Skip to main content
NCBI home page
The Journal of Physiology logoLink to The Journal of Physiology
. 1976 May;257(2):309–324. doi: 10.1113/jphysiol.1976.sp011370

Stimulus-secretion coupling in pancreatic acinar cells: inhibitory effects of calcium removal and manganese addition on pancreozymin-induced amylase release.

T Kanno, O Nishimura
PMCID: PMC1309361  PMID: 950596

Abstract

The role of Ca ions in stimulus-secretion coupling has been analysed in the isolated and perfused rat pancreas. 2. The omission of [Ca2+]O diminished but did not abolish the release of amylase in response to continuous stimulation with 5 m-u. pancreozymin (Pz)/ml. The addition of Mn2+ (1-0 mM) to this Ca-deficient environment abolished the residual release of amylase. This was followed by a complete recovery of amylase output when the control [Ca2+]O was reestablished. 3. The addition of Mn2+ (1-0 mM) to the extracellular environment containing 2-5 mM-Ca2+ reversibly inhibited the Pz-induced release of amylase. 4. A kinetic scheme based on competition of Ca and Mn at a carrier in the acinar cell membrane could quantitatively explain the effects of Ca and Mn upon the Pz-induced amylase release. 5. These results support the view that the Ca2+ influx into the acinar cells is the major contributor to the rise in [Ca2+]i which, in turn, mediates the processes in the stimulus-secretion coupling in the exocrine pancreas, and suggest that the mode of Ca influx is a facilitated diffusion.

