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. 1995 Oct 1;488(Pt 1):65–75. doi: 10.1113/jphysiol.1995.sp020946

A maxi Cl- channel coupled to endothelin B receptors in the basolateral membrane of guinea-pig parietal cells.

H Kajita 1, T Kotera 1, Y Shirakata 1, S Ueda 1, M Okuma 1, K Oda-Ohmae 1, M Takimoto 1, Y Urade 1, Y Okada 1
PMCID: PMC1156701  PMID: 8568666

Abstract

1. To study endothelin (ET) receptors in guinea-pig stomach, ET-binding assays and in vitro autoradiography were performed on fundic cell suspensions and on sections of the fundus, respectively. ETA and ETB receptor subtypes were found to coexist in the parietal cells. 2. Endothelin 1 (ET-1) added to the (basolateral) bathing solution was found to activate noisy whole-cell Cl- currents within about 1 min in both single, isolated parietal cells and those within gastric glands obtained from the fundus. 3. ET-1-induced Cl- currents were rapidly blocked by a Cl- channel blocker (NPPB) added to the (basolateral) bathing solution in a concentration-dependent manner with a half-maximum inhibition concentration of 33 microM. 4. The anion selectivity sequence of the ET-1-induced conductance was I- > Br- > Cl- > F-, corresponding to Eisenman's sequence I. 5. Changes in extracellular pH between 5 and 8 did not affect the ET-1-induced activation of Cl- currents. 6. Similar activating effects were also observed with ET-3 and a specific ETB receptor agonist (IRL1620). An ETB receptor antagonist (IRL1720) prevented the ET-1 effect, whereas an ETA-selective antagonist (FR139317 or BQ123) failed to antagonize the ET-1 effect. 7. In the whole-cell mode, unitary Cl- channel events could be observed in association with ET-1-activated macroscopic currents. The single-channel conductances were around 200 and 350 pS at negative and positive membrane potentials, respectively. 8. It is concluded that gastric parietal cells of guinea-pig possess pH-insensitive 'maxi' Cl- channels coupled to ETB receptors in the basolateral membrane.

