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. 1982 Jan;322:107–125. doi: 10.1113/jphysiol.1982.sp014026

Roles of stored calcium on the mechanical response evoked in smooth muscle cells of the porcine coronary artery

Takeo Itoh 1, Makoto Kajiwara 1, Kenji Kitamura 1, Hirosi Kuriyama 1
PMCID: PMC1249659  PMID: 7069609

Abstract

Effects of acetylcholine (ACh), caffeine and procaine on the membrane and mechanical properties of the intact and skinned muscle cells of the porcine coronary artery were investigated using the micro-electrode and isometric tension recording methods.

1. ACh (10-8-10-5 m) had no effect on the membrane potential and membrane resistance, as assessed from the current—voltage relationship.

2. Caffeine possessed dual actions on the membrane property, i.e. a low concentration (0·3-1 mm) hyperpolarized and a high concentration (over 1 mm) depolarized the membrane, while caffeine (over 0·3 mm) consistently increased the ionic conductance of the membrane. Procaine (over 1 mm) depolarized the membrane and decreased the ionic conductance of the membrane.

3. The spike and contraction evoked by outward current pulses in the presence of 10 mm-TEA were suppressed by treatment with caffeine (5 mm) or procaine (3 mm), but the spike was slightly and the electrically induced contraction was significantly suppressed by ACh (10-6 m) due to the marked increase in resting tension.

4. In Ca-free 2 mm-EGTA containing solution, the K-induced contraction (118 mm) rapidly ceased, but not the contraction evoked by ACh (10-5 m) or caffeine (5 mm). The ACh-induced contraction rapidly ceased in the presence of 1 mm-procaine; however, over 5 mm-procaine was required to abolish the caffeine-induced contraction.

5. The pCa—tension relationship was measured in saponin-treated skinned muscles. The minimum concentration of free Ca required to produce contraction was 2 × 10-7 m, while maximum contraction was observed at 10-5 m-free Ca. The maximum amplitude of Ca-induced contraction observed in skinned muscles was larger or the same as that evoked by ACh in the intact muscle. ACh (10-5 m), caffeine (5 mm) and procaine (5 mm) had no effect on the pCa—tension relationship.

6. After Ca has been loaded in skinned muscles, caffeine and replacement of K with choline (116 mm) in the Ca-free EGTA containing solution produced the contraction. However, the application of ACh did not result in a release of the stored Ca, and procaine suppressed the release of Ca activated by caffeine.

7. The present results indicate that ACh activates the muscarinic receptor distributed on the plasma membrane, thus releasing the stored Ca. However, this mechanism may not be a prerequisite for direct action of ACh on the Ca releasing site. The possible mechanism of ACh action on the Ca releasing site, mainly sarcoplasmic reticulum, was discussed in relation to actions of caffeine and procaine, particularly with regard to the functional relations between plasma membrane and sarcoplasmic reticulum.

