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. 1989 Jul;97(3):973–982. doi: 10.1111/j.1476-5381.1989.tb12039.x

Actions of guanine nucleotides and cyclic nucleotides on calcium stores in single patch-clamped smooth muscle cells from rabbit portal vein.

S Komori 1, T B Bolton 1
PMCID: PMC1854567  PMID: 2547494

Abstract

1. Single smooth muscle cells were obtained from the rabbit portal vein by enzymic digestion and membrane currents under voltage clamp measured by whole-cell patch clamp technique. 2. When held at depolarized potentials, spontaneous outward currents (STOCs) were discharged; it is likely that these represent the cyclical storage and release within the cell of calcium in relation to Ca-activated K-channels. 3. Application of lower concentrations of carbachol (10(-5)M) or caffeine (10(-3)M) accelerated STOC discharge. Higher concentrations of caffeine (10(-2)M) or carbachol (10(-4)M), or noradrenaline (10(-5)M), produced an outward current of 1-5 nA which disappeared within 5-15s and which was considered to result from the discharge of calcium stores; STOC discharge was abolished for a period. 4. Ryanodine (10(-5)-10(-4)M) or a non-hydrolysable GTP analogue, GTP gamma S (10(-5)-10(-3)M) introduced into the cell abolished STOC discharge within 2-5 min. STOCs were large in cells filled with GDP beta S (10(-3)M) and the action of GTP gamma S introduced at various concentrations was antagonized. 5. GTP gamma S (10(-4)-10(-3)M) in the cell reduced or abolished outward current to caffeine (10(-2)M) noradrenaline (10(-5)M) or carbachol (10(-4)M); the effect on caffeine outward current was antagonized by GDP beta S (10(-3)M) introduced into the cell. GDP beta S reduced noradrenaline outward current but not caffeine outward current implying the existence of a G-protein step in noradrenaline-evoked Ca-store release, possibly regulating phospholipase C enzyme activity and D-myo inositol 1,4,5 trisphosphate formation. 6. If cyclic AMP (10(-3)M) or cyclic GMP (10(-3)M) was introduced into the cell, or 8-bromo cyclic AMP (0.5 x 10(-3)M) or 8-bromo cyclic GMP (0.5 x 10(-3)M) applied to the cell in the bathing solution, STOC discharge was only slightly affected. However, the outward current to caffeine applied after noradrenaline was much enhanced. 7. The results could be explained if cyclic GMP and cyclic AMP enhance calcium storage whereas GTP gamma S depletes calcium stores, an action antagonized by GDP beta S.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Benham C. D., Bolton T. B., Lang R. J., Takewaki T. Calcium-activated potassium channels in single smooth muscle cells of rabbit jejunum and guinea-pig mesenteric artery. J Physiol. 1986 Feb;371:45–67. doi: 10.1113/jphysiol.1986.sp015961. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Benham C. D., Bolton T. B. Spontaneous transient outward currents in single visceral and vascular smooth muscle cells of the rabbit. J Physiol. 1986 Dec;381:385–406. doi: 10.1113/jphysiol.1986.sp016333. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Brown D. A., Constanti A., Adams P. R. Ca-activated potassium current in vertebrate sympathetic neurons. Cell Calcium. 1983 Dec;4(5-6):407–420. doi: 10.1016/0143-4160(83)90017-9. [DOI] [PubMed] [Google Scholar]
  4. Byerly L., Moody W. J. Intracellular calcium ions and calcium currents in perfused neurones of the snail, Lymnaea stagnalis. J Physiol. 1984 Jul;352:637–652. doi: 10.1113/jphysiol.1984.sp015314. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bülbring E., Tomita T. Catecholamine action on smooth muscle. Pharmacol Rev. 1987 Mar;39(1):49–96. [PubMed] [Google Scholar]
