Skip to main content
The Journal of Physiology logoLink to The Journal of Physiology
. 1979 Sep;294:51–68. doi: 10.1113/jphysiol.1979.sp012914

The action of acetylcholine and catecholamines on an intracellular calcium store in the smooth muscle cells of the guinea-pig taenia coli.

R Casteels, L Raeymaekers
PMCID: PMC1280541  PMID: 512955

Abstract

1. The role of an intracellular Ca store in excitation-contraction coupling was studied by recording isometric tension development of thin strips (100-150 micron in diameter) of taenia coli incubated in Ca-free solution containing 2 mM-EGTA. 2. The smooth muscle cells of taenia coli do not contract during exposure to a K+-rich and Ca-free solution. However a contractile response can be elicited by acetylcholine or carbachol at concentrations exceeding 10(-6) M. These contractions are probably induced by a release of intracellular Ca. Ca is also released from the same store, although less effectively, by histamine and caffeine. 3. The amount Ca in the intracellular store, as revealed by the magnitude of the carbachol contraction in Ca-free solution, increases after contractions have been induced by high (K+)0 or by solutions containing low concentrations of carbachol. This contraction amplitude decreases after stimulation with a high concentration of carbachol. The amount of Ca in the filled store is sufficient for a near-maximal contraction. 4. The activation of beta-receptors during a K+-depolarization reduces the height of the contracture and induces a carbachol response in Ca-free solution which is higher than that obtained after a preceding K+ depolarization without isoprenaline. This observation indicates that an increased uptake of Ca into the carbachol-sensitive store contributes to the relaxing effect of beta-agonists. 5. In the tissues which have been loaded with 45Ca in a K+-depolarizing solution, a release of Ca into Ca-free solution is observed when the muscle is stimulated with carbachol, but not when it is stimulated with Ca-free high K+. The release is larger when isoprenaline was present during the loading with 45Ca. 6. The removal of Na+ from the solution exerts a complex and unexplained action on the Ca store. Substitution of Na+ by Tris+ and by K+ have similar effects. 7. It is concluded that the smooth muscle cells of the guinea-pig taenia coli have an intracellular store of Ca which participates in excitation-contraction coupling. The store is sensitive to muscarinic agonists, beta-agonists and monovalent ions, but is not affected by depolarization of the outer membrane.

