Comprehensive Physiology Wiley Online Library
For Librarians For Authors Editors About

Calcium Signaling System in Salivary Glands

James W. Jr. Putney

10.1002/cphy.cp060303

Source: Supplement 18: Handbook of Physiology, The Gastrointestinal System, Salivary, Gastric, Pancreatic, and Hepatobiliary Secretion

Originally published: 1989

Published online: January 2011

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Stimulus‐Permeability Coupling in Salivary Glands
2 Phosphoinositides and Salivary Receptor Mechanisms
2.1 Phosphoinositide Turnover in Salivary Glands
2.2 Pathways of Phosphoinositide Turnover in Salivary Glands
2.3 Phosphoinositides and Intracellular Calcium Release
2.4 Mechanism of Action of 1,4,5‐IP3
2.5 Calcium Entry
2.6 Capacitative Calcium Entry in Parotid Gland
3 Conclusions
Figure 1.

Efflux of 86Rb from salivary gland. Ordinate values represent apparent first‐order rate coefficients (X100%). Agonist (i.e., acetylcholine) is present from 20 to 40 min. Solid line, Ca2+ present throughout. Dotted line, Ca2+ absent but restored from 30 to 40 min.

From Putney 65
Figure 2.

Structures of phosphatidylinositol (PI), phosphatidylinositol‐4‐phosphate (PIP), and phosphatidylinositol‐4,5‐bisphosphate (PIP2).
Figure 3.

Formation of [3H]inositol phosphates in parotid acinar cells during initial 60 s after addition of 10‐4 M methacholine. Closed circles, inositol monophosphate; open circles, inositol bisphosphate; open triangles, inositol trisphosphate. Values are means ± SE of 4 experiments. Control values did not change appreciably over 60‐s period.

From Aub and Putney 3
Figure 4.

Time course of inositol trisphosphate (IP3)‐stimulated Ca2+ mobilization. Isolated parotid acinar cells were permeabilized with saponin. CaCl2 was added and cells were allowed to reequilibrate, after which inositol‐1,4,5‐trisphosphate 1,4,5‐IP3) was added (t = 1 min). Change in quin 2 fluorescence was monitored as an indicator of changing free [Ca2+]. Excess Ca2+ was added after response was completed, followed by alkaline ethylene glycol‐bis(β‐aminoethylether)‐N,N'‐tetraacetic acid (EGTA) for calibration purposes. Representative traces for 3 concentrations of IP3 are superimposed; 0.3 μM, 1 μM, and 3 μM IP3 produced similarly graded increases in fluorescence.

From Aub 2
Figure 5.

Capacitative model for receptor regulation of Ca2+ release and entry. Agonist (Ag) binding to its receptor (RA) leads to breakdown of phosphatidylinositol‐4,5‐bisphosphate (PIP2) into diglyceride (DG) and inositol‐1,4,5‐trisphosphate 1,4,5‐IP3). 1,4,5‐IP3 binds to a receptor (R1) on the receptor‐regulated pool, presumably an endoplasmic reticulum component, which activates Ca2+ discharge to the cytosol and the Ca2+‐release phase of the response. Decrease in Ca2+ content of the pool relieves an inhibitory constraint on a direct pathway for Ca2+ to enter the pool from the extracellular space. With continued presence of 1,4,5‐IP3, Ca2+ continues down its concentration gradient to cytosol, resulting in a sustained Ca2+‐entry phase of the response.

From Putney 67


Figure 1.

Efflux of 86Rb from salivary gland. Ordinate values represent apparent first‐order rate coefficients (X100%). Agonist (i.e., acetylcholine) is present from 20 to 40 min. Solid line, Ca2+ present throughout. Dotted line, Ca2+ absent but restored from 30 to 40 min.

From Putney 65


Figure 2.

Structures of phosphatidylinositol (PI), phosphatidylinositol‐4‐phosphate (PIP), and phosphatidylinositol‐4,5‐bisphosphate (PIP2).



Figure 3.

Formation of [3H]inositol phosphates in parotid acinar cells during initial 60 s after addition of 10‐4 M methacholine. Closed circles, inositol monophosphate; open circles, inositol bisphosphate; open triangles, inositol trisphosphate. Values are means ± SE of 4 experiments. Control values did not change appreciably over 60‐s period.

From Aub and Putney 3


Figure 4.

Time course of inositol trisphosphate (IP3)‐stimulated Ca2+ mobilization. Isolated parotid acinar cells were permeabilized with saponin. CaCl2 was added and cells were allowed to reequilibrate, after which inositol‐1,4,5‐trisphosphate 1,4,5‐IP3) was added (t = 1 min). Change in quin 2 fluorescence was monitored as an indicator of changing free [Ca2+]. Excess Ca2+ was added after response was completed, followed by alkaline ethylene glycol‐bis(β‐aminoethylether)‐N,N'‐tetraacetic acid (EGTA) for calibration purposes. Representative traces for 3 concentrations of IP3 are superimposed; 0.3 μM, 1 μM, and 3 μM IP3 produced similarly graded increases in fluorescence.

From Aub 2


Figure 5.

Capacitative model for receptor regulation of Ca2+ release and entry. Agonist (Ag) binding to its receptor (RA) leads to breakdown of phosphatidylinositol‐4,5‐bisphosphate (PIP2) into diglyceride (DG) and inositol‐1,4,5‐trisphosphate 1,4,5‐IP3). 1,4,5‐IP3 binds to a receptor (R1) on the receptor‐regulated pool, presumably an endoplasmic reticulum component, which activates Ca2+ discharge to the cytosol and the Ca2+‐release phase of the response. Decrease in Ca2+ content of the pool relieves an inhibitory constraint on a direct pathway for Ca2+ to enter the pool from the extracellular space. With continued presence of 1,4,5‐IP3, Ca2+ continues down its concentration gradient to cytosol, resulting in a sustained Ca2+‐entry phase of the response.

