Skip to main content
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1975 Apr 1;65(1):88–102. doi: 10.1083/jcb.65.1.88

Calcium and pancreatic secretion. I. Subcellular distribution of calcium and magnesium in the exocrine pancreas of the guinea pig

PMCID: PMC2111169  PMID: 165206

Abstract

The distribution of calcium and magnesium has been studied in the acinar cells of the pancreas of the guinea pig. Most of the magnesium was found to be associated with the rough microsomes (probably bound to the ribosomes) and with the postmicrosomal supernate. In contrast, calcium was distributed among all the particulate fractions, primarily the mitochondria, microsomes (especially smooth surfaced), zymogen granules, and the plasmalemma, and was low in the postmicrosomal supernate. Most of the calcium recovered in the particulate fractions was found to be membrane bound. The highest concentrations were found in the membranes of the zymogen granules and in the plasmalemma. By means of control experiments using -45Ca as the tracer, it was established that a considerable redistribution of calcium occurs during homogenization and cell fractionation. At least some of the resulting artifacts were estimated quantitatively and the data were corrected accordingly. The biochemical results were confirmed with the cytochemical antimonate technique carried out on the tissue as well as on isolated fractions. The role of calcium associated with the zymogen granules and with their limiting membranes is discussed in relation to the architecture of the granule and to the functionality of the pancreatic juice.

Full Text

The Full Text of this article is available as a PDF (3.5 MB).

