Cited by 1,208Ion channel regulation and functionPancreatic function and diabetesIon Transport and Channel Regulation

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Intracellular ATP directly blocks K+ channels in pancreatic B-cells

Cook, Daniel L., Hales, Nicholas·1984·Nature

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Abstract

It is known that glucose-induced depolarization of pancreatic B-cells is due to reduced membrane K+-permeability and is coupled to an increase in the rate of glycolysis, but there has been no direct evidence linking specific metabolic processes or products to the closing of membrane K+ channels. During patch-clamp studies of proton inhibition of Ca2+-activated K+ channels [GK(Ca)] in B-cells, we identified a second K+-selective channel which is rapidly and reversibly inhibited by ATP applied to the cytoplasmic surface of the membrane. This channel is spontaneously active in excised patches and frequently coexists with GK(Ca) channels yet is insensitive to membrane potential and to intracellular free Ca2+ and pH. Blocking of the channel is ATP-specific and appears not to require metabolism of the ATP. This ATP-sensitive K+ channel [GK(ATP)] may be a link between metabolism and membrane K+-permeability in pancreatic B-cells.

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Background
4-Phenylureido/thioureido-substituted 2,2-dimethylchroman analogs of cromakalim bearing a bulky 'carbamate' moiety at the 6-position as potent inhibitors of glucose-sensitive insulin secretion.
Pirotte, B., Florence, X., Goffin, E., Medeiros, M. B., de Tullio, P., & Lebrun, P. (2016) · European journal of medicinal chemistry · doi:10.1016/j.ejmech.2016.05.042 · Cited by 7
A Benchtop Closed-loop System Controlled by a Bio-Inspired Silicon Implementation of the Pancreatic β Cell
Oliver, N. S., Georgiou, P., Johnston, D. G., & Toumazou, C. (2009) · Journal of Diabetes Science and Technology · doi:10.1177/193229680900300623 · Cited by 8
“The consequent rise in ATP causes closure of ATP-sensitive K+ channels, KATP.(7,8) This prevents active pumping of K+ out of the cell, changing the ionic gradient and causing depolarization of the cell membrane from –70 mV.”
Background
Interaction of a novel dihydropyridine K+ channel opener, A‐312110, with recombinant sulphonylurea receptors and KATP channels: comparison with the cyanoguanidine P1075
Felsch, H., Lange, U., Hambrock, A., Löffler‐Walz, C., Ruß, U., Carroll, W. A., Gopalakrishnan, M., & Quast, U. (2004) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0705718 · Cited by 7
“2/SUR1 channels close when plasma glucose increases and thereby couple the early phase of insulin secretion to the plasma glucose level (Cook & Hales, 1984; Seghers et al., 2000; Seino & Miki, 2003).”
Background
Critical protein domains and amino acid residues for gating the KIR6.2 channel by intracellular ATP
Wu, J.-P., Piao, H., Rojas, A., Wang, R.-P., Wang, Y., Cui, N., Shi, Y.-B., Chen, F.-X., & Jiang, C. (2004) · Journal of Cellular Physiology · doi:10.1002/jcp.10388 · Cited by 7
“The ATP-sensitive Kþ (KATP) channels are a group of Kþ channels whose activity is modulated by intracellular ATP (Noma, 1983; Cook and Hales, 1984).”
Background
Effect of the new imidazoline derivative S-22068 (PMS 847) on insulin secretion in vitro and glucose turnover in vivo in rats.
Pelé-Tounian, A., Chan, S., Rondu, F., Bihan, G. L., Giroix, M., Lamouri, A., Touboul, E., Pfeiffer, B., Manechez, D., Renard, P., et al. (1999) · European Journal of Pharmacology · doi:10.1016/s0014-2999(99)00395-7 · Cited by 7
RIN14B: a pancreatic δ‐cell line that maintains functional ATP‐dependent K+ channels and capability to secrete insulin under conditions where it no longer secretes somatostatin
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Studies on the essential role of ascorbic acid in the energy dependent release of insulin from pancreatic islets.