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Selected References

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  1. Batra V. K., McNeill J. R., Xu Y., Wilson T. W., Gopalakrishnan V. ETB receptors on aortic smooth muscle cells of spontaneously hypertensive rats. Am J Physiol. 1993 Feb;264(2 Pt 1):C479–C484. doi: 10.1152/ajpcell.1993.264.2.C479. [DOI] [PubMed] [Google Scholar]
  2. Becq F., Fanjul M., Mahieu I., Berger Z., Gola M., Hollande E. Anion channels in a human pancreatic cancer cell line (Capan-1) of ductal origin. Pflugers Arch. 1992 Jan;420(1):46–53. doi: 10.1007/BF00378640. [DOI] [PubMed] [Google Scholar]
  3. Brown M. A., Smith P. L. Endothelin: a potent stimulator of intestinal ion secretion in vitro. Regul Pept. 1991 Oct 1;36(1):1–19. doi: 10.1016/0167-0115(91)90191-i. [DOI] [PubMed] [Google Scholar]
  4. Brown P. D., Greenwood S. L., Robinson J., Boyd R. D. Chloride channels of high conductance in the microvillous membrane of term human placenta. Placenta. 1993 Jan-Feb;14(1):103–115. doi: 10.1016/s0143-4004(05)80253-x. [DOI] [PubMed] [Google Scholar]
  5. Edwards R. M., Pullen M., Nambi P. Activation of endothelin ETB receptors increases glomerular cGMP via an L-arginine-dependent pathway. Am J Physiol. 1992 Dec;263(6 Pt 2):F1020–F1025. doi: 10.1152/ajprenal.1992.263.6.F1020. [DOI] [PubMed] [Google Scholar]
  6. Habuchi Y., Tanaka H., Furukawa T., Tsujimura Y., Takahashi H., Yoshimura M. Endothelin enhances delayed potassium current via phospholipase C in guinea pig ventricular myocytes. Am J Physiol. 1992 Feb;262(2 Pt 2):H345–H354. doi: 10.1152/ajpheart.1992.262.2.H345. [DOI] [PubMed] [Google Scholar]
  7. Hanrahan J. W., Alles W. P., Lewis S. A. Single anion-selective channels in basolateral membrane of a mammalian tight epithelium. Proc Natl Acad Sci U S A. 1985 Nov;82(22):7791–7795. doi: 10.1073/pnas.82.22.7791. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Ihara M., Noguchi K., Saeki T., Fukuroda T., Tsuchida S., Kimura S., Fukami T., Ishikawa K., Nishikibe M., Yano M. Biological profiles of highly potent novel endothelin antagonists selective for the ETA receptor. Life Sci. 1992;50(4):247–255. doi: 10.1016/0024-3205(92)90331-i. [DOI] [PubMed] [Google Scholar]
  9. Inoue A., Yanagisawa M., Kimura S., Kasuya Y., Miyauchi T., Goto K., Masaki T. The human endothelin family: three structurally and pharmacologically distinct isopeptides predicted by three separate genes. Proc Natl Acad Sci U S A. 1989 Apr;86(8):2863–2867. doi: 10.1073/pnas.86.8.2863. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. James A. F., Xie L. H., Fujitani Y., Hayashi S., Horie M. Inhibition of the cardiac protein kinase A-dependent chloride conductance by endothelin-1. Nature. 1994 Jul 28;370(6487):297–300. doi: 10.1038/370297a0. [DOI] [PubMed] [Google Scholar]
  11. Jones C. M., Callaghan J. M., Gleeson P. A., Mori Y., Masuda T., Toh B. H. The parietal cell autoantigens recognized in neonatal thymectomy-induced murine gastritis are the alpha and beta subunits of the gastric proton pump [corrected]. Gastroenterology. 1991 Aug;101(2):287–294. doi: 10.1016/0016-5085(91)90002-3. [DOI] [PubMed] [Google Scholar]
  12. Kajita H., Morishima S., Shirakata Y., Kotera T., Ueda S., Okuma M., Okada Y. A mini Cl- channel sensitive to external pH in the basolateral membrane of guinea-pig parietal cells. J Physiol. 1995 Oct 1;488(Pt 1):57–64. doi: 10.1113/jphysiol.1995.sp020945. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Klöckner U., Isenberg G. Endothelin depolarizes myocytes from porcine coronary and human mesenteric arteries through a Ca-activated chloride current. Pflugers Arch. 1991 Mar;418(1-2):168–175. doi: 10.1007/BF00370467. [DOI] [PubMed] [Google Scholar]
  14. Kolb H. A., Brown C. D., Murer H. Identification of a voltage-dependent anion channel in the apical membrane of a Cl(-)-secretory epithelium (MDCK). Pflugers Arch. 1985 Mar;403(3):262–265. doi: 10.1007/BF00583597. [DOI] [PubMed] [Google Scholar]
  15. Koseki C., Imai M., Hirata Y., Yanagisawa M., Masaki T. Autoradiographic distribution in rat tissues of binding sites for endothelin: a neuropeptide? Am J Physiol. 1989 Apr;256(4 Pt 2):R858–R866. doi: 10.1152/ajpregu.1989.256.4.R858. [DOI] [PubMed] [Google Scholar]
  16. Kotera T., Hashimoto A., Ueda S., Okada Y. Whole-cell K+ current activation in response to voltages and carbachol in gastric parietal cells isolated from guinea pig. J Membr Biol. 1991 Oct;124(1):43–52. doi: 10.1007/BF01871363. [DOI] [PubMed] [Google Scholar]
  17. Light D. B., Schwiebert E. M., Fejes-Toth G., Naray-Fejes-Toth A., Karlson K. H., McCann F. V., Stanton B. A. Chloride channels in the apical membrane of cortical collecting duct cells. Am J Physiol. 1990 Feb;258(2 Pt 2):F273–F280. doi: 10.1152/ajprenal.1990.258.2.F273. [DOI] [PubMed] [Google Scholar]
