Skip to main content
Log in

Regulation of calcium handling by rat parotid acinar cells

  • Invited paper
  • Published:
Molecular and Cellular Biochemistry Aims and scope Submit manuscript

Summary

Salivary gland fluid secretion following neurotransmitter stimulation is Ca2+-dependent. We have studied the control of cellular Ca2+ following secretory stimuli in rat parotid gland acinar cells. After muscarinic-cholinergic receptor activation, cytosolic Ca2+ is elevated 4–5 fold, due to both intracellular Ca2+ pool mobilization and extracellular Ca2+ entry. Fluid movement ensues due to the Ca2+-activated enhancement of membrane permeability to K+ and Cl. Basal cytosolic Ca2+ levels are tightly controlled at ∼150–200 nM through the action of high affinity and high capacity ATP-dependent Ca2+ transporters in the basolateral and endoplasmic reticulum membranes. Activity of these Ca2+ transporters can be modulated to facilitate rapid responsiveness and a sustained fluid secretory response necessary for alimentary function.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Douglas WW Poisner AM: The influence of calcium on the secretory response of the submaxillary gland to acetylcholine or to noradrenaline. J Physiol (Lond) 165:528–541, 1963

    Google Scholar 

  2. Putney Jr JW: Identification of cellular activation mechanisms associated with salivary secretion. Ann Rev Physiol 48:75–88, 1986

    Google Scholar 

  3. Baum BJ: Neurotransmitter control of secretion. J Dent Res 66:628–632, 1987

    Google Scholar 

  4. Streb H, Irvine RF, Berridge MJ, Schulz I: Release of Ca2+ from a non-mitochondrial intracellular store in pancreatic acinar cells by inositol-1,4,5-trisphosphate. Nature 306:67–69, 1983

    Google Scholar 

  5. Joseph SK, Williamson JR: Characteristics of inositol trisphosphate-mediated Ca2− release from permeabilized hepatocytes. J Biol Chem 261:14658–14664, 1986

    Google Scholar 

  6. Irvine RF, Letcher AJ, Lander DJ, Downes CP: Inositol trisphosphates in carbachol-stimulated rat parotid glands. Biochem J 223:237–243, 1984

    Google Scholar 

  7. Putney Jr JW: A model for receptor-regulated calcium entry. Cell Calcium 7:1–12, 1986

    Google Scholar 

  8. Williamson JR, Cooper RH, Hoek JB: The role of calcium in the hormonal regulation of liver metabolism. Biochem Biophys Acta 639:243–295, 1981

    Google Scholar 

  9. Shamoo AE, Ambudkar IS: Regulation of calcium transport in cardiac cells. Can J Physiol Pharmacol 62:9–22, 1984

    Google Scholar 

  10. Carafoli E: Intracellular calcium homeostasis. Ann Rev Biochem 56:395–433, 1987

    Google Scholar 

  11. Helman J, Kuyatt BL, Takuma T, Seligmann B, Baum BJ: ATP-dependent calcium transport in rat parotid basolateral membrane vesicles. Modulation by agents which elevate cyclic AMP. J Biol Chem 261:8919–8923, 1986

    Google Scholar 

  12. Petersen OH, Findlay I, Iwatsuki N, Singh J, Gallacher DV, Fuller CM, Pearson GT, Dunne MJ, Morris AP: Human pancreatic acinar cells: studies of stimulus-secretion coupling. Gastroenterology 89:109–117, 1985

    Google Scholar 

  13. Nauntofte B, Poulsen JH: Effects of Ca2+ and furosemide on Cl transport and O2 uptake in rat parotid acini. Am J Physiol 251:C175-C185, 1986

    Google Scholar 

  14. Melvin JE, Kawaguchi M, Baum BJ, Turner RJ: A muscarinic agonist-stimulated chloride efflux pathway is associated with fluid secretion in rat parotid acinar cells. Biochem Biophys Res Comm 145:754–759, 1987

    Google Scholar 

  15. Mangos JA, Braun G, Hamann KF: Micropuncture study of sodium and potassium excretion in rat parotid saliva. Arch Ges Physiol 291:99–106, 1966

    Google Scholar 

  16. Leslie BA, Landis CA, Butcher FR, Putney Jr JW: Retention of nerve terminals in dispersed parotid acinar cells. Life Sciences 25:1017–1022, 1979

    Google Scholar 

  17. Selinger Z, Naim E, Lasser M: ATP-dependent calcium uptake by microsomal preparations from rat parotid and submaxillary glands. Biochim Biophys Acta 203:326–334

