Abstract
Ca2+-activated K+ channels in the basolateral plasma membrane of bullfrog oxynticopeptic cells are intimately involved in the regulation of acid secretion. Patch-clamp techniques were applied to study the regulating mechanism of these channels. In the excised inside-out configuration, intracellular Mg2+ decreased channel activity in a dose-dependent manner. In the absence of Mg2+, administration of adenosine 5′ triphosphate (ATP) to the cytoplasmic side also inhibited channel activity. On the other hand, in the presence of Mg2+, addition of ATP markedly increased channel activity. At a fixed concentration of free Mg2+ the Mg-ATP complex caused channel activation and shifted the dose response relationship between channel activity and the intracellular Ca2+ concentration to the left. A nonhydrolysable ATP analogue, adenosine 5′-[β,γ-imido]triphosphate (AMP-PNP) adenylyl [β,γ-methylene]diphosphate (AMP-PCP), could not substitute for ATP in channel activation, but a hydrolysable ATP analogue, adenosine 5′-O-(3-thiotriphosphate) (ATP[γS]) could do so. Furthermore, application of alkaline phosphatase to the cytoplasmic side inhibited channel activity. These results demonstrate that Ca2+-activated K+ channels are regulated by Mg2+ and ATP, and suggest that a phosphorylation reaction may be involved in the regulation mechanism of these channels.
Similar content being viewed by others
References
Ashcroft SJ, Ashcroft FM (1990) Properties and functions of ATP-sensitive K-channels. Cell Signal 2:197–214
Carl A, Kenyon JL, Uemura D, Fusetani N, Sanders KM (1991) Regulation of Ca2+-activated K+ channels by protein kinase A and phosphatase inhibitors. Am J Physiol 261: C387-C392
Chen QX, Stelzer A, Kay AR, Wong RK (1990) GABAA receptor function is regulated by phosphorylation in acutely dissociated guinea-pig hippocampal neurones. J Physiol (Lond) 420:207–221
Chung SK, Reinhart PH, Martin BL, Brautigan D, Levitan IB (1991) Protein kinase activity closely associated with a reconstituted calcium-activated potassium channel. Science 253: 560–562
Egan TM, Dagan D, Levitan IB (1993) Properties and modulation of a calcium-activated potassium channel in rat olfactory bulb neurons. J Neurophysiol 69:1433–1442
Ferguson WB (1991) Competitive Mg2+ block of a large-conductance, Ca(2+)-activated K+ channel in rat skeletal muscle. Ca2+, Sr2+, and Ni2+ also block. J Gen Physiol 98:163–181
Findlay I (1988) ATP4- and ATP-Mg inhibit the ATP-sensitive K+ channel of rat ventricular myocytes. Pflügers Arch 412:37–41
Friedman M (1937) Oesophageal and gastric secretion in the frog. J Cell Comp Physiol 10:37–50
Gelband CH, Silberberg SD, Groschner K, van Breemen C (1990) ATP inhibits smooth muscle Ca2+-activated K+ channels. Proc R Soc Lond [Biol] 242:23–28
Godt RE, Maughan DW (1988) On the composition of the cytosol of relaxed skeletal muscle of the frog. Am J Physiol 254:C591-C604
Hamada E, Nakajima T, Ota S, Terano A, Omata M, Nakade S, Mikoshiba K, Kurachi Y (1993) Activation of Ca2+-dependent K+ current by acetylcholine and histamine in a human gastric epithelial cell line. J Gen Physiol 102:667–692
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 391:85–100
Horie M, Irisawa H (1989) Dual effects of intracellular magnesium on muscarinic potassium channel current in single guineapig atrial cells. J Physiol (Lond) 408:313–332
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) 387:251–272
Hunter M, Giebisch G (1988) Calcium-activated K-channels of Amphiuma early distal tubule: inhibition by ATP. Pflügers Arch 412:331–333
Inoue M, Sham FG, Hirschowitz BI (1983) Seasonal variations in pepsinogen secretion from frog esophageal peptic glands. Gastroenterology 84:1195
Kaibara M, Nakajima T, Irisawa H, Giles W (1991) Regulation of spontaneous opening of muscarinic K+ channels in rabbit atrium. J Physiol (Lond) 433:589–613
Komatsu H, Shirakawa T, Katayama N, Harada W, Mieno H, Inoue M, Kajiyama G (1993) MgATP regulates Ca2+-activated K+ channels of frog oxyntic cells (Abstract). Gastroenterology 104: A122
Kotera T, Hashimoto A, Ueda S, Okada Y (1991) Whole-cell K+ current activation in response to voltages and carbachol in gastric parietal cells isolated from guinea pig. J Membr Biol 124:43–52
Leonard A, Cuq P, Magous R, Bali JP (1991) M3-subtype muscarinic receptor that controls intracellular calcium release and inositol phosphate accumulation in gastric parietal cells. Biochem Pharmacol 42:839–845
Matsuda H (1988) Open-state substructure of inwardly rectifying potassium channels revealed by magnesium block in guinea-pig heart cells. J Physiol (Lond) 397:237–258
Metzger HP, Weingart R (1982) Free magnesium in sheep, ferret and frog striated muscle at rest measured with ion-selective micro-electrodes. J Phsiol (Lond) 333:173–188
Mieno H, Kajiyama G (1991) Electrical characteristics of inward-rectifying K+ channels in isolated bullfrog oxyntic cells. Am J Physiol 261:G206-G212
Mieno H, Komatsu H, Harada W, Katayama N, Shirakawa T, Inoue M, Kajiyama G (1994) Regulation of Ca2+-activated K+ channel activity in bullfrog oxyntic cells. J Gastroenterol 29 [Suppl VII]: 55–58
Petersen OH (1992) Stimulus-secretion coupling: cytoplasmic calcium signals and the control of ion channels in exocrine acinar cells. J Physiol (Lond) 448:1–51
Roche S, Gusdinar T, Bali JP, Magous R (1991) Biphasic kinetics of inositiol 1, 4, 5-trisphosphate accumulation in gastrinstimulated parietal cells. Effects of pertussis toxin and extracellular calcium. FEBS Lett 282:147–151
Sandle GI, Fraser G, Long S, Warhurst G (1990) A cAMP-activated chloride channel in the plasma membrane of cultured human gastric cells (HGT-1). Pflügers Arch 417:259–263
Schoenmakers TJ, Visser GJ, Flik G, Theuvenet AP (1992) CHELATOR: an improved method for computing metal ion concentrations in physiological solutions. Biotechniques 12:870–874, 876
Ueda S, Loo DD, Sachs G (1987) Regulation of K+ channels in the basolateral membrane of Necturus oxyntic cells. J Membr Biol 97:31–41
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Komatsu, H., Mieno, H., Tamaki, K. et al. Modulation of Ca2+-activated K+ channels by Mg2+ and ATP in frog oxyntic cells. Pflugers Arch. 431, 494–503 (1996). https://doi.org/10.1007/BF02191895
Received:
Revised:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF02191895