Selected References

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

  1. 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]
  2. Berg N. B., Young R. W. Sulfate metabolism in pancreatic acinar cells. J Cell Biol. 1971 Aug;50(2):469–483. doi: 10.1083/jcb.50.2.469. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Berneis K. H., Pletscher A., Da Prada M. Metal-dependent aggregation of biogenic amines: a hypothesis for their storage and release. Nature. 1969 Oct 18;224(5216):281–282. doi: 10.1038/224281a0. [DOI] [PubMed] [Google Scholar]
  4. COOPERSTEIN S. J., LAZAROW A. A microspectrophotometric method for the determination of cytochrome oxidase. J Biol Chem. 1951 Apr;189(2):665–670. [PubMed] [Google Scholar]
  5. Case R. M. Calcium and gastrointestinal secretion. Digestion. 1973;8(3):269–288. doi: 10.1159/000197324. [DOI] [PubMed] [Google Scholar]
  6. Case T. C. Primary lymphosarcoma of the breast in a 75-year-old woman: case report. J Am Geriatr Soc. 1973 May;21(5):235–238. doi: 10.1111/j.1532-5415.1973.tb01678.x. [DOI] [PubMed] [Google Scholar]
  7. DESNUELLE P., GABELOTEAU C. Sur le role du calcium pendant l'activation du trypsinogène par la trypsine. Arch Biochem Biophys. 1957 Jul;69:475–485. doi: 10.1016/0003-9861(57)90512-x. [DOI] [PubMed] [Google Scholar]
  8. DOUGLAS W. W., POISNER A. M. On the mode of action of acetylcholine in evoking adrenal medullary secretion: increased uptake of calcium during the secretory response. J Physiol. 1962 Aug;162:385–392. doi: 10.1113/jphysiol.1962.sp006940. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. DRAHOTA Z., CARAFOLI E., ROSSI C. S., GAMBLE R. L., LEHNINGER A. L. THE STEADY STATE MAINTENANCE OF ACCUMULATED CA++ IN RAT LIVER MITOCHONDRIA. J Biol Chem. 1965 Jun;240:2712–2720. [PubMed] [Google Scholar]
  10. DREISBACH R. H. EFFECT OF ISOPROTERENOL ON CALCIUM METABOLISM IN RAT SALIVARY GLAND. Proc Soc Exp Biol Med. 1964 Aug-Sep;116:953–956. doi: 10.3181/00379727-116-29418. [DOI] [PubMed] [Google Scholar]
  11. Dean P. M., Matthews E. K. Electrical activity in pancreatic islet cells: effect of ions. J Physiol. 1970 Sep;210(2):265–275. doi: 10.1113/jphysiol.1970.sp009208. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Delaage M., Lazdunski M. The binding of Ca2+ to trypsinogen and its relation to the mechanism of activation. Biochem Biophys Res Commun. 1967 Aug 7;28(3):390–394. doi: 10.1016/0006-291x(67)90323-3. [DOI] [PubMed] [Google Scholar]
  13. 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]
  14. Feinstein H., Schramm M. Energy production in rat parotid gland. Relation tonzyme secretion and effects of caium. Eur J Biochem. 1970 Mar 1;13(1):158–163. doi: 10.1111/j.1432-1033.1970.tb00912.x. [DOI] [PubMed] [Google Scholar]
  15. GREENE L. J., HIRS C. H., PALADE G. E. On the protein composition of bovine pancreatic zymogen granules. J Biol Chem. 1963 Jun;238:2054–2070. [PubMed] [Google Scholar]
  16. HOKIN L. E. Isolation of the zymogen granules of dog pancreas and a study of their properties. Biochim Biophys Acta. 1955 Nov;18(3):379–388. doi: 10.1016/0006-3002(55)90101-3. [DOI] [PubMed] [Google Scholar]
  17. 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]
  18. Herman L., Sato T., Hales C. N. The electron microscopic localization of cations to pancreatic islets of Langerhans and their possible tole in insulin secretion. J Ultrastruct Res. 1973 Feb;42(3):298–311. doi: 10.1016/s0022-5320(73)90058-0. [DOI] [PubMed] [Google Scholar]
  19. 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]
  20. LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
  21. Libanati C. M., Tandler C. J. The distribution of the water-soluble inorganic orthophosphate ions within the cell: accumulation in the nucleus. Electron probe microanalysis. J Cell Biol. 1969 Sep;42(3):754–765. doi: 10.1083/jcb.42.3.754. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. 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]
  23. Meldolesi J., Cova D. Composition of cellular membranes in the pancreas of the guinea pig. IV. Polyacrylamide gel electrophoresis and amino acid composition of membrane proteins. J Cell Biol. 1972 Oct;55(1):1–18. doi: 10.1083/jcb.55.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Meldolesi J., Jamieson J. D., Palade G. E. Composition of cellular membranes in the pancreas of the guinea pig. 3. Enzymatic activities. J Cell Biol. 1971 Apr;49(1):150–158. doi: 10.1083/jcb.49.1.150. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Meldolesi J., Jamieson J. D., Palade G. E. Composition of cellular membranes in the pancreas of the guinea pig. I. Isolation of membrane fractions. J Cell Biol. 1971 Apr;49(1):109–129. doi: 10.1083/jcb.49.1.109. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Nijjar M. S., Pritchard E. T. Calcium binding by a plasma membrane fraction isolated from rat submandibular glands. Biochim Biophys Acta. 1973 Oct 25;323(3):391–395. doi: 10.1016/0005-2736(73)90184-3. [DOI] [PubMed] [Google Scholar]
  27. Poisner A. M., Hava M. The role of adenosine triphosphate and adenosine triphosphatase in the release of catecholamines from the adrenal medulla. IV. Adenosine triphosphate-- activated uptake of calcium by microsomes and mitochondria. Mol Pharmacol. 1970 Jul;6(4):407–415. [PubMed] [Google Scholar]
  28. Rasmussen H. Cell communication, calcium ion, and cyclic adenosine monophosphate. Science. 1970 Oct 23;170(3956):404–412. doi: 10.1126/science.170.3956.404. [DOI] [PubMed] [Google Scholar]
  29. 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]
  30. STEIN E. A., HSIU J., FISCHER E. H. ALPHA-AMYLASES AS CALCIUM-METALLOENZYMES. I. PREPARATION OF CALCIUM-FREE APOAMYLASES BY CHELATION AND ELECTRODIALYSIS. Biochemistry. 1964 Jan;3:56–61. doi: 10.1021/bi00889a010. [DOI] [PubMed] [Google Scholar]
  31. Sandow A. Excitation-contraction coupling in skeletal muscle. Pharmacol Rev. 1965 Sep;17(3):265–320. [PubMed] [Google Scholar]
  32. Selinger Z., Naim E., Lasser M. ATP-dependent calcium uptake by microsomal preparations from rat parotid and submaxillary glands. Biochim Biophys Acta. 1970 Apr 21;203(2):326–334. doi: 10.1016/0005-2736(70)90147-1. [DOI] [PubMed] [Google Scholar]
  33. Shlatz L., Marinetti G. V. Calcium binding to the rat liver plasma membrane. Biochim Biophys Acta. 1972 Dec 1;290(1):70–83. doi: 10.1016/0005-2736(72)90053-3. [DOI] [PubMed] [Google Scholar]
  34. Smillie L. B., Enenkel A. G., Kay C. M. Physicochemical properties and amino acid composition of chymotrypsinogen B. J Biol Chem. 1966 May 10;241(9):2097–2102. [PubMed] [Google Scholar]
  35. Spicer S. S., Hardin J. H., Greene W. B. Nuclear precipitates in pyroantimonate-osmium tetroxide-fixed tissues. J Cell Biol. 1968 Oct;39(1):216–221. doi: 10.1083/jcb.39.1.216. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. THIERS R. E., VALLEE B. L. Distribution of metals in subcellular fractions of rat liver. J Biol Chem. 1957 Jun;226(2):911–920. [PubMed] [Google Scholar]
  37. Toury R. Etude de la fixation de faible affineitè du Ca2+ par les membranes externe et interne des mitochondries et par le rèticulum endoplasmique lisse et rugueux de foie de rat. Biochim Biophys Acta. 1973 May 25;307(3):607–612. doi: 10.1016/0005-2736(73)90305-2. [DOI] [PubMed] [Google Scholar]
  38. Uram M., Lamy F. Purification of two proelastases from porcine pancreas. Biochim Biophys Acta. 1969 Nov 11;194(1):102–111. doi: 10.1016/0005-2795(69)90185-8. [DOI] [PubMed] [Google Scholar]
  39. Wallach D., Schramm M. Calcium and the exportable protein in rat parotid gland. Parallel subcellular distribution and concomitant secretion. Eur J Biochem. 1971 Aug 16;21(3):433–437. doi: 10.1111/j.1432-1033.1971.tb01489.x. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES