Home LiteratureArticle Details
PMID: 7760018 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Phosphatase is responsible for run down, and probably G protein-mediated inhibition of inwardly rectifying K+ currents in guinea pig chromaffin cells.

The Journal of general physiology ·Vol. 105 ·No. 2 ·1995-02-00 ·Pages 249-66

Inoue M, Imanaga I

Abstract

The mechanism of G protein-mediated inhibition of an inwardly rectifying K+ current (IIR) in adrenal chromaffin cells was investigated using the whole-cell version of the patch clamp technique. In case of recording with use of ATP-containing patch solution, the IIR was well maintained; otherwise, it ran down within 15 min. This run down was not prevented by replacement with adenylyl-imidodiphosphate, a nonhydrolysable analogue of ATP, but was markedly reduced by the addition to the ATP-free solution of 1 microM calyculin A, a specific inhibitor of serine/threonine phosphatase 1 (PP1) and 2A (PP2A). The addition of alkaline phosphatase to the ATP-containing solution facilitated run down of the current, and application of 100 microM H-7, a general kinase inhibitor, reversibly suppressed IIR. These results taken together suggest that inwardly rectifying K+ channels are under the influence of kinase and phosphatase without external signals. Infusion of nonhydrolysable analogues of GTP, guanosine-5'-O-(3-thiophosphate) (GTP gamma S) or guanylyl-imidodiphosphate, through the pipette produced little inward current at -55 mV, but completely inhibited IIR within approximately 5 or 6 min in all cells tested in the presence of 12 microM Mg2+ inside the cell. In contrast, infusion of aluminum fluoride (AlF) complex, another GTP binding (G) protein activator, consistently produced large inward currents, but did not alter IIR noticeably for 15 min in 17% of the cells tested. In the other cells, the inhibition of IIR developed slowly after long latent periods. This inhibitory potency of AlF was not enhanced by an increase in Mg2+ concentrations. Subtraction of the current-voltage relationship before from that noted during the generation of inward current by AlF complex revealed that the inward current diminished progressively with hyperpolarizations, as is the case with a nonselective cation current (INS) induced by a muscarinic agonist. Thus, AlF complex seems to be potent with the generation of INS, but not with IIR inhibition. The addition of 3 microM calyculin A significantly retarded the IIR inhibition by GTP gamma S, whereas that of 1 microM okadaic acid, another inhibitor of PPI and PP2A, markedly prevented the decline of IIR by AIF complex. Our observations suggest that the low potency of AlF complex in inhibiting IIR may be due to interference with phosphatase activity and that the activation of G protein suppresses IIR, probably by enhancing the apparent activity of phosphatase, which may explain run down of the current.

