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  • Transport Processes, Metabolism And Endocrinology; Kidney, Gastrointestinal Tract, And Exocrine Glands
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The role of calcium in parotid amylase secretion evoked by excitation of cholinergic, α- andβ-adrenergic receptors

  • 28 Accesses

  • 15 Citations

Summary

  1. 1.

    The output of amylase from superfused mouse parotid segments was monitored by an on-line automated fluorometric method.

  2. 2.

    During exposure to Ca2+-free solution, containing the Ca2+-chelating agent EGTA, excitation of α-adrenoceptors or cholinergic receptors only resulted in a very small and transient increase in amylase output. Admission of Ca2+ during sustained stimulation caused a marked rise in amylase output which was sustained.

  3. 3.

    During exposure to Ca2+-free solution containing EGTA excitation of β-adrenoceptors caused the usual very marked rise in amylase output and the enhanced amylase secretion was sustained. Admission of Ca2+ during sustained isoprenaline stimulation only caused a small transient rise in amylase output.

  4. 4.

    The effect of ACh on amylase output varied with the extracellular Ca2+ concentration, being reduced at subnormal extracellular levels and enhanced during superfusion with fluid containing 20 mM Ca2+.

  5. 5.

    5 mM Mn2+ acted as a stimulant of amylase secretion even in the presence of blocking agents for the cholinergic, α- and β-adrenergic receptor sites. The effect of Mn2+ was biphasic; an initial transient increase in amylase output followed by a slowly developing sustained increase in secretion. The initial response was abolished after pretreatment with EGTA in a Ca2+-free solution.

  6. 6.

    Adding Mn2+ (5 mM) just after addition of ACh had caused maximal amylase secretion resulted in an immediate reduction in amylase output. Adding Mn2+ and ACh simultaneously to the superfusion solution resulted in a response smaller than that expected for ACh alone. The effect of ACh during continued exposure to Mn2+ (5 mM) was greatly reduced compared to control conditions. Stimulation with Mn2+ during continued exposure to isoprenaline resulted in a marked transient increase in amylase output.

  7. 7.

    The action of stimulants exciting cholinergic and α-adrenergic receptors is entirely dependent on extracellular Ca2+ whereas the action of stimulants exciting adrenergic β-receptors is relatively independent of Ca2+. Mn2+ immediately inhibits ACh-evoked amylase secretion probably by reducing Ca2+-influx. Mn2+ is, however also a stimulant of amylase secretion probably acting by displacing membrane-bound cell Ca2+.

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References

  1. Albano, J., Bhoola, K. D., Heap, P. F., Lemon, M. J. C.: Stimulus-secretion coupling: role of cyclic AMP, cyclic GMP and calcium in mediating enzyme (kallikrein) secretion in the submandibular gland. J. Physiol. (Lond.)258, 631–658 (1976)

  2. Baker, P. F., Meves, H., Ridgway, E. G.: Effects of manganese and other agents on the calcium uptake that follows depolarization of squid axons. J. Physiol. (Lond.)231, 511–526 (1973a)

  3. Baker, P. F., Meves, H., Ridgway, E. B.: Calcium entry in response to maintained depolarization of squid axons. J. Physiol. (Lond.)231, 527–548 (1973b)

  4. Batzri, S., Selinger, Z.: Enzyme secretion mediated by the epinephrine β-receptor in rat parotid slices. J. Biol. Chem.248, 356–360 (1973)

  5. Douglas, W. W., Poisner, A. M.: The influence of calcium on the secretory response of the submaxillary gland to acetylcholine or to noradrenaline. J. Physiol. (Lond.)105, 528–541 (1963)

  6. Fatt, P., Ginsborg, B. L.: The ionic requirements for the production of action potentials in crustacean muscle fibres. J. Physiol. (Lond.)142, 516–543 (1958)

  7. Iwatsuki, N., Petersen, O. H.: Acetylcholine-like effects of intracellular calcium application in pancreatic acinar cells. Nature268, 147–149 (1977)

  8. Kanagasuntheram, P., Randle, P. J.: Calcium metabolism and amylase release in rat parotid acinar cells. Biochem. J.160, 547–564 (1976)

  9. Kanno, T., Nishimura, O.: Stimulus-secretion coupling in pancreatic acinar cells: inhibitory effects of calcium removal and manganese addition on pancreozymin-induced amylase release. J. Physiol. (Lond.)257, 309–324 (1976)

  10. Kaufmann, R., Fleckenstein, A.: Ca2+-kompetitive elektromechanische Entkoppelung durch Ni2+- und Co2+-Ionen am Warmblütermyokard. Pflügers Arch.282, 290–297 (1965)

  11. Katz, B., Miledi, R.: The effect of divalent cations on transmission in the squid giant synapse. Publ. Staz. Zool. Napoli37, 303–310 (1969)

  12. Koelz, H. R., Kondo, S., Blum, A. L., Schulz, I.: Calcium ion uptake induced by cholinergic and α-adrenergic stimulation in isolated cells of rat salivary glands. Pflügers Arch.370, 37–44 (1977)

