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. 1995 Jun 15;485(Pt 3):659–669. doi: 10.1113/jphysiol.1995.sp020760

Effects of high-energy phosphates on carbachol-evoked cationic current in single smooth muscle cells from guinea-pig ileum.

A Bakhramov 1
PMCID: PMC1158035  PMID: 7562608

Abstract

1. Single smooth muscle cells from the longitudinal muscle layer of guinea-pig small intestine were voltage clamped in the whole-cell recording mode with patch pipettes. The cationic current (Icat) evoked by application of 50 microM carbachol (CCh) was examined when free internal calcium in the cell was 'clamped' at 10(-7) M with 20 mM BAPTA. The effects of varying the composition of the pipette solution were studied. 2. Phosphocreatine (PCr, 6 mM) added to the pipette solution increased Icat by about 7-fold (to near 620 pA); lower concentrations had similar, generally lesser, effects. Na2ATP (3 or 6 mM) with or without 5 mM MgCl2 was much less effective than phosphocreatine alone. Addition of 3 mM Na2ATP reduced Icat, whether or not phosphocreatine was present. 3. Creatine (6 mM) with or without 2 mM Na2ATP was less effective than phosphocreatine in maintaining Icat. 4. GTP (0.1 mM) did not affect Icat evoked by CCh, whether phosphocreatine was present or not. 5. GTP gamma S (0.2 mM) included in pipette solution mimicked the effect of CCH and evoked Icat independently of whether PCr was present or not in the pipette solution. Including 5 mM ATP in the pipette reduced this current, whereas 5'-adenylyl imidodiphosphate (AMP-PNP) and ADP were without effect. 6. The results show that phosphocreatine increases membrane channel responsiveness to receptor activation and that ATP above 2 mM suppresses it.