  6. Cockcroft S., Gomperts B. D. Role of guanine nucleotide binding protein in the activation of polyphosphoinositide phosphodiesterase. Nature. 1985 Apr 11;314(6011):534–536. doi: 10.1038/314534a0. [DOI] [PubMed] [Google Scholar]
  7. Diamond J., Holmes T. G. Effects of potassium chloride and smooth muscle relaxants on tension and cyclic nucleotide levels in rat myometrium. Can J Physiol Pharmacol. 1975 Dec;53(6):1099–1107. doi: 10.1139/y75-153. [DOI] [PubMed] [Google Scholar]
  8. 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]
  9. Hwang K. S., van Breemen C. Ryanodine modulation of 45Ca efflux and tension in rabbit aortic smooth muscle. Pflugers Arch. 1987 Apr;408(4):343–350. doi: 10.1007/BF00581127. [DOI] [PubMed] [Google Scholar]
  10. Imagawa T., Smith J. S., Coronado R., Campbell K. P. Purified ryanodine receptor from skeletal muscle sarcoplasmic reticulum is the Ca2+-permeable pore of the calcium release channel. J Biol Chem. 1987 Dec 5;262(34):16636–16643. [PubMed] [Google Scholar]
  11. Itoh T., Izumi H., Kuriyama H. Mechanisms of relaxation induced by activation of beta-adrenoceptors in smooth muscle cells of the guinea-pig mesenteric artery. J Physiol. 1982 May;326:475–493. doi: 10.1113/jphysiol.1982.sp014207. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Katsuki S., Arnold W. P., Murad F. Effects of sodium nitroprusside, nitroglycerin, and sodium azide on levels of cyclic nucleotides and mechanical activity of various tissues. J Cyclic Nucleotide Res. 1977 Aug;3(4):239–247. [PubMed] [Google Scholar]
  13. Kobayashi S., Somlyo A. P., Somlyo A. V. Guanine nucleotide- and inositol 1,4,5-trisphosphate-induced calcium release in rabbit main pulmonary artery. J Physiol. 1988 Sep;403:601–619. doi: 10.1113/jphysiol.1988.sp017267. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Mueller E., van Breemen C. Role of intracellular Ca2+ sequestration in beta-adrenergic relaxation of a smooth muscle. Nature. 1979 Oct 25;281(5733):682–683. doi: 10.1038/281682a0. [DOI] [PubMed] [Google Scholar]
  15. Nishikori K., Maeno H. Close relationship between adenosine 3':5'-monophosphate-dependent endogenous phosphorylation of a specific protein and stimulation of calcium uptake in rat uterine microsomes. J Biol Chem. 1979 Jul 10;254(13):6099–6106. [PubMed] [Google Scholar]
  16. Ohya Y., Kitamura K., Kuriyama H. Cellular calcium regulates outward currents in rabbit intestinal smooth muscle cell. Am J Physiol. 1987 Apr;252(4 Pt 1):C401–C410. doi: 10.1152/ajpcell.1987.252.4.C401. [DOI] [PubMed] [Google Scholar]
  17. Parker I., Ito Y., Kuriyama H., Miledi R. Beta-adrenergic agonists and cyclic AMP decrease intracellular resting free-calcium concentration in ileum smooth muscle. Proc R Soc Lond B Biol Sci. 1987 Mar 23;230(1259):207–214. doi: 10.1098/rspb.1987.0016. [DOI] [PubMed] [Google Scholar]
  18. Sasaguri T., Hirata M., Itoh T., Koga T., Kuriyama H. Guanine nucleotide binding protein involved in muscarinic responses in the pig coronary artery is insensitive to islet-activating protein. Biochem J. 1986 Nov 1;239(3):567–574. doi: 10.1042/bj2390567. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Stryer L., Bourne H. R. G proteins: a family of signal transducers. Annu Rev Cell Biol. 1986;2:391–419. doi: 10.1146/annurev.cb.02.110186.002135. [DOI] [PubMed] [Google Scholar]
  20. Suematsu E., Hirata M., Kuriyama H. Effects of cAMP- and cGMP-dependent protein kinases, and calmodulin on Ca2+ uptake by highly purified sarcolemmal vesicles of vascular smooth muscle. Biochim Biophys Acta. 1984 Jun 13;773(1):83–90. doi: 10.1016/0005-2736(84)90552-2. [DOI] [PubMed] [Google Scholar]

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