MeSH Terms
1-(5-Isoquinolinesulfonyl)-2-Methylpiperazine Adenosine Triphosphate/pharmacology Adenylyl Imidodiphosphate/pharmacology Alkaline Phosphatase/pharmacology Aluminum Compounds/pharmacology Animals Chromaffin System/cytology,enzymology Down-Regulation/physiology Electrophysiology Female Fluorides/pharmacology GTP-Binding Proteins/physiology Guanosine 5'-O-(3-Thiotriphosphate)/pharmacology Guanylyl Imidodiphosphate/pharmacology Guinea Pigs Isoquinolines/pharmacology Marine Toxins Membrane Potentials Oxazoles/pharmacology Patch-Clamp Techniques Phosphoprotein Phosphatases/antagonists & inhibitors,physiology Phosphorylation Piperazines/pharmacology Potassium Channel Blockers Potassium Channels/physiology Protein Phosphatase 1 Sulfonamides
Chemicals
Aluminum Compounds Isoquinolines Marine Toxins Oxazoles Piperazines Potassium Channel Blockers Potassium Channels Sulfonamides Adenylyl Imidodiphosphate Guanylyl Imidodiphosphate Guanosine 5'-O-(3-Thiotriphosphate) calyculin A 1-(5-Isoquinolinesulfonyl)-2-Methylpiperazine Adenosine Triphosphate N-(2-guanidinoethyl)-5-isoquinolinesulfonamide Alkaline Phosphatase Phosphoprotein Phosphatases Protein Phosphatase 1 GTP-Binding Proteins Fluorides aluminum fluoride
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Inoue M
Department of Physiology, School of Medicine, Fukuoka University, Japan.
Imanaga I
References (40)
40 references, click to expand
  1. An inward-rectifying K+ current in clonal rat pituitary cells and its modulation by thyrotrophin-releasing hormone.
    J Physiol. 1990 Oct;429:169-89 PMID: 2126040
  2. Receptor-effector coupling by G proteins.
    Biochim Biophys Acta. 1990 May 7;1031(2):163-224 PMID: 2160274
  3. Calyculin A and okadaic acid: inhibitors of protein phosphatase activity.
    Biochem Biophys Res Commun. 1989 Mar 31;159(3):871-7 PMID: 2539153
  4. Muscarinic receptor is coupled with a cation channel through a GTP-binding protein in guinea-pig chromaffin cells.
    J Physiol. 1991 May;436:511-29 PMID: 1712039
  5. Regulation of Ca(2+)-activated K+ channels by protein kinase A and phosphatase inhibitors.
    Am J Physiol. 1991 Aug;261(2 Pt 1):C387-92 PMID: 1651653
  6. Fluoride is not an activator of the smaller (20-25 kDa) GTP-binding proteins.
    J Biol Chem. 1991 Aug 25;266(24):15595-7 PMID: 1908456
  7. Modulation of acetylcholine-activated K+ channel function in rat atrial cells by phosphorylation.
    J Physiol. 1991 Jun;437:133-55 PMID: 1653850
  8. Mechanism of fluoride activation of G protein-gated muscarinic atrial K+ channels.
    J Biol Chem. 1991 Dec 5;266(34):22872-7 PMID: 1744080
  9. Modulation of ion channels by somatostatin and acetylcholine.
    Prog Neurobiol. 1992;38(2):203-30 PMID: 1372125
  10. Characterization of the aluminum and beryllium fluoride species which activate transducin. Analysis of the binding and dissociation kinetics.
    J Biol Chem. 1992 Apr 5;267(10):6710-8 PMID: 1551879
  11. Effects of protein kinase inhibitors on canine Purkinje fibre pacemaker depolarization and the pacemaker current i(f).
    J Physiol. 1991;440:367-84 PMID: 1804968
  12. Alpha 1-adrenoceptors reduce background K+ current in rabbit ventricular myocytes.
    J Physiol. 1991 Sep;441:673-84 PMID: 1667803
  13. Intracellular signaling by hydrolysis of phospholipids and activation of protein kinase C.
    Science. 1992 Oct 23;258(5082):607-14 PMID: 1411571
  14. Characteristics and modulation by thyrotropin-releasing hormone of an inwardly rectifying K+ current in patch-perforated GH3 anterior pituitary cells.
    Pflugers Arch. 1992 Oct;422(1):31-9 PMID: 1331977
  15. Inositol-lipid-specific phospholipase C isoenzymes and their differential regulation by receptors.
    Biochem J. 1992 Nov 15;288 ( Pt 1):1-14 PMID: 1332691
  16. Phosphatase inhibition by calyculin A increases i(f) in canine Purkinje fibers and myocytes.
    Pflugers Arch. 1993 Mar;422(6):614-6 PMID: 8385773
  17. On target with a new mechanism for the regulation of protein phosphorylation.
    Trends Biochem Sci. 1993 May;18(5):172-7 PMID: 8392229