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New mechanisms for sulfonylurea control of insulin secretion
Satin, L. S. (1996) · Endocrine · doi:10.1007/bf02738684 · Cited by 17
“Cook and Hales (1984) first described the KATe channels of pancreatic islet [3-cells and proposed that they coupled cellular ATP production to membrane depolarization.”
BackgroundMethodInfluential
Relaxant effect of levcromakalim in isolated human small subcutaneous arteries.
Hüsken, B. C. P., Vroom, M., Timmenga, E. J. F., Pfaffendorf, M., & van Zwieten, P. (1995) · European Journal of Pharmacology · doi:10.1016/0014-2999(95)00714-8 · Cited by 7
ADP exerts a protective effect against rundown of the Ca2+ current in bovine chromaffin cells
Elhamdani, A., Bossu, J., & Feltz, A. (1995) · Pflügers Archiv · doi:10.1007/bf00373916 · Cited by 7
“Estimates under cell-attached conditions point to even smaller concentrations of cytoplasmic ATP: 15 50 gM in/~ cells of the pancreas [ 9 ], 150 gM in cardiac muscles [24].”
BackgroundMethod
Femoral Vasodilation to Cromakalim is Blocked by U37883A, a Non‐sulphonylurea that Selectively Inhibits KATP Channels
Lippton, H., Choe, E., Franklin, E. W., Grivas, T., Flint, L. M., Hyman, A. L., & Ferrara, J. (1995) · The Journal of pharmacy and pharmacology · doi:10.1111/j.2042-7158.1995.tb05787.x · Cited by 7
Potassium channel openers and asthma
Morley, J. (1994) · Clinical Reviews in Allergy · doi:10.1007/bf02815513 · Cited by 7
Structural Study of Pinacidil, a Potassium‐Channel Opener Belonging to the chemical class of N‐alkyl‐N″‐cyano‐N′‐pyridylguanidines
Pirotte, B., Dupont, L., de Tullio, P., Masereel, B., Schynts, M., & Delarge, J. (1993) · doi:10.1002/hlca.19930760318 · Cited by 7
Activation of the ATP-sensitive K+ channel by decavanadate in guinea-pig ventricular myocytes.
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Biology Of Sodium‐Absorbing Epithelial Cells: Dawning of a New Era
Schultz, S. G., & Hudson, R. L. (1991) · Comprehensive physiology · doi:10.1002/j.2040-4603.1991.tb01400.x · Cited by 20
“Potassium channels have been identified in cardiac muscle (215) and pancreatic p-cells (34,67) that are inhibited by ATP; this inhibitory effect is observed over a physiological range of intracellular ATP concentrations and is not dependent on ATP hydrolysis (i.e., it appears to be a purinergic…”
Analysis and use of the perforated patch technique for recording ionic currents in pancreaticβ-cells
Sala, S., Parsey, R. V., Cohen, A., & Matteson, D. (1991) · Journal of Membrane Biology · doi:10.1007/bf01872640 · Cited by 7
Acute stimulation of pancreatic islets by inhibitors of lactic acid transport
Best, L. C., Trebilcock, R., & Tomlinson, S. (1991) · Biochemical Pharmacology · doi:10.1016/0006-2952(91)90537-f · Cited by 9
Studies of the mechanism of activation of HIT-T15 cells by lactate
Lynch, A. M., Trebilcock, R., Tomlinson, S., & Best, L. C. (1991) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/0167-4889(91)90053-z · Cited by 5
The effect of inactivation of calcium channels by intracellular Ca2+ ions in the bursting pancreatic β-cells
Chay, T. R. (1987) · Cell Biophysics · doi:10.1007/bf02797114 · Cited by 29
Inhibition of L-type calcium channels by internal GTP [?S] in mouse pancreatic ? cells
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Evidence of enhancement of malate-aspartate shuttle activity in beta cells of streptozotocin-induced non-insulin-dependent diabetic rats.
Song, D.-K., Ahn, Y., Bae, J., Park, W., Hong, Y.-S., Ho, W., & Earm, Y. (2000) · Metabolism: Clinical and Experimental · doi:10.1016/s0026-0495(00)90838-2 · Cited by 7
Chapter 20 Structure and Function of ATP-Sensitive Potassium Channels
Miki, T., Inagaki, N., Nagashima, K., Gonoi, T., & Seino, S. (1999) · Current topics in membranes · doi:10.1016/s0070-2161(08)60936-3 · Cited by 6
Physiology and Pathophysiology of the Islets of Langerhans