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Selected References

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  1. Barron J. T., Kopp S. J., Tow J. P., Messer J. V. Effects of altering carbohydrate metabolism on energy status and contractile function of vascular smooth muscle. Biochim Biophys Acta. 1989 Aug 17;976(1):42–52. doi: 10.1016/s0005-2728(89)80187-2. [DOI] [PubMed] [Google Scholar]
  2. Beech D. J., Zhang H., Nakao K., Bolton T. B. K channel activation by nucleotide diphosphates and its inhibition by glibenclamide in vascular smooth muscle cells. Br J Pharmacol. 1993 Oct;110(2):573–582. doi: 10.1111/j.1476-5381.1993.tb13849.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bessman S. P., Carpenter C. L. The creatine-creatine phosphate energy shuttle. Annu Rev Biochem. 1985;54:831–862. doi: 10.1146/annurev.bi.54.070185.004151. [DOI] [PubMed] [Google Scholar]
  4. Champigny G., Verrier B., Lazdunski M. A voltage, calcium, and ATP sensitive non selective cation channel in human colonic tumor cells. Biochem Biophys Res Commun. 1991 May 15;176(3):1196–1203. doi: 10.1016/0006-291x(91)90412-z. [DOI] [PubMed] [Google Scholar]
  5. Clark J. F., Khuchua Z., Kuznetsov A., Saks V. A., Ventura-Clapier R. Compartmentation of creatine kinase isoenzymes in myometrium of gravid guinea-pig. J Physiol. 1993 Jul;466:553–572. [PMC free article] [PubMed] [Google Scholar]
  6. Dawson M. J., Wray S. The effects of pregnancy and parturition on phosphorus metabolites in rat uterus studied by 31P nuclear magnetic resonance. J Physiol. 1985 Nov;368:19–31. doi: 10.1113/jphysiol.1985.sp015844. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Dupuis Y., Tardivel S., Lacour B., Fournier P. Modulation of ileal calcium transport by phosphate-exchanging compounds. Miner Electrolyte Metab. 1992;18(1):61–68. [PubMed] [Google Scholar]
  8. Gray M. A., Argent B. E. Non-selective cation channel on pancreatic duct cells. Biochim Biophys Acta. 1990 Nov 2;1029(1):33–42. doi: 10.1016/0005-2736(90)90433-o. [DOI] [PubMed] [Google Scholar]
  9. Hamill O. P., Marty A., Neher E., Sakmann B., Sigworth F. J. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch. 1981 Aug;391(2):85–100. doi: 10.1007/BF00656997. [DOI] [PubMed] [Google Scholar]
  10. Hardin C. D., Wiseman R. W., Kushmerick M. J. Vascular oxidative metabolism under different metabolic conditions. Biochim Biophys Acta. 1992 Jan 13;1133(2):133–141. doi: 10.1016/0167-4889(92)90060-o. [DOI] [PubMed] [Google Scholar]
  11. Hellstrand P., Paul R. J. Phosphagen content, breakdown during contraction, and O2 consumption in rat portal vein. Am J Physiol. 1983 Mar;244(3):C250–C258. doi: 10.1152/ajpcell.1983.244.3.C250. [DOI] [PubMed] [Google Scholar]
  12. Hellstrand P., Vogel H. J. Phosphagens and intracellular pH in intact rabbit smooth muscle studied by 31P-NMR. Am J Physiol. 1985 Mar;248(3 Pt 1):C320–C329. doi: 10.1152/ajpcell.1985.248.3.C320. [DOI] [PubMed] [Google Scholar]
  13. Inoue R., Isenberg G. Acetylcholine activates nonselective cation channels in guinea pig ileum through a G protein. Am J Physiol. 1990 Jun;258(6 Pt 1):C1173–C1178. doi: 10.1152/ajpcell.1990.258.6.C1173. [DOI] [PubMed] [Google Scholar]
  14. Ishida Y., Paul R. J. Effects of hypoxia on high-energy phosphagen content, energy metabolism and isometric force in guinea-pig taenia caeci. J Physiol. 1990 May;424:41–56. doi: 10.1113/jphysiol.1990.sp018054. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Ishida Y., Wyss M., Hemmer W., Wallimann T. Identification of creatine kinase isoenzymes in the guinea-pig. Presence of mitochondrial creatine kinase in smooth muscle. FEBS Lett. 1991 May 20;283(1):37–43. doi: 10.1016/0014-5793(91)80548-h. [DOI] [PubMed] [Google Scholar]
  16. Komori S., Bolton T. B. Role of G-proteins in muscarinic receptor inward and outward currents in rabbit jejunal smooth muscle. J Physiol. 1990 Aug;427:395–419. doi: 10.1113/jphysiol.1990.sp018178. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Komori S., Kawai M., Takewaki T., Ohashi H. GTP-binding protein involvement in membrane currents evoked by carbachol and histamine in guinea-pig ileal muscle. J Physiol. 1992 May;450:105–126. doi: 10.1113/jphysiol.1992.sp019118. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Konorev E. A., Medvedeva N. V., Jaliashvili I. V., Lakomkin V. L., Saks V. A. Participation of calcium ions in the molecular mechanism of cardioprotective action of exogenous phosphocreatine. Basic Res Cardiol. 1991 Jul-Aug;86(4):327–339. doi: 10.1007/BF02191530. [DOI] [PubMed] [Google Scholar]
  19. Kryzhanovskii S. A., Kacharava V. G., Marko R., Kelemen K., Kaverina N. V., Sakhs V. A. Elektrofiziologicheskoe issledovanie mekhanizmov antiaritmicheskogo deistviia fosfokreatina pri ostroi ishemii i reperfuzii miokarda. Kardiologiia. 1991 Nov;31(11):66–69. [PubMed] [Google Scholar]
  20. Kupriianov V. V., Lakomkin V. L., Shteinshneider A. Ia, Veksler V. I., Korchazhkina O. V., Kapel'ko V. I., Saks V. A. Adrenergicheskaia stimuliatsiia serdtsa pri ingibirovanii fosfokreatinovogo ili adenilatnogo puti transporta énergii v kardiomiotsitakh. Fiziol Zh. 1991 Nov-Dec;37(6):9–19. [PubMed] [Google Scholar]
