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PMID: 8722562 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Mechanism of action of K channel openers on skeletal muscle KATP channels. Interactions with nucleotides and protons.

The Journal of general physiology ·Vol. 107 ·No. 4 ·1996-04-00 ·Pages 489-502

Forestier C, Pierrard J, Vivaudou M

Abstract

The molecular mechanisms underlying the actions of K channel openers (KCOs) on KATP channels were studied with the patch clamp technique in excised inside-out patches from frog skeletal muscle fibers. Benzopyran KCOs (levcromakalim and SR 47063) opened channels partially blocked by ATP, ADP, or ATP gamma s, with and without Mg2+, but they had no effects in the absence of internal nucleotides, even after channel activity had significantly declined because of rundown. The effects of KCOs could therefore be attributed solely to a competitive interaction between KCOs and nucleotides, as confirmed by observations that ATP decreased the apparent affinity for KCOs and that, conversely, KCOs decreased ATP or ADP sensitivity. Protons antagonized the action of the non-benzopyran KCOs, pinacidil and aprikalim, by enhancing their dissociation rate. This effect resembled the effect of acidification on benzopyran KCOs (Forestier, C., Y. Depresle, and M. Vivaudou. FEBS Lett. 325:276-280, 1993), suggesting that, in spite of their structural diversity, KCOs could act through the same binding sites. Detailed analysis of the inhibitory effects of protons on channel activity induced by levcromakalim or SR 47063 revealed that, in the presence of 100 microM ATP, this effect developed steeply between pH 7 and 6 and was half maximal at pH 6.6. These results are in quantitative agreement with an allosteric model of the KATP channel possessing four protonation sites, two nucleotidic sites accessible preferentially to Mg(2+)-free nucleotides, and one benzopyran KCO site. The structural implications of this model are discussed.