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Selected References

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

  1. Abe Y., Tomita T. Cable properties of smooth muscle. J Physiol. 1968 May;196(1):87–100. doi: 10.1113/jphysiol.1968.sp008496. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. BULBRING E. Membrane potentials of smooth muscle fibres of the taenia coli of the guinea-pig. J Physiol. 1954 Aug 27;125(2):302–315. doi: 10.1113/jphysiol.1954.sp005159. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Brading A. F., Burnett M., Sneddon P. The effect of sodium removal on the contractile response of the guinea-pig taenia coli to carbachol. J Physiol. 1980 Sep;306:411–429. doi: 10.1113/jphysiol.1980.sp013404. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Brading A. F. Maintenance of ionic composition. Br Med Bull. 1979 Sep;35(3):227–234. doi: 10.1093/oxfordjournals.bmb.a071582. [DOI] [PubMed] [Google Scholar]
  5. Casteels R., Kitamura K., Kuriyama H., Suzuki H. Excitation-contraction coupling in the smooth muscle cells of the rabbit main pulmonary artery. J Physiol. 1977 Sep;271(1):63–79. doi: 10.1113/jphysiol.1977.sp011990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Droogmans G., Casteels R. Sodium and calcium interactions in vascular smooth muscle cells of the rabbit ear artery. J Gen Physiol. 1979 Jul;74(1):57–70. doi: 10.1085/jgp.74.1.57. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Ebashi S. Excitation-contraction coupling. Annu Rev Physiol. 1976;38:293–313. doi: 10.1146/annurev.ph.38.030176.001453. [DOI] [PubMed] [Google Scholar]
  8. Endo M. Calcium release from the sarcoplasmic reticulum. Physiol Rev. 1977 Jan;57(1):71–108. doi: 10.1152/physrev.1977.57.1.71. [DOI] [PubMed] [Google Scholar]
  9. Gabella G. Smooth muscle cell junctions and structural aspects of contraction. Br Med Bull. 1979 Sep;35(3):213–218. doi: 10.1093/oxfordjournals.bmb.a071580. [DOI] [PubMed] [Google Scholar]
  10. Harafuji H., Ogawa Y. Re-examination of the apparent binding constant of ethylene glycol bis(beta-aminoethyl ether)-N,N,N',N'-tetraacetic acid with calcium around neutral pH. J Biochem. 1980 May;87(5):1305–1312. doi: 10.1093/oxfordjournals.jbchem.a132868. [DOI] [PubMed] [Google Scholar]
  11. Hartshorne D. J. Biochemical basis for contraction of vascular smooth muscle. Chest. 1980 Jul;78(1 Suppl):140–149. doi: 10.1378/chest.78.1_supplement.140. [DOI] [PubMed] [Google Scholar]
  12. Hirata M., Mikawa T., Nonomura Y., Ebashi S. Ca2+ regulation in vascular smooth muscle. II. Ca2+ binding of aorta leiotonin. J Biochem. 1980 Feb;87(2):369–378. doi: 10.1093/oxfordjournals.jbchem.a132757. [DOI] [PubMed] [Google Scholar]
  13. Hirst G. D., Neild T. O. Evidence for two populations of excitatory receptors for noradrenaline on arteriolar smooth muscle. Nature. 1980 Feb 21;283(5749):767–768. doi: 10.1038/283767a0. [DOI] [PubMed] [Google Scholar]
  14. Holman M. E., Surprenant A. M. Some properties of the excitatory junction potentials recorded from saphenous arteries of rabbits. J Physiol. 1979 Feb;287:337–351. doi: 10.1113/jphysiol.1979.sp012663. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Ito Y., Kitamura K., Kuriyama H. Actions of nitroglycerine on the membrane and mechanical properties of smooth muscles of the coronary artery of the pig. Br J Pharmacol. 1980 Oct;70(2):197–204. doi: 10.1111/j.1476-5381.1980.tb07925.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Ito Y., Kitamura K., Kuriyama H. Effects of acetylcholine and catecholamines on the smooth muscle cell of the porcine coronary artery. J Physiol. 1979 Sep;294:595–611. doi: 10.1113/jphysiol.1979.sp012948. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Ito Y., Suzuki H., Kuriyama H. Effects of caffeine and procaine on the membrane and mechanical properties of the smooth muscle cells of the rabbit main pulmonary artery. Jpn J Physiol. 1977;27(4):467–481. doi: 10.2170/jjphysiol.27.467. [DOI] [PubMed] [Google Scholar]
  18. Kitamura K., Kuriyama H. Effects of acetylcholine on the smooth muscle cell of isolated main coronary artery of the guinea-pig. J Physiol. 1979 Aug;293:119–133. doi: 10.1113/jphysiol.1979.sp012881. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kuriyama H., Suzuki H. The effects of acetylcholine on the membrane and contractile properties of smooth muscle cells of the rabbit superior mesenteric artery. Br J Pharmacol. 1978 Dec;64(4):493–501. doi: 10.1111/j.1476-5381.1978.tb17310.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Mikawa T., Nonomura Y., Hirata M., Ebashi S., Kakiuchi S. Involvement of an acidic protein in regulation of smooth muscle contraction by the tropomyosin-leiotonin system. J Biochem. 1978 Dec;84(6):1633–1636. doi: 10.1093/oxfordjournals.jbchem.a132290. [DOI] [PubMed] [Google Scholar]
  21. SU C., BEVAN J. A., URSILLO R. C. ELECTRICAL QUIESCENCE OF PULMONARY ARTERY SMOOTH MUSCLE DURING SYMPATHOMIMETIC STIMULATION. Circ Res. 1964 Jul;15:26–27. doi: 10.1161/01.res.15.1.20. [DOI] [PubMed] [Google Scholar]
  22. Saida K., Nonomura Y. Characteristics of Ca2+- and Mg2+-induced tension development in chemically skinned smooth muscle fibers. J Gen Physiol. 1978 Jul;72(1):1–14. doi: 10.1085/jgp.72.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Somlyo A. V., Somlyo A. P. Electromechanical and pharmacomechanical coupling in vascular smooth muscle. J Pharmacol Exp Ther. 1968 Jan;159(1):129–145. [PubMed] [Google Scholar]
  24. Takata Y. Regional differences in electrical and mechanical properties of guinea-pig mesenteric vessels. Jpn J Physiol. 1980;30(5):709–728. doi: 10.2170/jjphysiol.30.709. [DOI] [PubMed] [Google Scholar]
  25. van Breemen C., Aaronson P., Loutzenhiser R., Meisheri K. Ca2+ movements in smooth muscle. Chest. 1980 Jul;78(1 Suppl):157–165. doi: 10.1378/chest.78.1_supplement.157. [DOI] [PubMed] [Google Scholar]

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