  21. Lim S. P., Bolton T. B. A calcium-dependent rather than a G-protein mechanism is involved in the inward current evoked by muscarinic receptor stimulation in dialysed single smooth muscle cells of small intestine. Br J Pharmacol. 1988 Oct;95(2):325–327. doi: 10.1111/j.1476-5381.1988.tb11649.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Lynch R. M., Paul R. J. Compartmentation of carbohydrate metabolism in vascular smooth muscle. Am J Physiol. 1987 Mar;252(3 Pt 1):C328–C334. doi: 10.1152/ajpcell.1987.252.3.C328. [DOI] [PubMed] [Google Scholar]
  23. Nakayama S., Tomita T. Depletion of intracellular free Mg2+ in Mg2(+)- and Ca2(+)-free solution in the taenia isolated from guinea-pig caecum. J Physiol. 1990 Feb;421:363–378. doi: 10.1113/jphysiol.1990.sp017949. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Nakayama S., Tomita T. Regulation of intracellular free magnesium concentration in the taenia of guinea-pig caecum. J Physiol. 1991 Apr;435:559–572. doi: 10.1113/jphysiol.1991.sp018525. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Nishimura J., van Breemen C. Energetic aspects of the regulation of Ca++ sensitivity of permeabilized rabbit mesenteric artery: possible involvement of a second Ca++ regulatory system in smooth muscle contraction. J Pharmacol Exp Ther. 1991 Aug;258(2):397–402. [PubMed] [Google Scholar]
  26. Popp R., Gögelein H. A calcium and ATP sensitive nonselective cation channel in the antiluminal membrane of rat cerebral capillary endothelial cells. Biochim Biophys Acta. 1992 Jul 8;1108(1):59–66. doi: 10.1016/0005-2736(92)90114-2. [DOI] [PubMed] [Google Scholar]
  27. Rosenshtraukh L. V., Witt R. C., Nance P. N., Rozanski G. J. Electrophysiologic effects of exogenous phosphocreatine in cardiac tissue: potential antiarrhythmic actions. Am Heart J. 1990 Nov;120(5):1111–1119. doi: 10.1016/0002-8703(90)90124-g. [DOI] [PubMed] [Google Scholar]
  28. Rozenshtraukh L. V., Witt R., Rozanski G. Elektrofiziologicheskie aspekty deistviia kreatinfosfata na kletochnuiu aktivnost' miokarda v normal'nykh usloviiakh i pri ishemii. Kardiologiia. 1990 Nov;30(11):97–101. [PubMed] [Google Scholar]
  29. Scott D. P., Coburn R. F. Phosphocreatine and oxidative metabolism-contraction coupling in rabbit aorta. Am J Physiol. 1989 Aug;257(2 Pt 2):H597–H602. doi: 10.1152/ajpheart.1989.257.2.H597. [DOI] [PubMed] [Google Scholar]
  30. Seppet E. K., Kadaya L. Y., Hata T., Kallikorm A. P., Saks V. A., Vetter R., Dhalla N. S. Thyroid control over membrane processes in rat heart. Am J Physiol. 1991 Oct;261(4 Suppl):66–71. doi: 10.1152/ajplung.1991.261.4.L66. [DOI] [PubMed] [Google Scholar]
  31. Stout M. A. Calcium transport by sarcoplasmic reticulum of vascular smooth muscle: I. MgATP-dependent and MgATP-independent calcium uptake. J Cell Physiol. 1991 Dec;149(3):383–395. doi: 10.1002/jcp.1041490305. [DOI] [PubMed] [Google Scholar]
  32. Thorn P., Petersen O. H. Activation of nonselective cation channels by physiological cholecystokinin concentrations in mouse pancreatic acinar cells. J Gen Physiol. 1992 Jul;100(1):11–25. doi: 10.1085/jgp.100.1.11. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Trautwein W., Hescheler J. Regulation of cardiac L-type calcium current by phosphorylation and G proteins. Annu Rev Physiol. 1990;52:257–274. doi: 10.1146/annurev.ph.52.030190.001353. [DOI] [PubMed] [Google Scholar]
  34. Tsien R. Y. New calcium indicators and buffers with high selectivity against magnesium and protons: design, synthesis, and properties of prototype structures. Biochemistry. 1980 May 27;19(11):2396–2404. doi: 10.1021/bi00552a018. [DOI] [PubMed] [Google Scholar]
  35. Wallimann T., Wyss M., Brdiczka D., Nicolay K., Eppenberger H. M. Intracellular compartmentation, structure and function of creatine kinase isoenzymes in tissues with high and fluctuating energy demands: the 'phosphocreatine circuit' for cellular energy homeostasis. Biochem J. 1992 Jan 1;281(Pt 1):21–40. doi: 10.1042/bj2810021. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Wieland T., Jakobs K. H. Receptor-regulated formation of GTP[gamma S] with subsequent persistent Gs-protein activation in membranes of human platelets. FEBS Lett. 1989 Mar 13;245(1-2):189–193. doi: 10.1016/0014-5793(89)80219-4. [DOI] [PubMed] [Google Scholar]
  37. Yoshizaki K., Watari H., Radda G. K. Role of phosphocreatine in energy transport in skeletal muscle of bullfrog studied by 31P-NMR. Biochim Biophys Acta. 1990 Feb 19;1051(2):144–150. doi: 10.1016/0167-4889(90)90186-h. [DOI] [PubMed] [Google Scholar]
  38. Yount R. G. ATP analogs. Adv Enzymol Relat Areas Mol Biol. 1975;43:1–56. doi: 10.1002/9780470122884.ch1. [DOI] [PubMed] [Google Scholar]
  39. Zang W. J., Yu X. J., Honjo H., Kirby M. S., Boyett M. R. On the role of G protein activation and phosphorylation in desensitization to acetylcholine in guinea-pig atrial cells. J Physiol. 1993 May;464:649–679. doi: 10.1113/jphysiol.1993.sp019656. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Zholos A. V., Bolton T. B. G-protein control of voltage dependence as well as gating of muscarinic metabotropic channels in guinea-pig ileum. J Physiol. 1994 Jul 15;478(Pt 2):195–202. doi: 10.1113/jphysiol.1994.sp020242. [DOI] [PMC free article] [PubMed] [Google Scholar]

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