  18. Little P. J., Neylon C. B., Tkachuk V. A., Bobik A. Endothelin-1 and endothelin-3 stimulate calcium mobilization by different mechanisms in vascular smooth muscle. Biochem Biophys Res Commun. 1992 Mar 16;183(2):694–700. doi: 10.1016/0006-291x(92)90538-v. [DOI] [PubMed] [Google Scholar]
  19. Masuda E., Kawano S., Nagano K., Tsuji S., Ishigami Y., Tsujii M., Hayashi N., Fusamoto H., Kamada T. Effect of intravascular ethanol on modulation of gastric mucosal integrity: possible role of endothelin-1. Am J Physiol. 1992 May;262(5 Pt 1):G785–G790. doi: 10.1152/ajpgi.1992.262.5.G785. [DOI] [PubMed] [Google Scholar]
  20. McGill J. M., Basavappa S., Fitz J. G. Characterization of high-conductance anion channels in rat bile duct epithelial cells. Am J Physiol. 1992 Apr;262(4 Pt 1):G703–G710. doi: 10.1152/ajpgi.1992.262.4.G703. [DOI] [PubMed] [Google Scholar]
  21. McGill J. M., Gettys T. W., Basavappa S., Fitz J. G. GTP-binding proteins regulate high conductance anion channels in rat bile duct epithelial cells. J Membr Biol. 1993 May;133(3):253–261. doi: 10.1007/BF00232024. [DOI] [PubMed] [Google Scholar]
  22. Nelson D. J., Tang J. M., Palmer L. G. Single-channel recordings of apical membrane chloride conductance in A6 epithelial cells. J Membr Biol. 1984;80(1):81–89. doi: 10.1007/BF01868692. [DOI] [PubMed] [Google Scholar]
  23. Oda K., Fujitani Y., Watakabe T., Inui T., Okada T., Urade Y., Okuda-Ashitaka E., Ito S. Endothelin stimulates both cAMP formation and phosphatidylinositol hydrolysis in cultured embryonic bovine tracheal cells. FEBS Lett. 1992 Mar 9;299(2):187–191. doi: 10.1016/0014-5793(92)80244-b. [DOI] [PubMed] [Google Scholar]
  24. Roden M., Plass H., Vierhapper H., Turnheim K. Endothelin-1 stimulates chloride and potassium secretion in rabbit descending colon. Pflugers Arch. 1992 Jun;421(2-3):163–167. doi: 10.1007/BF00374823. [DOI] [PubMed] [Google Scholar]
  25. Schneider G. T., Cook D. I., Gage P. W., Young J. A. Voltage sensitive, high-conductance chloride channels in the luminal membrane of cultured pulmonary alveolar (type II) cells. Pflugers Arch. 1985 Aug;404(4):354–357. doi: 10.1007/BF00585348. [DOI] [PubMed] [Google Scholar]
  26. Schwiebert E. M., Light D. B., Fejes-Toth G., Naray-Fejes-Toth A., Stanton B. A. A GTP-binding protein activates chloride channels in a renal epithelium. J Biol Chem. 1990 May 15;265(14):7725–7728. [PubMed] [Google Scholar]
  27. Simonson M. S., Dunn M. J. Endothelin-1 stimulates contraction of rat glomerular mesangial cells and potentiates beta-adrenergic-mediated cyclic adenosine monophosphate accumulation. J Clin Invest. 1990 Mar;85(3):790–797. doi: 10.1172/JCI114505. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Sogabe K., Nirei H., Shoubo M., Nomoto A., Ao S., Notsu Y., Ono T. Pharmacological profile of FR139317, a novel, potent endothelin ETA receptor antagonist. J Pharmacol Exp Ther. 1993 Mar;264(3):1040–1046. [PubMed] [Google Scholar]
  29. Takahashi K., Jones P. M., Kanse S. M., Lam H. C., Spokes R. A., Ghatei M. A., Bloom S. R. Endothelin in the gastrointestinal tract. Presence of endothelinlike immunoreactivity, endothelin-1 messenger RNA, endothelin receptors, and pharmacological effect. Gastroenterology. 1990 Dec;99(6):1660–1667. doi: 10.1016/0016-5085(90)90472-d. [DOI] [PubMed] [Google Scholar]
  30. Takai M., Umemura I., Yamasaki K., Watakabe T., Fujitani Y., Oda K., Urade Y., Inui T., Yamamura T., Okada T. A potent and specific agonist, Suc-[Glu9,Ala11,15]-endothelin-1(8-21), IRL 1620, for the ETB receptor. Biochem Biophys Res Commun. 1992 Apr 30;184(2):953–959. doi: 10.1016/0006-291x(92)90683-c. [DOI] [PubMed] [Google Scholar]
  31. Van Renterghem C., Lazdunski M. Endothelin and vasopressin activate low conductance chloride channels in aortic smooth muscle cells. Pflugers Arch. 1993 Oct;425(1-2):156–163. doi: 10.1007/BF00374516. [DOI] [PubMed] [Google Scholar]
  32. Velasco G., Prieto M., Alvarez-Riera J., Gascòn S., Barros F. Characteristics and regulation of a high conductance anion channel in GBK kidney epithelial cells. Pflugers Arch. 1989 Jul;414(3):304–310. doi: 10.1007/BF00584631. [DOI] [PubMed] [Google Scholar]
  33. Wallace J. L., Cirino G., De Nucci G., McKnight W., MacNaughton W. K. Endothelin has potent ulcerogenic and vasoconstrictor actions in the stomach. Am J Physiol. 1989 Apr;256(4 Pt 1):G661–G666. doi: 10.1152/ajpgi.1989.256.4.G661. [DOI] [PubMed] [Google Scholar]
  34. Wallace J. L., Keenan C. M., MacNaughton W. K., McKnight G. W. Comparison of the effects of endothelin-1 and endothelin-3 on the rat stomach. Eur J Pharmacol. 1989 Aug 11;167(1):41–47. doi: 10.1016/0014-2999(89)90745-0. [DOI] [PubMed] [Google Scholar]

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