Full text

PDF
309

Selected References

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

  1. Argent B. E., Case R. M., Scratcherd T. Amylase secretion by the perfused cat pancreas in relation to the secretion of calcium and other electrolytes and as influenced by the external ionic environment. J Physiol. 1973 May;230(3):575–593. doi: 10.1113/jphysiol.1973.sp010205. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Balnave R. J., Gage P. W. The inhibitory effect of manganese on transmitter release at the neuromuscular junction of the toad. Br J Pharmacol. 1973 Feb;47(2):339–352. doi: 10.1111/j.1476-5381.1973.tb08332.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Benz L., Eckstein B., Matthews E. K., Williams J. A. Control of pancreatic amylase release in vitro: effects of ions, cyclic AMP, and colchicine. Br J Pharmacol. 1972 Sep;46(1):66–67. doi: 10.1111/j.1476-5381.1972.tb06849.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bülbring E., Tomita T. Effect of calcium, barium and manganese on the action of adrenaline in the smooth muscle of the guinea-pig taenia coli. Proc R Soc Lond B Biol Sci. 1969 Mar 11;172(1027):121–136. doi: 10.1098/rspb.1969.0015. [DOI] [PubMed] [Google Scholar]
  5. CRICK J., HARPER A. A., RAPER H. S. On the preparation of secretin and pancreozymin. J Physiol. 1949 Dec;110(3-4):367–376. doi: 10.1113/jphysiol.1949.sp004445. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Case R. M. Calcium and gastrointestinal secretion. Digestion. 1973;8(3):269–288. doi: 10.1159/000197324. [DOI] [PubMed] [Google Scholar]
  7. Case R. M., Clausen T. The relationship between calcium exchange and enzyme secretion in the isolated rat pancreas. J Physiol. 1973 Nov;235(1):75–102. doi: 10.1113/jphysiol.1973.sp010379. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Chandler D. E., Williams J. A. Pancreatic acinar cells: effects of lanthanum ions on amylase release and calcium ion fluxes. J Physiol. 1974 Dec;243(3):831–846. doi: 10.1113/jphysiol.1974.sp010779. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. DEL CASTILLO J., KATZ B. The effect of magnesium on the activity of motor nerve endings. J Physiol. 1954 Jun 28;124(3):553–559. doi: 10.1113/jphysiol.1954.sp005128. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Dean P. M., Matthews E. K. Pancreatic acinar cells: measurement of membrane potential and miniature depolarization potentials. J Physiol. 1972 Aug;225(1):1–13. doi: 10.1113/jphysiol.1972.sp009926. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Dockray G. J. The action of scretin, cholecystokinin-pancreozymin and caerulein on pancreatic secretion in the rat. J Physiol. 1972 Sep;225(3):679–692. doi: 10.1113/jphysiol.1972.sp009963. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Douglas W. W. Stimulus-secretion coupling: the concept and clues from chromaffin and other cells. Br J Pharmacol. 1968 Nov;34(3):451–474. doi: 10.1111/j.1476-5381.1968.tb08474.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Foreman J. C., Mongar J. L. The action of lanthanum and manganese on anaphylactic histamine secretion. Br J Pharmacol. 1973 Jul;48(3):527–537. doi: 10.1111/j.1476-5381.1973.tb08359.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Heatley N. G. The assay of pancreozymin, and of secretin and pancreozymin simultaneously, in the rat. J Endocrinol. 1968 Dec;42(4):549–557. doi: 10.1677/joe.0.0420549. [DOI] [PubMed] [Google Scholar]
  15. Heisler S., Fast D., Tenenhouse A. Role of Ca 2+ and cyclic AMP in protein secretion from rat exocrine pancreas. Biochim Biophys Acta. 1972 Oct 25;279(3):561–572. doi: 10.1016/0304-4165(72)90178-x. [DOI] [PubMed] [Google Scholar]
  16. Heisler S., Grondin G. Effect of lanthanum on 45Ca flux and secretion of protein from rat exocrine pancreas. Life Sci. 1973 Oct 1;13(7):783–794. doi: 10.1016/0024-3205(73)90069-6. [DOI] [PubMed] [Google Scholar]
  17. Hokin L. E. Effects of calcium omission on acetylcholine-stimulated amylase secretion and phospholipid synthesis in pigeon pancreas slices. Biochim Biophys Acta. 1966 Jan 25;115(1):219–221. doi: 10.1016/0304-4165(66)90066-3. [DOI] [PubMed] [Google Scholar]
  18. Hubbard J. I. Microphysiology of vertebrate neuromuscular transmission. Physiol Rev. 1973 Jul;53(3):674–723. doi: 10.1152/physrev.1973.53.3.674. [DOI] [PubMed] [Google Scholar]
  19. JENKINSON D. H. The nature of the antagonism between calcium and magnesium ions at the neuromuscular junction. J Physiol. 1957 Oct 30;138(3):434–444. doi: 10.1113/jphysiol.1957.sp005860. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Kajimoto N., Kirpekar S. M. Effect of manganese and lanthanum on spontaneous release of acetylcholine at frog motor nerve terminals. Nat New Biol. 1972 Jan 5;235(53):29–30. doi: 10.1038/newbio235029a0. [DOI] [PubMed] [Google Scholar]
  21. Kanno T. Calcium-dependent amylase release and electrophysiological measurements in cells of the pancreas. J Physiol. 1972 Oct;226(2):353–371. doi: 10.1113/jphysiol.1972.sp009988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Kanno T., Cochrane D. E., Douglas W. W. Exocytosis (secretory granule extrusion) induced by injection of calcium into mast cells. Can J Physiol Pharmacol. 1973 Dec;51(12):1001–1004. doi: 10.1139/y73-153. [DOI] [PubMed] [Google Scholar]
  23. Kanno T. The electrogenic sodium pump in the hyperpolarizing and secretory effects of pancreozymin in the pancreatic acinar cell. J Physiol. 1975 Mar;245(3):599–616. doi: 10.1113/jphysiol.1975.sp010864. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Kirpekar S. M., Dixon W., Prat J. C. Inhibitory effect of manganese on norepinephrine release from the splenic nerves of cats. J Pharmacol Exp Ther. 1970 Jul;174(1):72–76. [PubMed] [Google Scholar]
  25. Kostial K., Landeka M., Slat B. Manganese ions and synaptic transmission in the superior cervical ganglion of the cat. Br J Pharmacol. 1974 Jun;51(2):231–235. doi: 10.1111/j.1476-5381.1974.tb09652.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Kostyuk P. G., Krishtal O. A., Doroshenko P. A. Calcium currents in snail neurones. I. Identification of calcium current. Pflugers Arch. 1974 Apr 11;348(2):83–93. doi: 10.1007/BF00586471. [DOI] [PubMed] [Google Scholar]
  27. Matthews E. K., Petersen O. H. Pancreatic acinar cells: ionic dependence of the membrane potential and acetycholine-induced depolarization. J Physiol. 1973 Jun;231(2):283–295. doi: 10.1113/jphysiol.1973.sp010233. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Matthews E. K., Petersen O. H., Williams J. A. Pancreatic acinar cells: acetylcholine-induced membrane depolarization, calcium efflux and amylase release. J Physiol. 1973 Nov;234(3):689–701. doi: 10.1113/jphysiol.1973.sp010367. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Nishiyama A., Petersen O. H. Pancreatic acinar cells: ionic dependence of acetylcholine-induced membrane potential and resistance change. J Physiol. 1975 Jan;244(2):431–465. doi: 10.1113/jphysiol.1975.sp010807. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Nonomura Y., Hotta Y., Ohashi H. Tetrodotoxin and manganese ions: effects on electrical activity and tension in taenia coli of guinea pig. Science. 1966 Apr 1;152(3718):97–98. doi: 10.1126/science.152.3718.97. [DOI] [PubMed] [Google Scholar]
  31. Robberecht P., Christophe J. Secretion of hydrolases by perfused fragments of rat pancreas: effect of calcium. Am J Physiol. 1971 Apr;220(4):911–917. doi: 10.1152/ajplegacy.1971.220.4.911. [DOI] [PubMed] [Google Scholar]
  32. Rubin R. P. The role of calcium in the release of neurotransmitter substances and hormones. Pharmacol Rev. 1970 Sep;22(3):389–428. [PubMed] [Google Scholar]
  33. Sabatini-Smith S., Holland W. C. Influence of manganese and ouabain on the rate of action of calcium on atrial contractions. Am J Physiol. 1969 Feb;216(2):244–248. doi: 10.1152/ajplegacy.1969.216.2.244. [DOI] [PubMed] [Google Scholar]
  34. Simpson L. L. The role of calcium in neurohumoral and neurohormonal extrusion processes. J Pharm Pharmacol. 1968 Dec;20(12):889–910. doi: 10.1111/j.2042-7158.1968.tb09672.x. [DOI] [PubMed] [Google Scholar]
  35. Ueda N. Proceedings: An improved method for perfusion of the isolated rat pancreas. J Physiol. 1975 Aug;250(1):4P–5P. [PubMed] [Google Scholar]
  36. van Breemen C., Farinas B. R., Casteels R., Gerba P., Wuytack F., Deth R. Factors controlling cytoplasmic Ca 2+ concentration. Philos Trans R Soc Lond B Biol Sci. 1973 Mar 15;265(867):57–71. doi: 10.1098/rstb.1973.0009. [DOI] [PubMed] [Google Scholar]

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

RESOURCES