Pflügers Archiv

, Volume 414, Issue 6, pp 622–628 | Cite as

ATP-sensitive potassium channels in adult mouse skeletal muscle: Different modes of blockage by internal cations, ATP and tolbutamide

  • K. H. Woll
  • U. Lönnendonker
  • B. Neumcke
Excitable Tissues and Central Nervous Physiology

Abstract

Single ATP-sensitive K channels were studied in membrane patches excised from enzymatically dissociated mouse toe muscle. The channel conductance is 74 pS in symmetrical 160 mM KCl solutions. Replacement of K+ by Na+ in the internal solution or 2 mM internal Ca2+ or Mg2+ induced a rectification of the current-voltage curve at positive potentials. No change of the current-voltage curve was observed by adding small amounts of the channel blockers ATP (20–100 μM) or tolbutamide (0.5 mM) to internal 160 mM KCl solutions. The openings of the channel occurred in bursts. Open (τo), closed (τc) times within bursts and pauses (τp) between bursts were determined over a wide range of positive and negative membrane potentials. At increasing potentials τo increases, τc reaches a minimum near 0 mV and τp decreases. According to the voltage dependence and the time scale of channel blockage three types of blocking agents could be distinguished: (i) small internal cations (Na+, Ca2+, Mg2+) are “fast” blockers at positive voltages; at negative voltages they decrease τo and increase τc. (ii) Internal ATP anions produce a voltage-dependent decline of the open-state probability and strongly decrease τo. (iii) Tolbutamide causes a voltage-independent decrease of the open-probability and its main effect is an increase of τp. The results suggest that the ATP-sensitive K channel has an internal gate like those of other voltage-gated cation channels and that different blockers interfere with different transitions in channel gating.

