skinned muscle cells. J Physiol (Paris) 1979;75(5):463–505. [PubMed] [Google Scholar]
  20. 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]
  21. Györke S., Palade P. Calcium-induced calcium release in crayfish skeletal muscle. J Physiol. 1992 Nov;457:195–210. doi: 10.1113/jphysiol.1992.sp019373. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Hamilton S. L., Alvarez R. M., Fill M., Hawkes M. J., Brush K. L., Schilling W. P., Stefani E. [3H]PN200-110 and [3H]ryanodine binding and reconstitution of ion channel activity with skeletal muscle membranes. Anal Biochem. 1989 Nov 15;183(1):31–41. doi: 10.1016/0003-2697(89)90167-x. [DOI] [PubMed] [Google Scholar]
  23. Harigaya S., Schwartz A. Rate of calcium binding and uptake in normal animal and failing human cardiac muscle. Membrane vesicles (relaxing system) and mitochondria. Circ Res. 1969 Dec;25(6):781–794. doi: 10.1161/01.res.25.6.781. [DOI] [PubMed] [Google Scholar]
  24. Heistracher P., Hunt C. C. The effect of procaine on snake twitch muscle fibres. J Physiol. 1969 May;201(3):627–638. doi: 10.1113/jphysiol.1969.sp008776. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Hess P., Lansman J. B., Tsien R. W. Calcium channel selectivity for divalent and monovalent cations. Voltage and concentration dependence of single channel current in ventricular heart cells. J Gen Physiol. 1986 Sep;88(3):293–319. doi: 10.1085/jgp.88.3.293. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Hess P., Tsien R. W. Mechanism of ion permeation through calcium channels. 1984 May 31-Jun 6Nature. 309(5967):453–456. doi: 10.1038/309453a0. [DOI] [PubMed] [Google Scholar]
  27. Hille B. Local anesthetics: hydrophilic and hydrophobic pathways for the drug-receptor reaction. J Gen Physiol. 1977 Apr;69(4):497–515. doi: 10.1085/jgp.69.4.497. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Holmberg S. R., Williams A. J. The cardiac sarcoplasmic reticulum calcium-release channel: modulation of ryanodine binding and single-channel activity. Biochim Biophys Acta. 1990 Feb 28;1022(2):187–193. doi: 10.1016/0005-2736(90)90113-3. [DOI] [PubMed] [Google Scholar]
  29. Hondeghem L. M., Katzung B. G. Time- and voltage-dependent interactions of antiarrhythmic drugs with cardiac sodium channels. Biochim Biophys Acta. 1977 Nov 14;472(3-4):373–398. doi: 10.1016/0304-4157(77)90003-x. [DOI] [PubMed] [Google Scholar]
  30. Kawano S., DeHaan R. L. Analysis of the T-type calcium channel in embryonic chick ventricular myocytes. J Membr Biol. 1990 Jun;116(1):9–17. doi: 10.1007/BF01871667. [DOI] [PubMed] [Google Scholar]
  31. Kawano S., DeHaan R. L. Developmental changes in the calcium currents in embryonic chick ventricular myocytes. J Membr Biol. 1991 Feb;120(1):17–28. doi: 10.1007/BF01868587. [DOI] [PubMed] [Google Scholar]
  32. Kawasaki T., Kasai M. Disulfonic stilbene derivatives open the Ca2+ release channel of sarcoplasmic reticulum. J Biochem. 1989 Sep;106(3):401–405. doi: 10.1093/oxfordjournals.jbchem.a122865. [DOI] [PubMed] [Google Scholar]
  33. Klein M. G., Simon B. J., Schneider M. F. Effects of procaine and caffeine on calcium release from the sarcoplasmic reticulum in frog skeletal muscle. J Physiol. 1992;453:341–366. doi: 10.1113/jphysiol.1992.sp019232. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Lansman J. B., Hess P., Tsien R. W. Blockade of current through single calcium channels by Cd2+, Mg2+, and Ca2+. Voltage and concentration dependence of calcium entry into the pore. J Gen Physiol. 1986 Sep;88(3):321–347. doi: 10.1085/jgp.88.3.321. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Levi R., DeFelice L. J. Sodium-conducting channels in cardiac membranes in low calcium. Biophys J. 1986 Jul;50(1):5–9. doi: 10.1016/S0006-3495(86)83433-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Lindsay A. R., Manning S. D., Williams A. J. Monovalent cation conductance in the ryanodine receptor-channel of sheep cardiac muscle sarcoplasmic reticulum. J Physiol. 1991 Aug;439:463–480. doi: 10.1113/jphysiol.1991.sp018676. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. 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]
  38. Magleby K. L., Pallotta B. S. Burst kinetics of single calcium-activated potassium channels in cultured rat muscle. J Physiol. 1983 Nov;344:605–623. doi: 10.1113/jphysiol.1983.sp014958. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. McLaughlin S., Whitaker M. Cations that alter surface potentials of lipid bilayers increase the calcium requirement for exocytosis in sea urchin eggs. J Physiol. 1988 Feb;396:189–204. doi: 10.1113/jphysiol.1988.sp016958. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Nagasaki K., Kasai M. Calcium-induced calcium release from sarcoplasmic reticulum vesicles. J Biochem. 1981 Sep;90(3):749–755. doi: 10.1093/oxfordjournals.jbchem.a133529. [DOI] [PubMed] [Google Scholar]