  13. Kohlhardt, M., Bauer, B., Krause, H., Fleckenstein, A.: Selective inhibition of the transmembrane Ca conductivity of mammalian myocardial fibres by Ni, Co and Mn ions. Pflügers Arch.338, 115–123 (1973)

  14. Matthews, E. K., Petersen, O. H., Williams, J. A.: Analysis of tissue amylase output by an automated method. Anal. Biochem.58, 155–160 (1974)

  15. Miledi, R.: Transitter release induced by injection of calcium ions into nerve terminals. Proc. R. Soc. Lond. B183, 421–425 (1973)

  16. Nielsen, S. P., Petersen, O. H.: Transport of calcium in the perfused submandibular gland of the cat. J. Physiol. (Lond.)223, 685–697 (1972)

  17. Nishiyama, A., Petersen, O. H.: Membrane potential and resistance measurement in acinar cells from salivary glands in vitro: effect of acetylcholine. J. Physiol. (Lond.)242, 173–188 (1974)

  18. Petersen, O. H.: Some factors influencing stimulation-induced release of potassium from the cat submandibular gland to fluid perfused through the gland. J. Physiol. (Lond.)208, 431–447 (1970)

  19. Petersen, O. H.: Stimulus-secretion coupling of salivary acinar cells: the role of membrane permeability change, Ca2+ and cyclic AMP. In: Stimulus-secretion coupling in the gastrointestinal tract (R. M. Case and H. Goebell, eds.), pp. 281–293 Lancaster: MTP 1976a

  20. Petersen, O. H.: Electrophysiology of mammalian gland cells. Physiol. Rev.56, 535–577 (1976b)

  21. Petersen, O. H., Iwatsuki, N.: The role of calcium in pancreatic acinar cell stimulus-secretion coupling: an electrophysiological approach. Ann. N.Y. Acad. Sci. (in press, 1977)

  22. Petersen, O. H., Pedersen, G. L.: Membrane effects mediated by alpha- and beta-adrenoceptors in mouse parotid acinar cells. J. Membr. Biol.16, 353–362 (1974)

  23. Petersen, O. H., Ueda, N.: Pancreatic acinar cells: the role of calcium in stimulus-secretion coupling. J. Physiol. (Lond.)254, 583–606 (1976)

  24. Petersen, O. H., Poulsen, J. H., Thorn, N. A.: Secretory potentials, secretory rate and water permeability of the duct system in the cat submandibular gland during perfusion with calcium-free Locke's solution. Acta Physiol. Scand.71, 203–210 (1967)

  25. Petersen, O. H., Gray, T. A., Hall, R. A.: The relationship between stimulation-induced potassium release and amylase secretion in the mouse parotid. Pflügers Arch.369, 207–211 (1977)

  26. Poulsen, J. H.: Acetylcholine-induced transport of Na+ and K+ in the perfused cat submandibular gland. Pflügers Arch.349, 215–220 (1974)

  27. Rossignol, B., Herman, G., Chambaut, A. M., Kerger, G.: The calcium ionophore A 23187 as a probe for studying the role of Ca2+ ions in the mediation of carbachol effects on rat salivary glands: protein secretion and metabolism of phospholipids and glycogen. FEBS Lett.43, 241–246 (1974)

  28. Rossignol, B., Kerger, G., Herman, G., Chambaut-Guérin, A. M., Cahoreau, C.: Function of cholinergic and adrenergic receptors in the control of metabolism and protein secretion in rat salivary glands. In: Hormonal Receptors in Digestive Tract Physiology (S. Bonfils, P. Fromageot, and G. Rosselin, eds), pp. 311–323. Amsterdam: North Holland 1977

  29. Schramm, M., Naim, E.: Adenyl cyclase of rat parotid gland. J. Biol. Chem.245, 3225–3231 (1970)

  30. Schramm, M., Selinger, Z.: Neurotransmitters, receptors, second messengers and responses in parotid gland and pancreas. In: Stimulus-Secretion Coupling in the Gastrointestinal Tract R. M. Case and H. Goebell, eds.), pp. 49–64. Lancaster: MTP 1976

  31. Schultz, G., Hardman, J. G., Schultz, K., Baird, C. E., Sutherland, E. W.: The importance of calcium ions for the regulation of guanosine 3′:5′ cyclic monophosphate levels. Proc. Natl. Acad. Sci. U.S.A.70, 3889–3893 (1973)

  32. Selinger, Z., Eimerl, S., Schramm, M.: A calcium ionophore simulating the action of epinephrine on the α-adrenergic receptor. Proc. Natl. Acad. Sci. U.S.A.71, 128–131 (1974)

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Petersen, O.H., Ueda, N., Hall, R.A. et al. The role of calcium in parotid amylase secretion evoked by excitation of cholinergic, α- andβ-adrenergic receptors. Pflugers Arch. 372, 231–237 (1977). https://doi.org/10.1007/BF01063857

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Key words

  • Parotid
  • Amylase secretion
  • Calcium
  • Manganese
  • α- and β-Adrenoceptor
  • Acetylcholine