Full text

PDF
54

Selected References

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

  1. Batra S. The role of mitochondrial calcium uptake in contraction and relaxation of the human myometrium. Biochim Biophys Acta. 1973 May 30;305(2):428–432. doi: 10.1016/0005-2728(73)90188-6. [DOI] [PubMed] [Google Scholar]
  2. Bozler E. Role of calcium in initiation of activity of smooth muscle. Am J Physiol. 1969 Mar;216(3):671–674. doi: 10.1152/ajplegacy.1969.216.3.671. [DOI] [PubMed] [Google Scholar]
  3. Brading A. F. Calcium-induced increase in membrane permeability in the guinea-pig taenia coli: evidence for involvement of a sodium-calcium exchange mechanism. J Physiol. 1978 Feb;275:65–84. doi: 10.1113/jphysiol.1978.sp012178. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Brading A., Bülbring E., Tomita T. The effect of sodium and calcium on the action potential of the smooth muscle of the guinea-pig taenia coli. J Physiol. 1969 Feb;200(3):637–654. doi: 10.1113/jphysiol.1969.sp008713. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bülbring E., Kuriyama H. The action of catecholamines on guinea-pig taenia coli. Philos Trans R Soc Lond B Biol Sci. 1973 Mar 15;265(867):115–121. doi: 10.1098/rstb.1973.0014. [DOI] [PubMed] [Google Scholar]
  6. Casteels R., Droogmans G., Hendrickx H. Membrane potential of smooth muscle cells in K-free solution. J Physiol. 1971 Sep;217(2):281–295. doi: 10.1113/jphysiol.1971.sp009571. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. 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]
  8. Casteels R., Raeymaekers L. The effect of beta-agonists and of K+-depolarization on an intracellular Ca store in smooth muscle of guinea-pig taenia coli [proceedings]. J Physiol. 1978 Dec;285:49P–50P. [PubMed] [Google Scholar]
  9. Casteels R., Van Breemen C. Active and passive Ca2+ fluxes across cell membranes of the guinea-pig taenia coli. Pflugers Arch. 1975 Sep 9;359(3):197–207. doi: 10.1007/BF00587379. [DOI] [PubMed] [Google Scholar]
  10. Deth R., Casteels R. A study of releasable Ca fractions in smooth muscle cells of the rabbit aorta. J Gen Physiol. 1977 Apr;69(4):401–416. doi: 10.1085/jgp.69.4.401. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Deth R., van Breemen C. Relative contributions of Ca2+ influx and cellular Ca2+ release during drug induced activation of the rabbit aorta. Pflugers Arch. 1974 Apr 4;348(1):13–22. doi: 10.1007/BF00587735. [DOI] [PubMed] [Google Scholar]
  12. Devine C. E., Somlyo A. V., Somlyo A. P. Sarcoplasmic reticulum and excitation-contraction coupling in mammalian smooth muscles. J Cell Biol. 1972 Mar;52(3):690–718. doi: 10.1083/jcb.52.3.690. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Droogmans G., Raeymaekers L., Casteels R. Electro- and pharmacomechanical coupling in the smooth muscle cells of the rabbit ear artery. J Gen Physiol. 1977 Aug;70(2):129–148. doi: 10.1085/jgp.70.2.129. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. EDMAN K. A., SCHILD H. O. The need for calcium in the contractile responses induced by acetylcholine and potassium in the rat uterus. J Physiol. 1962 May;161:424–441. doi: 10.1113/jphysiol.1962.sp006897. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Gabella G. Cellular structures and electrophysiological behaviour. Fine structure of smooth muscle. Philos Trans R Soc Lond B Biol Sci. 1973 Mar 15;265(867):7–16. doi: 10.1098/rstb.1973.0004. [DOI] [PubMed] [Google Scholar]
  16. Gabella G., Raeymaekers L. Proceedings: The sphincter pupillae: contractions in Ca2+-free solution. J Physiol. 1975 Jul;249(1):28P–29P. [PubMed] [Google Scholar]
  17. Hiraoka M., Yamagishi S., Sano T. Role of calcium ions in the contraction of vascular smooth muscle. Am J Physiol. 1968 May;214(5):1084–1089. doi: 10.1152/ajplegacy.1968.214.5.1084. [DOI] [PubMed] [Google Scholar]
  18. Keatinge W. R. Ca concentration and flux in Ca-deprived arteries. J Physiol. 1972 Jul;224(1):35–59. doi: 10.1113/jphysiol.1972.sp009880. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Magaribuchi T., Kuriyama H. Effects of noradrenaline and isoprenaline on the electrical and mechanical activities of guinea pig depolarized taenia coli. Jpn J Physiol. 1972 Jun;22(3):253–270. doi: 10.2170/jjphysiol.22.253. [DOI] [PubMed] [Google Scholar]
  20. Mayer C. J., van Breemen C., Casteels T. The action of lanthanum and D600 on the calcium exchange in the smooth muscle cells of the guinea-pig Taenia coli. Pflugers Arch. 1972;337(4):333–350. doi: 10.1007/BF00586650. [DOI] [PubMed] [Google Scholar]
  21. McGuffee L. J., Bagby R. M. Ultrastructure, calcium accumulation, and contractile response in smooth muscle. Am J Physiol. 1976 May;230(5):1217–1224. doi: 10.1152/ajplegacy.1976.230.5.1217. [DOI] [PubMed] [Google Scholar]
  22. Oashi H., Takewaki T., Okada T. Calcium and the contractile effect of carbachol in the depolarized guinea-pig taenia caecum. Jpn J Pharmacol. 1974 Aug;24(4):601–611. doi: 10.1254/jjp.24.601. [DOI] [PubMed] [Google Scholar]
  23. Riemer J., Dörfler F., Mayer C. J., Ulbrecht G. Calcium-antagonistic effects on the spontaneous activity of guinea-pig taenia coli. Pflugers Arch. 1974;351(3):241–258. doi: 10.1007/BF00586921. [DOI] [PubMed] [Google Scholar]
  24. Shibata N., Ohashi H., Takewaki T., Okada T. Calcium source for contractile response of guinea pig taenia caecum to carbachol in a calcium deficient, potassium rich solution. Jpn J Pharmacol. 1978 Aug;28(4):561–568. doi: 10.1254/jjp.28.561. [DOI] [PubMed] [Google Scholar]
  25. Van Breemen C. Calcium requirement for activation of intact aortic smooth muscle. J Physiol. 1977 Nov;272(2):317–329. doi: 10.1113/jphysiol.1977.sp012046. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Van Breemen C., Farinas B. R., Gerba P., McNaughton E. D. Excitation-contraction coupling in rabbit aorta studied by the lanthanum method for measuring cellular calcium influx. Circ Res. 1972 Jan;30(1):44–54. doi: 10.1161/01.res.30.1.44. [DOI] [PubMed] [Google Scholar]
  27. Van Breemen C., Wuytack F., Casteels R., Martinelli B., Campailla E., Ferrari G. Stimulation of 45Ca efflux from smooth muscle cells by metabolic inhibition and high K depolarization. Pflugers Arch. 1975 Sep 9;359(3):183–196. doi: 10.1007/BF00587378. [DOI] [PubMed] [Google Scholar]
  28. Weisbrodt N. W., Hug C. C., Jr, Bass P. Separation of the effects of alpha and beta adrenergic receptor stimulation on taenia coli. J Pharmacol Exp Ther. 1969 Dec;170(2):272–280. [PubMed] [Google Scholar]

Articles from The Journal of Physiology are provided here courtesy of The Physiological Society

RESOURCES