  41. Neher E., Steinbach J. H. Local anaesthetics transiently block currents through single acetylcholine-receptor channels. J Physiol. 1978 Apr;277:153–176. doi: 10.1113/jphysiol.1978.sp012267. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Ondrias K., Borgatta L., Kim D. H., Ehrlich B. E. Biphasic effects of doxorubicin on the calcium release channel from sarcoplasmic reticulum of cardiac muscle. Circ Res. 1990 Nov;67(5):1167–1174. doi: 10.1161/01.res.67.5.1167. [DOI] [PubMed] [Google Scholar]
  43. Pike G. K., Abramson J. J., Salama G. Effects of tetracaine and procaine on skinned muscle fibres depend on free calcium. J Muscle Res Cell Motil. 1989 Oct;10(5):337–349. doi: 10.1007/BF01758430. [DOI] [PubMed] [Google Scholar]
  44. Rardon D. P., Cefali D. C., Mitchell R. D., Seiler S. M., Jones L. R. High molecular weight proteins purified from cardiac junctional sarcoplasmic reticulum vesicles are ryanodine-sensitive calcium channels. Circ Res. 1989 Apr;64(4):779–789. doi: 10.1161/01.res.64.4.779. [DOI] [PubMed] [Google Scholar]
  45. Rosenberg R. L., Hess P., Tsien R. W. Cardiac calcium channels in planar lipid bilayers. L-type channels and calcium-permeable channels open at negative membrane potentials. J Gen Physiol. 1988 Jul;92(1):27–54. doi: 10.1085/jgp.92.1.27. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Rousseau E., Meissner G. Single cardiac sarcoplasmic reticulum Ca2+-release channel: activation by caffeine. Am J Physiol. 1989 Feb;256(2 Pt 2):H328–H333. doi: 10.1152/ajpheart.1989.256.2.H328. [DOI] [PubMed] [Google Scholar]
  47. Rousseau E., Smith J. S., Henderson J. S., Meissner G. Single channel and 45Ca2+ flux measurements of the cardiac sarcoplasmic reticulum calcium channel. Biophys J. 1986 Nov;50(5):1009–1014. doi: 10.1016/S0006-3495(86)83543-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Sitsapesan R., Williams A. J. Mechanisms of caffeine activation of single calcium-release channels of sheep cardiac sarcoplasmic reticulum. J Physiol. 1990 Apr;423:425–439. doi: 10.1113/jphysiol.1990.sp018031. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. 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]
  50. 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]
  51. 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]
  52. Stephenson D. G., Wendt I. R. Effects of procaine on calcium accumulation by the sarcoplasmic reticulum of mechanically disrupted rat cardiac muscle. J Physiol. 1986 Apr;373:195–207. doi: 10.1113/jphysiol.1986.sp016042. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Thorpe W. R., Seeman P. The site of action of caffeine and procaine in skeletal muscle. J Pharmacol Exp Ther. 1971 Nov;179(2):324–330. [PubMed] [Google Scholar]
  54. Uhrík B., Zacharová D. Recovery of ultrastructural changes accompanying caffeine contractures in isolated muscle fibres of the crayfish. Pflugers Arch. 1976 Jul 30;364(2):183–190. doi: 10.1007/BF00585188. [DOI] [PubMed] [Google Scholar]
  55. Valdivia H. H., Valdivia C., Ma J., Coronado R. Direct binding of verapamil to the ryanodine receptor channel of sarcoplasmic reticulum. Biophys J. 1990 Aug;58(2):471–481. doi: 10.1016/S0006-3495(90)82392-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Weber A., Herz R. The relationship between caffeine contracture of intact muscle and the effect of caffeine on reticulum. J Gen Physiol. 1968 Nov;52(5):750–759. doi: 10.1085/jgp.52.5.750. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Williams A. J., Holmberg S. R. Sulmazole (AR-L 115BS) activates the sheep cardiac muscle sarcoplasmic reticulum calcium-release channel in the presence and absence of calcium. J Membr Biol. 1990 May;115(2):167–178. doi: 10.1007/BF01869455. [DOI] [PubMed] [Google Scholar]
  58. Xu L., Jones R., Meissner G. Effects of local anesthetics on single channel behavior of skeletal muscle calcium release channel. J Gen Physiol. 1993 Feb;101(2):207–233. doi: 10.1085/jgp.101.2.207. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Young H. S., Skita V., Mason R. P., Herbette L. G. Molecular basis for the inhibition of 1,4-dihydropyridine calcium channel drugs binding to their receptors by a nonspecific site interaction mechanism. Biophys J. 1992 May;61(5):1244–1255. doi: 10.1016/S0006-3495(92)81933-1. [DOI] [PMC free article] [PubMed] [Google Scholar]

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