Home LiteratureArticle Details
PMID: 8218909 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Charged local anesthetics block ionic conduction in the sheep cardiac sarcoplasmic reticulum calcium release channel.

Biophysical journal ·Vol. 65 ·No. 2 ·1993-08-00 ·Pages 852-64

Tinker A, Williams AJ

Abstract

We have examined the effect of the charged local anesthetics QX314, QX222, and Procaine on monovalent cation conduction in the Ca2+ release channel of the sheep cardiac sarcoplasmic reticulum. All three blockers only affect cation conductance when present at the cytoplasmic face of the channel. QX222 and Procaine act as voltage-dependent blockers. With 500 Hz filtering, this is manifest as a relatively smooth reduction in single-channel current amplitude most prominent at positive holding potentials. Quantitative analysis gives an effective valence of approximately 0.9 for both ions and Kb(0)s of 9.2 and 15.8 mM for QX222 and Procaine, respectively. Analysis of the concentration dependence of block suggests that QX222 is binding to a single site with a Km of 491 microM at a holding potential of 60 mV. The use of amplitude distribution analysis, with the data filtered at 1 to 2 kHz, reveals that the voltage and concentration dependence of QX222 block occurs largely because of changes in the blocker on rate. The addition of QX314 has a different effect, leading to the production of a substate with an amplitude of approximately one-third that of the control. The substate's occurrence is dependent on holding potential and QX314 concentration. Quantitative analysis reveals that the effect is highly voltage dependent, with a valence of approximately 1.5 caused by approximately equal changes in the on and off rates. Kinetic analysis of the concentration dependence of the substate occurrence reveals positive cooperativity with at least two QX314s binding to the conduction pathway, and this is largely accounted for by changes in the on rate. A paradoxical increase in the off rate at high positive holding potentials and with increasing QX314 concentration at 80 mV suggests the existence of a further QX314-dependent reaction that is both voltage and concentration dependent. The substate block is interpreted physically as a form of partial occlusion in the vestibule of the conduction pathway giving a reduction in single-channel current by electrostatic means.