Key words

Skeletal muscle Patch clamp K channel Adenosine triphosphate Channel blockage 

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References

  1. Allen CN, Akaike A, Albuquerque EX (1984) The frog interosseal muscle fiber as a new model for patch clamp studies of chemosensitive- and voltage-sensitive ion channels: actions of acetylcholine and batrachotoxin. J Physiol (Paris) 79:338–343Google Scholar
  2. Ashcroft FM (1988) Adenosine 5′-triphosphate-sensitive potassium channels. Annu Rev Neurosci 11:97–118Google Scholar
  3. Asheroft FM, Ashcroft SJH, Harrison DE (1988) Properties of single potassium channels modulated by glucose in rat pancreatic B-cells. J Physiol (Lond) 400:501–527Google Scholar
  4. Belles B, Hescheler J, Trube G (1987) Changes of membrane currents in cardiac cells induced by long whole-cell recordings and tolbutamide. Pflügers Arch 409:582–588Google Scholar
  5. Brehm P, Kullberg R (1987) Acetylcholine receptor channels on adult mouse skeletal muscle are functionally identical in synaptic and nonsynaptic membrane. Proc Natl Acad Sci USA 84:2550–2554Google Scholar
  6. Burton F, Dörstelmann U, Hutter OF (1988) Single-channel activity in sarcolemmal vesicles from human and other mammalian muscles. Muscle Nerve 11:1029–1038Google Scholar
  7. Colquhoun D, Sigworth FJ (1983) Fitting and statistical analysis of single-channel records. In: Sakman B, Neher E (eds) Single-channel recording. Plenum Press, New York, pp 191–263Google Scholar
  8. Cook DL, Hales N (1984) Intracellular ATP directly blocks K+ channels in pancreatic B-cells. Nature 311:271–273Google Scholar
  9. Dunne MJ, Illot MC, Petersen OH (1987) Interaction of diazoxide, tolbutamide and ATP4− on nucleotide-dependent K+ channels in an insulin-secreting cell line. J Membr Biol 99:215–224Google Scholar
  10. Dunne MJ, Bullet MJ, Li G, Wollheim CB, Petersen OH (1989) Galanin activates nucleotide-dependent K+ channels in insulin-secreting cells via a pertussis toxin-sensitive G-protein. EMBO J 8:413–420Google Scholar
  11. Findlay I (1987) ATP-sensitive K+ channels in rat ventricular myocytes are blocked and inactivated by internal divalent cations. Pflügers Arch 410:313–320Google Scholar
  12. Findlay I, Dunne MJ, Petersen OH (1985) ATP-sensitive inward rectifier and voltage- and calcium-activated K+ channels in cultured pancreatic islet cells. J Membr Biol 88:165–172Google Scholar
  13. Fink R, Lüttgau HC (1976) An evaluation of the membrane constants and the potassium conductance in metabolically exhausted muscle fibres. J Physiol (Lond) 263:215–238Google Scholar
  14. Hamill OP, Marty A, Neher E, Sakmann B, Sigworth FJ (1981) Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflügers Arch 391:85–100Google Scholar
  15. Hille B (1984) Ionic channels of excitable membranes. Sinauer, Sunderland, MAGoogle Scholar
  16. Horie M, Irisawa H, Noma A (1987) Voltage-dependent magnesium block of adenosine-triphosphate-sensitive potassium channel in guinea-pig ventricular cells. J Physiol (Lond) 387:251–272Google Scholar
  17. Kakei M, Noma A (1984) Adenosine-5′-triphosphate-sensitive single potassium channel in the atrioventricular node cell of the rabbit heart. J Physiol (Lond) 352:265–284Google Scholar
  18. McManus OB, Blatz AL, Magleby KL (1987) Sampling, log binning, fitting, and plotting durations of open and shut intervals from single channels and the effects of noise. Pflügers Arch 410:530–553Google Scholar
  19. Misler S, Falke LC, Gillis K, McDaniel ML (1986) A metabolite-regulated potassium channel in rat pancreatic B-cells. Proc Natl Acad Sci USA 83:7119–7123Google Scholar
  20. Neumcke B, Lönnendonker U, Woll KH (1988) Electrically and chemically gated ion channels in skeletal muscle. Ber Bunsenges Phys Chem 92:1028–1031Google Scholar
  21. Noma A (1983) ATP-regulated K+ channels in cardiac muscle. Nature 305:147–148Google Scholar
  22. Ribalet B, Ciani S (1987) Regulation by cell metabolism and adenine nucleotides of a K channel in insulin-secreting B cells (RIN m5F). Proc Natl Acad Sci USA 84:1721–1725Google Scholar
  23. Schmid-Antomarchi H, DeWeille J, Fosset M, Lazdunski M (1987) The receptor for antidiabetic sulfonylureas controls the activity of the ATP-modulated K+ channel in insulin-secreting cells. J Biol Chem 262:15840–15844Google Scholar
  24. Spruce AE, Standen NB, Stanfield PR (1985) Voltage-dependent ATP-sensitive potassium channels of skeletal muscle membrane. Nature 316:736–738Google Scholar
  25. Spruce AE, Standen NB, Stanfield PR (1987) Studies of the unitary properties of adenosine-5′-triphosphate-regulated potassium channels of frog skeletal muscle. J Physiol (Lond) 382:213–236Google Scholar
  26. Sturgess NC, Ashford MLJ, Cook DL, Hales CN (1985) The sulphonylurea receptor may be an ATP-sensitive potassium channel. Lancet 8453:474–475Google Scholar
  27. Trube G, Hescheler J (1984) Inward-rectifying channels in isolated patches of the heart cell membrane: ATP-dependence and comparison with cell-attached patches. Pflügers Arch 401:178–184Google Scholar
  28. Trube G, Rorsman P, Ohno-Shosaku T (1986) Opposite effects of tolbutamide and diazoxide on the ATP-dependent K+ channel in mouse pancreatic β-cells. Pflügers Arch 407:493–499Google Scholar
  29. Woll KH, Leibowitz MD, Neumcke B, Hille B (1987) A highconductance anion channel in adult amphibian skeletal muscle. Pflügers Arch 410:632–640Google Scholar
  30. Woll KH, Lönnendonker U, Neumcke B (1988) ATP sensitive K channels in adult mouse skeletal muscle. Pflügers Arch 411 (Suppl No 1): R 186 (abstract)Google Scholar
  31. Zilberter Yu, Burnashev N, Papin A, Portnov V, Khodorov B (1988) Gating kinetics of ATP-sensitive single potassium channels in myocardial cells depends on electromotive force. Pflügers Arch 411:584–589Google Scholar

Copyright information

© Springer-Verlag 1989

Authors and Affiliations

  • K. H. Woll
    • 1
  • U. Lönnendonker
    • 1
  • B. Neumcke
    • 1
  1. 1.Physiologisches Institut der Universität des SaarlandesHomburg/SaarFederal Republic of Germany

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