MeSH Terms
Adenosine Diphosphate/pharmacology Adenosine Triphosphate/pharmacology Animals Chromans/pharmacology Dose-Response Relationship, Drug Hydrogen-Ion Concentration Magnesium/pharmacology Muscle, Skeletal/physiology Nucleotides/pharmacology Patch-Clamp Techniques Potassium Channels/drug effects Protons Rana esculenta
Chemicals
Chromans Nucleotides Potassium Channels Protons SR 47063 Adenosine Diphosphate Adenosine Triphosphate Magnesium
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Forestier C
Laboratoire de Biophysique Moléculaire et Cellulaire (Unité de Recherche Associée 520 du Centre National de la Recherche Scientifique), Departement de Biologie Moleculaire et Structurale, Grenoble, France.
Pierrard J
Vivaudou M
References (43)
43 references, click to expand
  1. Voltage-dependent ATP-sensitive potassium channels of skeletal muscle membrane.
    Nature. 1985 Aug 22-28;316(6030):736-8 PMID: 2412127
  2. Effect of channel blockers on potassium efflux from metabolically exhausted frog skeletal muscle.
    J Physiol. 1987 Feb;383:31-43 PMID: 2443648
  3. Potassium channel openers act through an activation of ATP-sensitive K+ channels in guinea-pig cardiac myocytes.
    Pflugers Arch. 1989 Sep;414(6):669-75 PMID: 2510125
  4. Effects of activation of ATP-sensitive K+ channels in mammalian ventricular myocytes.
    Am J Physiol. 1989 Nov;257(5 Pt 2):H1551-9 PMID: 2589510
  5. Apparent competition between ATP and the potassium channel opener RP 49356 on ATP-sensitive K+ channels of cardiac myocytes.
    Mol Pharmacol. 1989 Dec;36(6):897-902 PMID: 2601686
  6. Modulation of ATP-sensitive K+ channels in skeletal muscle by intracellular protons.
    Nature. 1990 Jan 25;343(6256):375-7 PMID: 2153936
  7. Nucleotide modulation of the activity of rat heart ATP-sensitive K+ channels in isolated membrane patches.
    J Physiol. 1989 Dec;419:193-211 PMID: 2621629
  8. The effects of cromakalim on ATP-sensitive potassium channels in insulin-secreting cells.
    Br J Pharmacol. 1990 Jan;99(1):169-75 PMID: 2184910
  9. Properties and functions of ATP-sensitive K-channels.
    Cell Signal. 1990;2(3):197-214 PMID: 2119205
  10. Modulation of ATP-sensitive K+ channel activity and contractile behavior in mammalian ventricle by the potassium channel openers cromakalim and RP49356.
    J Pharmacol Exp Ther. 1990 Nov;255(2):429-35 PMID: 2243335
  11. Effects of potassium channel openers on single potassium channels in mouse skeletal muscle.
    Naunyn Schmiedebergs Arch Pharmacol. 1990 Sep;342(3):258-63 PMID: 2280794
  12. Two different types of potassium channels in human skeletal muscle activated by potassium channel openers.
    Neurosci Lett. 1990 Nov 13;119(2):191-4 PMID: 2126363
  13. ATP-sensitive K channels in heart muscle. Spare channels.
    FEBS Lett. 1991 Feb 11;279(1):95-7 PMID: 1995351
  14. Determination of the subunit stoichiometry of a voltage-activated potassium channel.
    Nature. 1991 Mar 21;350(6315):232-5 PMID: 1706481
  15. Multiple actions of pinacidil on adenosine triphosphate-sensitive potassium channels in guinea-pig ventricular myocytes.
    J Physiol. 1990 Nov;430:273-95 PMID: 2086765
  16. Skeletal muscle ATP-sensitive K+ channels recorded from sarcolemmal blebs of split fibers: ATP inhibition is reduced by magnesium and ADP.
    J Membr Biol. 1991 Jun;122(2):165-75 PMID: 1910095
  17. Action of nicorandil on ATP-sensitive K+ channel in guinea-pig ventricular myocytes.
    Br J Pharmacol. 1991 Jul;103(3):1641-8 PMID: 1834294
  18. Essential role of nucleotide diphosphates in nicorandil-mediated activation of cardiac ATP-sensitive K+ channel. A comparison with pinacidil and lemakalim.
    Circ Res. 1991 Oct;69(4):1152-8 PMID: 1834361
  19. ATP dependence of KATP channel kinetics in isolated membrane patches from rat ventricle.
    Biophys J. 1991 Nov;60(5):1164-77 PMID: 1760506
  20. ATP-sensitive potassium channels and myocardial ischemia: why do they open?
    Cardiovasc Drugs Ther. 1992 Jun;6(3):201-8 PMID: 1637728
  21. The effect of intracellular pH on ATP-dependent potassium channels of frog skeletal muscle.
    J Physiol. 1992 Jan;445:549-68 PMID: 1501145
  22. Activation of ATP-sensitive K+ channels by cromakalim. Effects on cellular K+ loss and cardiac function in ischemic and reperfused mammalian ventricle.
    Circ Res. 1992 Dec;71(6):1324-33 PMID: 1423930
  23. Nucleotide diphosphates activate the ATP-sensitive potassium channel in mouse skeletal muscle.
    Pflugers Arch. 1992 Nov;422(2):185-92 PMID: 1488275
  24. Binding of the K+ channel opener [3H]P1075 in rat isolated aorta: relationship to functional effects of openers and blockers.
    Mol Pharmacol. 1993 Mar;43(3):474-81 PMID: 8450836
  25. Modulation by Mg2+ and ADP of ATP-sensitive potassium channels in frog skeletal muscle.
    J Membr Biol. 1993 Feb;132(1):87-94 PMID: 8459449
  26. Intracellular protons control the affinity of skeletal muscle ATP-sensitive K+ channels for potassium-channel-openers.
    FEBS Lett. 1993 Jul 5;325(3):276-80 PMID: 8391482
  27. HOE-234, a second generation K+ channel opener, antagonizes the ATP-dependent gating of cardiac ATP-sensitive K+ channels.
    J Pharmacol Exp Ther. 1994 Feb;268(2):818-25 PMID: 8113994
  28. Cloning and functional expression of a rat heart KATP channel.
    Nature. 1994 Aug 11;370(6489):456-9 PMID: 8047164
  29. Nucleotide regulation of ATP sensitive potassium channels.
    Cardiovasc Res. 1994 Jun;28(6):746-53 PMID: 7923274
  30. Intracellular acidification and ADP enhance nicorandil induction of ATP sensitive potassium channel current in cardiomyocytes.
    Cardiovasc Res. 1994 Jun;28(6):831-5 PMID: 7923287
  31. Diverse effects of pinacidil on KATP channels in mouse skeletal muscle in the presence of different nucleotides.
    Cardiovasc Res. 1994 Jun;28(6):841-6 PMID: 7923289
  32. Mechanism of action of a K+ channel activator BRL 38227 on ATP-sensitive K+ channels in mouse skeletal muscle fibres.
    J Physiol. 1994 Aug 1;478 Pt 3:523-32 PMID: 7965862
  33. Molecular mechanism of cyclic-nucleotide-gated channel activation.
    Nature. 1994 Nov 24;372(6504):369-74 PMID: 7969497
  34. Acetylcholine receptor channel imaged in the open state.
    Nature. 1995 Jan 5;373(6509):37-43 PMID: 7800037
  35. Ion channels, electrical activity and insulin secretion.
    Diabete Metab. 1994 Mar-Apr;20(2):138-45 PMID: 7528694
  36. The G-protein-gated atrial K+ channel IKACh is a heteromultimer of two inwardly rectifying K(+)-channel proteins.
    Nature. 1995 Mar 9;374(6518):135-41 PMID: 7877685
  37. Cloning of the beta cell high-affinity sulfonylurea receptor: a regulator of insulin secretion.
    Science. 1995 Apr 21;268(5209):423-6 PMID: 7716547
  38. Heterologous multimeric assembly is essential for K+ channel activity of neuronal and cardiac G-protein-activated inward rectifiers.
    Biochem Biophys Res Commun. 1995 Jul 17;212(2):657-63 PMID: 7626080
  39. Time-dependent fading of the activation of KATP channels, induced by aprikalim and nucleotides, in excised membrane patches from cardiac myocytes.
    Br J Pharmacol. 1995 May;115(1):117-27 PMID: 7647966
  40. Modification by protons of frog skeletal muscle KATP channels: effects on ion conduction and nucleotide inhibition.
    J Physiol. 1995 Aug 1;486 ( Pt 3):629-45 PMID: 7473225
  41. Cardiac ATP-sensitive K+ channels: regulation by intracellular nucleotides and K+ channel-opening drugs.
    Am J Physiol. 1995 Sep;269(3 Pt 1):C525-45 PMID: 7573382
  42. Subunit-dependent assembly of inward-rectifier K+ channels.
    Proc Biol Sci. 1995 Aug 22;261(1361):251-61 PMID: 7568278
  43. ON THE NATURE OF ALLOSTERIC TRANSITIONS: A PLAUSIBLE MODEL.
    J Mol Biol. 1965 May;12:88-118 PMID: 14343300
Article Info
Journal
The Journal of general physiology
Abbr.
J Gen Physiol
ISSN
0022-1295
Published
1996-04-00
Pages
489-502
Language
English
Region
United States
NLM ID
2985110R
PMCID
PMC2217007
Subset
IM
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