Soria, B. (1997) · Advances in Experimental Medicine and Biology · doi:10.1007/978-1-4899-1819-2 · Cited by 7
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BackgroundInfluential
Glucose Dose Response of Pancreatic β-Cells: Experimental and Theoretical Results
Sherman, A., Carroll, P. B., Santos, R. M., & Atwater, I. J. (1990) · Springer eBooks · doi:10.1007/978-1-4684-5736-0_9 · Cited by 6
Anoxia Reversibly Inactivates Hippocampal Ca-Currents
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Lysine Potentiates Insulin Secretion via AASS-Dependent Catabolism and Regulation of GABA Content and SignalingPreprint
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Muscarinic Agonist Ameliorates Insulin Secretion in Wfs1-Deficient Mice
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Pharmacology of the K‐ATP Channel Blocking Morpholinoguanidine PNU‐37883A
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“Many other reports have further described how K-ATP channels help to control insulin secretion (3,24,96), vascular smooth muscle tone (31,94,109), myocardial contractility and preconditioning (5,32,37,64), and renal tubular function (46, 93,104,118).”
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Loperamide mobilizes intracellular Ca2+ stores in insulin‐secreting HIT‐T15 cells
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“First, an ATPsensitive channel is blocked by intracellular ATP (Cook & Hales, 1984) or by glucose metabolism (Ashcroft et al., 1984; Misler et al., 1986) and has been linked to the depolarization of*Author for correspondence; E-mail: lipinghe40@hotmail.com British Journal of Pharmacology (2003)…”
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Enhanced effect of sulfonylurea (SU) in copolymer comprising a sugar moiety and SU derivative as double ligands on insulin secretion from MIN6 cells
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“Under physiological conditions, the maintenance of homeostatic blood glucose concentrations mainly depends on the appropriate secretion of insulin from pancreatic 3-cells, It has been reported that glucose metabolism gives rise to increased ATP/ADP ratios leading to the closure of ATP-sensitive l( (KATp) channels [1],…”
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Protein kinase A takes center stage in ATP-dependent insulin secretion
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The effect of AL0671, a novel potassium channel opener, on potassium current in rat aortic smooth muscle cells.
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Authors: Cook, D. L., & Hales, N.
Affiliations: United States Department of Veterans Affairs (US)
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 1984-09
Volume: 311
Issue: 5983
Pages: 271-273
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/311271a0
OpenAlex: W1985770721
Cited by: 1,208
References: 24
Citations by year: 2026: 11 · 2025: 16 · 2024: 12 · 2023: 22 · 2022: 14 · 2021: 21 · 2020: 12 · 2019: 19 · 2018: 13 · 2017: 9 · 2016: 15 · 2015: 21 · 2014: 34 · 2013: 14 · 2012: 29
FWCI: 13.20
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
Locations: Nature (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion channel regulation and function
Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Pancreatic function and diabetes
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion Transport and Channel Regulation
Keywords: ATP-sensitive potassium channels, pancreatic beta cells, intracellular ATP, potassium channel inhibition, glycolysis, proton inhibition, calcium-activated potassium channels
MeSH terms: Adenosine Triphosphate, Animals, Cell Membrane Permeability, Cells, Cultured, Cytoplasm, Electric Conductivity, Ion Channels, Islets of Langerhans, Potassium, Rats

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Intracellular ATP directly blocks K+ channels in pancreatic B-cells

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