  18. Phosphorylation-dependent regulation of nonselective cation channels in guinea pig chromaffin cells.
    Am J Physiol. 1993 Aug;265(2 Pt 1):C343-8 PMID: 7690184
  19. G protein-mediated inhibition of inwardly rectifying K+ channels in guinea pig chromaffin cells.
    Am J Physiol. 1993 Oct;265(4 Pt 1):C946-56 PMID: 8238320
  20. Protein kinase activity closely associated with a reconstituted calcium-activated potassium channel.
    Science. 1991 Aug 2;253(5019):560-2 PMID: 1857986
  21. Reconstitution of catecholamine-sensitive adenylate cyclase. Association of a regulatory component of the enzyme with membranes containing the catalytic protein and beta-adrenergic receptors.
    J Biol Chem. 1979 Apr 10;254(7):2287-95 PMID: 218930
  22. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches.
    Pflugers Arch. 1981 Aug;391(2):85-100 PMID: 6270629
  23. Aluminum: a requirement for activation of the regulatory component of adenylate cyclase by fluoride.
    Proc Natl Acad Sci U S A. 1982 Aug;79(16):4888-91 PMID: 6289322
  24. Properties of a Mr = 38,000 phosphoprotein phosphatase. Modulation by divalent cations, ATP, and fluoride.
    J Biol Chem. 1983 Apr 10;258(7):4214-9 PMID: 6300079
  25. Isoquinolinesulfonamides, novel and potent inhibitors of cyclic nucleotide dependent protein kinase and protein kinase C.
    Biochemistry. 1984 Oct 9;23(21):5036-41 PMID: 6238627
  26. Purification and characterization of a high molecular weight phosphoprotein phosphatase from rabbit liver.
    J Biol Chem. 1985 Nov 15;260(26):14335-43 PMID: 2997204
  27. Activation of polyphosphoinositide phospholipase C by fluoride in WRK1 cell membranes.
    FEBS Lett. 1986 Aug 18;204(2):183-8 PMID: 3015678
  28. The effect of activating ligands on the intrinsic fluorescence of guanine nucleotide-binding regulatory proteins.
    J Biol Chem. 1987 Jan 15;262(2):752-6 PMID: 3100518
  29. Protein phosphatases of the guinea-pig parotid gland.
    Eur J Biochem. 1987 Sep 1;167(2):377-82 PMID: 3040407
  30. Fluoride complexes of aluminium or beryllium act on G-proteins as reversibly bound analogues of the gamma phosphate of GTP.
    EMBO J. 1987 Oct;6(10):2907-13 PMID: 2826123
  31. Pertussis toxin-insensitive G protein mediates substance P-induced inhibition of potassium channels in brain neurons.
    Proc Natl Acad Sci U S A. 1988 May;85(10):3643-7 PMID: 2453066
  32. Inhibitory effect of a marine-sponge toxin, okadaic acid, on protein phosphatases. Specificity and kinetics.
    Biochem J. 1988 Nov 15;256(1):283-90 PMID: 2851982
  33. Angiotensin II induces oscillations of intracellular calcium and blocks anomalous inward rectifying potassium current in mouse renal juxtaglomerular cells.
    Proc Natl Acad Sci U S A. 1989 May;86(9):3423-7 PMID: 2541447
  34. An improved procedure for identifying and quantitating protein phosphatases in mammalian tissues.
    FEBS Lett. 1989 Jul 3;250(2):596-600 PMID: 2546812
  35. An essential role for postsynaptic calmodulin and protein kinase activity in long-term potentiation.
    Nature. 1989 Aug 17;340(6234):554-7 PMID: 2549423
  36. The structure and regulation of protein phosphatases.
    Annu Rev Biochem. 1989;58:453-508 PMID: 2549856
  37. Dendrotoxin-binding brain membrane protein displays a K+ channel activity that is stimulated by both cAMP-dependent and endogenous phosphorylations.
    Biochemistry. 1989 Jul 25;28(15):6455-60 PMID: 2790006
  38. ATP-dependent decay and recovery of K+ channels in guinea pig cardiac myocytes.
    Am J Physiol. 1990 Jan;258(1 Pt 2):H45-50 PMID: 2301614
  39. G protein control of potassium channel activity in a mast cell line.
    J Gen Physiol. 1990 Feb;95(2):205-27 PMID: 2106571
  40. Protein phosphatases: recent progress.
    Adv Second Messenger Phosphoprotein Res. 1991;23:1-121 PMID: 1847640
Article Info
Journal
The Journal of general physiology
Abbr.
J Gen Physiol
ISSN
0022-1295
Published
1995-02-00
Pages
249-66
Language
English
Region
United States
NLM ID
2985110R
PMCID
PMC2216937
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