MeSH Terms
Anesthetics, Local/pharmacology Animals Calcium Channels/drug effects,physiology Dose-Response Relationship, Drug Electric Conductivity/drug effects Ion Channel Gating/drug effects Kinetics Lidocaine/analogs & derivatives,pharmacology Lipid Bilayers Membrane Potentials/drug effects Procaine/pharmacology Sarcoplasmic Reticulum/drug effects,physiology Sheep
Chemicals
Anesthetics, Local Calcium Channels Lipid Bilayers QX-222 QX-314 Procaine Lidocaine
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Tinker A
Department of Cardiac Medicine, National Heart and Lung Institute, University of London, England.
Williams A J
References (43)
43 references, click to expand
  1. Monovalent cation conductance in the ryanodine receptor-channel of sheep cardiac muscle sarcoplasmic reticulum.
    J Physiol. 1991 Aug;439:463-80 PMID: 1716676
  2. Effects of local anesthetics on single channel behavior of skeletal muscle calcium release channel.
    J Gen Physiol. 1993 Feb;101(2):207-33 PMID: 8384242
  3. Examination of subconductance levels arising from a single ion channel.
    J Theor Biol. 1991 Dec 7;153(3):401-23 PMID: 1724679
  4. Ion conduction and discrimination in the sarcoplasmic reticulum ryanodine receptor/calcium-release channel.
    J Muscle Res Cell Motil. 1992 Feb;13(1):7-26 PMID: 1313441
  5. Relaxation and fluctuations of membrane currents that flow through drug-operated channels.
    Proc R Soc Lond B Biol Sci. 1977 Nov 14;199(1135):231-62 PMID: 22856
  6. Local anaesthetics transiently block currents through single acetylcholine-receptor channels.
    J Physiol. 1978 Apr;277:153-76 PMID: 306437
  7. Bis-quaternary ammonium blockers as structural probes of the sarcoplasmic reticulum K+ channel.
    J Gen Physiol. 1982 May;79(5):869-91 PMID: 6284862
  8. Mechanism of calcium release from skeletal sarcoplasmic reticulum.
    J Membr Biol. 1982;66(3):193-201 PMID: 6284941
  9. Open-state substructure of single chloride channels from Torpedo electroplax.
    Philos Trans R Soc Lond B Biol Sci. 1982 Dec 1;299(1097):401-11 PMID: 6130538
  10. On the stochastic properties of bursts of single ion channel openings and of clusters of bursts.
    Philos Trans R Soc Lond B Biol Sci. 1982 Dec 24;300(1098):1-59 PMID: 6131450
  11. Calcium-induced calcium release from purified cardiac sarcoplasmic reticulum vesicles. General characteristics.
    J Biol Chem. 1984 Jun 25;259(12):7540-6 PMID: 6736018
  12. Inhibition of calcium-induced calcium release from purified cardiac sarcoplasmic reticulum vesicles.
    J Biol Chem. 1984 Jun 25;259(12):7547-53 PMID: 6736019
  13. The surprising heart: a review of recent progress in cardiac electrophysiology.
    J Physiol. 1984 Aug;353:1-50 PMID: 6090637
  14. Ionic permeation and blockade in Ca2+-activated K+ channels of bovine chromaffin cells.
    J Gen Physiol. 1984 Aug;84(2):157-86 PMID: 6092514
  15. Sarcoplasmic reticulum contains adenine nucleotide-activated calcium channels.
    Nature. 1985 Aug 1-7;316(6027):446-9 PMID: 2410798
  16. Ion-channel entrances influence permeation. Net charge, size, shape, and binding considerations.
    Biophys J. 1986 Mar;49(3):607-18 PMID: 2421791
  17. 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):573-88 PMID: 2431098
  18. Single channel and 45Ca2+ flux measurements of the cardiac sarcoplasmic reticulum calcium channel.
    Biophys J. 1986 Nov;50(5):1009-14 PMID: 2431724
  19. Quantitative description of three modes of activity of fast chloride channels from rat skeletal muscle.
    J Physiol. 1986 Sep;378:141-74 PMID: 2432249
  20. 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):1740-7 PMID: 3805051
  21. Direct measurement of proton transfer rates to a group controlling the dihydropyridine-sensitive Ca2+ channel.
    Nature. 1987 Sep 17-23;329(6136):243-6 PMID: 2442620
  22. Isolation of the ryanodine receptor from cardiac sarcoplasmic reticulum and identity with the feet structures.
    J Biol Chem. 1987 Nov 15;262(32):15637-42 PMID: 3680217
  23. Purification and reconstitution of the calcium release channel from skeletal muscle.
    Nature. 1988 Jan 28;331(6154):315-9 PMID: 2448641
  24. Ionic blockage of sodium channels in nerve.
    J Gen Physiol. 1973 Jun;61(6):687-708 PMID: 4541078
  25. Calcium release from the sarcoplasmic reticulum.
    Physiol Rev. 1977 Jan;57(1):71-108 PMID: 13441
  26. The pH-dependent rate of action of local anesthetics on the node of Ranvier.
    J Gen Physiol. 1977 Apr;69(4):475-96 PMID: 16078
  27. Delayed afterdepolarizations in heart muscle: mechanisms and relevance.
    Pharmacol Rev. 1988 Sep;40(3):219-27 PMID: 3065793
  28. The voltage-dependent block of ATP-sensitive potassium channels of frog skeletal muscle by caesium and barium ions.
    J Physiol. 1988 Nov;405:677-97 PMID: 3267155
  29. Single channel recordings from human cardiac sarcoplasmic reticulum.
    Circ Res. 1989 Nov;65(5):1445-9 PMID: 2478313
  30. Interactions of protons with single open L-type calcium channels. pH dependence of proton-induced current fluctuations with Cs+, K+, and Na+ as permeant ions.
    J Gen Physiol. 1989 Jul;94(1):1-21 PMID: 2553855
  31. Appraisal of the physiological relevance of two hypothesis for the mechanism of calcium release from the mammalian cardiac sarcoplasmic reticulum: calcium-induced release versus charge-coupled release.
    Mol Cell Biochem. 1989 Sep 7;89(2):135-40 PMID: 2682207
  32. Cytoplasmic [Ca2+] in mammalian ventricle: dynamic control by cellular processes.
    Annu Rev Physiol. 1990;52:467-85 PMID: 2184764
  33. Divalent cation activation and inhibition of single calcium release channels from sheep cardiac sarcoplasmic reticulum.
    J Gen Physiol. 1990 May;95(5):981-1005 PMID: 2163436
  34. Zn2(+)-induced subconductance events in cardiac Na+ channels prolonged by batrachotoxin. Current-voltage behavior and single-channel kinetics.
    J Gen Physiol. 1991 Jan;97(1):117-42 PMID: 1848882
  35. Divalent cation selectivity for external block of voltage-dependent Na+ channels prolonged by batrachotoxin. Zn2+ induces discrete substates in cardiac Na+ channels.
    J Gen Physiol. 1991 Jan;97(1):89-115 PMID: 1848885
  36. Functional characterisation of the ryanodine receptor purified from sheep cardiac muscle sarcoplasmic reticulum.
    Biochim Biophys Acta. 1991 Apr 26;1064(1):89-102 PMID: 2025638
  37. The mechanical hypothesis of excitation-contraction (EC) coupling in skeletal muscle.
    J Muscle Res Cell Motil. 1991 Apr;12(2):127-35 PMID: 1648106
  38. On the interaction of bovine pancreatic trypsin inhibitor with maxi Ca(2+)-activated K+ channels. A model system for analysis of peptide-induced subconductance states.
    J Gen Physiol. 1991 Jun;97(6):1295-319 PMID: 1714938
  39. Large tetraalkyl ammonium cations produce a reduced conductance state in the sheep cardiac sarcoplasmic reticulum Ca(2+)-release channel.
    Biophys J. 1992 May;61(5):1122-32 PMID: 1318091
  40. Block of the sheep cardiac sarcoplasmic reticulum Ca(2+)-release channel by tetra-alkyl ammonium cations.
    J Membr Biol. 1992 Apr;127(2):149-59 PMID: 1625325
  41. Divalent cation conduction in the ryanodine receptor channel of sheep cardiac muscle sarcoplasmic reticulum.
    J Gen Physiol. 1992 Sep;100(3):479-93 PMID: 1279095
  42. A model for ionic conduction in the ryanodine receptor channel of sheep cardiac muscle sarcoplasmic reticulum.
    J Gen Physiol. 1992 Sep;100(3):495-517 PMID: 1279096
  43. Bovine pancreatic trypsin inhibitor as a probe of large conductance Ca(2+)-activated K+ channels at an internal site of interaction.
    Biochem Pharmacol. 1992 Jan 9;43(1):21-8 PMID: 1370897
Article Info
Journal
Biophysical journal
Abbr.
Biophys J
ISSN
0006-3495
Published
1993-08-00
Pages
852-64
Language
English
Region
United States
NLM ID
0370626
PMCID
PMC1225786
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com