  18. Kanagasuntheram P, Teo TS: Parotid microsomal Ca2+ transport. Biochem J 208:789–794, 1982

    Google Scholar 

  19. Immelman A, Soling H-D: ATP-dependent calcium sequestration and calcium/ATP stoichiometry in isolated microsomes from guinea pig parotid glands. FEBS Lett 162:406–410, 1983

    Google Scholar 

  20. Takuma T, Kuyatt BL, Baum BJ: Calcium transport mechanisms in basolateral membrane-enriched vesicles from rat parotid gland. Biochem J 227:239–245, 1985

    Google Scholar 

  21. Turner RJ, George IN, Baum BJ: Evidence for a Na+/K+/Cl cotransport system in basolateral membrane vesicles from the rabbit parotid. J Membrane Biol 94:143–152, 1986

    Google Scholar 

  22. Bayerdorffer E, Eckhardt L, Haase W, Schulz I: Electrogenic calcium transport in plasma membrane of rat pancreatic acinar cells. J Membrane Biol 84:45–60, 1985

    Google Scholar 

  23. Helman J, Ambudkar IS, Baum BJ: Adrenoreceptor mobilization of calcium in rat submandibular cells. Eur J Pharmacol 143:65–72, 1987

    Google Scholar 

  24. Tsien RY, Pozzan T, Rink TJ: Calcium homeostasis in intact lymphocytes: cytoplasmic free calcium monitored with a new, intracellularly trapped fluorescent indicator. J Cell Biol 94:325–334

  25. Bodner L, Hoopes MT, Gee M, Ito H, Roth GS, Baum BJ: Multiple transduction mechanisms are likely involved in calcium-mediated exocrine secretory events in rat parotid cells. J Biol Chem 258:2774–2777, 1983

    Google Scholar 

  26. Aub DL, Putney Jr JW: Properties of receptor-controlled inositol trisphosphate formation in parotid acinar cells. Biochem J 225:263–266, 1985

    Google Scholar 

  27. Merritt JE, Rink TJ: Rapid increases in cytosolic free calcium in response to muscarinic stimulation of rat parotid acinar cells. J Biol Chem 262:4958–4960, 1987

    Google Scholar 

  28. Maruyama Y, Gallacher DV, Petersen OH: Voltage and Ca2+-activated K+ channel in baso-lateral acinar cell membranes of mammalian salivary glands. Nature 302:827–829, 1983

    Google Scholar 

  29. Muallem S, Schoeffield M, Pandol S, Sachs G: Inositol trisphosphate modification of ion transport in rough endoplasmic reticulum. Proc Natl Acad Sci USA 82:4433–4437, 1985

    Google Scholar 

  30. Martinez JR, Cassity N: Effect of transport inhibitors on secretion by perfused rat submandibular gland. Am J Physiol 245:G711-G716, 1983

    Google Scholar 

  31. Novak I, Young JA: Two independent anion transport systems in rabbit mandibular salivary glands. Pflugers Arch 407:649–656, 1986

    Google Scholar 

  32. Gallacher DV, Petersen OH: Substance P increases membrane conductance in parotid acinar cells. Nature 283:393–395, 1980

    Google Scholar 

  33. Gallacher DV: The electrophysiology of salivary exocrine cells. In: AM Poisner and JM Trifaro (eds) Electrophysiology of the Secretory Cell. Elsevier, New York, 1985, pp 39–60

    Google Scholar 

  34. Landis CA, Putney Jr JW: Calcium and receptor regulation of radiosodium uptake by dispersed rat parotid acinar cells. J Physiol (Lond) 297:369–377, 1979

    Google Scholar 

  35. Ambudkar IS, Melvin JE, Baum BJ: α1-Adrenergic regulation of Cl and Ca2+ fluxes in rat parotid acinar cells in vitro. Pflugers Arch (in press)

  36. Ambudkar IS, Kuyatt BL, Roth GS, Baum BJ: Modification of ATP-dependent Ca2+ transport in rat parotid basolateral membranes during aging. Mech Ageing Develop 43:45–60, 1988

    Google Scholar 

  37. Ambudkar IS, Baum BJ: ATP dependent Ca2+ transport in rat parotid basolateral membrane vesicles is modulated by membrane potential. J Membrane Biol 102:59–69, 1988

    Google Scholar 

  38. Baum BJ, Ambudkar IS, Horn VJ: Evidence that ATP-dependent Ca2+-transport in rat parotid microsomal membranes requires charge compensation. Biochem J (in press)

  39. Case RM: The role of Ca2+ stores in secretion. Cell Calcium 5:89–110, 1984

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Baum, B.J., Ambudkar, I.S. Regulation of calcium handling by rat parotid acinar cells. Mol Cell Biochem 82, 67–73 (1988). https://doi.org/10.1007/BF00242518

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00242518

Key words

Navigation