From Putney 67
References
 1. Abdel‐Latif, A. A., R. A. Akhtar, and J. N. Hawthorne. Acetylcholine increases the breakdown of triphosphoinositide of rabbit iris muscle prelabelled with [32P]phosphate. Biochem. J. 162: 61-73, 1977.
 2. Aub, D. L. Role of Inositol Phosphates in Stimulus‐Response Coupling. Richmond: Virginia Commonwealth University, 1985. PhD thesis.
 3. Aub, D. L., and J. W. Putney,Jr. Metabolism of inositol phosphates in parotid cells: implications for the pathways of the phosphoinositide effect and for the possible messenger role of inositol trisphosphate. Life Sci. 23: 1347-1355, 1984.
 4. Batty, I. R., S. R. Nahorski, and R. F. Irvine. Rapid formation of inositol 1,3,4,5‐tetrakisphosphate following muscarinic receptor stimulation of rat cerebral cortical slices. Biochem. J. 232: 211-215, 1985.
 5. Batzri, S., A. Amsterdam, Z. Selinger, I. Ohad, and M. Schramm. Epinephrine‐induced vacuole formation in parotid gland cells and its independence of the secretory process. Proc. Natl. Acad. Sci. USA 68: 121-123, 1971.
 6. Batzri, S., Z. Selinger, and M. Schramm. Potassium ion release and enzyme secretion: adrenergic regulation by α‐ and β‐receptors. Science Wash. DC 174: 1029-1031, 1971.
 7. Batzri, S., Z. Selinger, M. Schramm, and M. R. Robinovitch. Potassium release mediated by the epinephrine α‐receptor in rat parotid slices. Properties and relation to enzyme secretion. J. Biol. Chem. 248: 361-368, 1973.
 8. Berridge, M. J. Relationship between calcium and the cyclic nucleotides in ion secretion. In: Mechanisms of Intestinal Secretion, edited by H. J. Binder. New York: Liss, 1979, p. 65-81. (Kroc Found. Ser., vol. 12.).
 9. Berridge, M. J. Rapid accumulation of inositol trisphosphate reveals that agonists hydrolyze polyphosphoinositides instead of phosphatidylinositol. Biochem. J. 212: 849-858, 1983.
 10. Berridge, M. J. Inositol trisphosphate and diacylglycerol as second messengers. Biochem. J. 220: 345-360, 1984.
 11. Berridge, M. J., R. M. C. Dawson, C. P. Downes, J. P. Heslop, and R. F. Irvine. Changes in the levels of inositol phosphates following agonist‐dependent hydrolysis of membrane phosphoinositides. Biochem. J. 212: 473-482, 1983.
 12. Berridge, M. J., and R. F. Irvine. Inositol trisphosphate, a novel second messenger in cellular signal transduction. Nature Land. 312: 315-321, 1984.
 13. Bogart, B. I., and J. Picarelli. Agonist‐induced secretions and potassium release from rat submandibular gland slices. Am. J. Physiol. 235 (Cell Physiol. 4): C256-C268, 1978.
 14. Bolton, T. B. Mechanisms of action of transmitters and other substances on smooth muscle. Physiol. Rev. 59: 606-718, 1979.
 15. Burgess, G. M., R. F. Irvine, M. J. Berridge, J. S. McKinney, and J. W. Putney,Jr. Actions of inositol phosphates on Ca2+ pools in guinea‐pig hepatocytes. Biochem. J. 224: 741-746, 1984.
 16. Burgess, G. M., J. S. McKinney, R. F. Irvine, and J. W. Putney,Jr. Inositol 1,4,5‐trisphosphate and inositol 1,3,4‐trisphosphate formation in Ca2+‐mobilizing hormone‐activated cells. Biochem. J. 232: 237-243, 1985.
 17. Butcher, F. R. The role of calcium and cyclic nucleotides in α‐amylase release from slices of rat parotid: studies with the divalent cation ionophore A‐23187. Metabolism 24: 409-418, 1975.
 18. Butcher, F. R. The calcium requirement for stimulation of rubidium efflux from isolated rat parotid acinar cells by carbachol. Life Sci. 24: 1979-1982, 1979.
 19. Butcher, F. R., P. A. McBride, and L. Rudich. Cholinergic regulation of cyclic nucleotide levels, amylase release and K+ efflux from rat parotid glands. Mol. Cell. Endocrinol. 5: 243-254, 1976.
 20. Butcher, F. R., and J. W. Putney,Jr. Regulation of parotid gland function by cyclic nucleotides and calcium. In: Advances in Cyclic Nucleotide Research, edited by P. Greengard and A. Robison. New York: Raven, 1980, vol. 13, p. 215-249.
 21. Butcher, F. R., L. Rudich, C. Emler, and M. Nemerovski. Adrenergic regulation of cyclic nucleotide levels, amylase release, and potassium efflux in rat parotid gland. Mol. Pharmacol. 12: 862-870, 1976.
 22. Case, R. M. Synthesis, intracellular transport and discharge of exportable proteins in the pancreatic acinar cell and other cells. Biol. Rev. 53: 211-354, 1978.
 23. Casteels, R., and G. Droogmans. Exchange characteristics of the noradrenaline‐sensitive calcium store in vascular smooth muscle cells of rabbit ear artery. J. Physiol. Lond. 317: 263-279, 1981.
 24. Dawson, H. The effect of some metabolic poisons on the permeability of the rabbit erythrocyte to potassium. J. Cell. Comp. Physiol. 18: 173-185, 1941.
 25. Devine, C. E., A. V. Somlyo, and A. P. Somlyo. Sarcoplasmic reticulum and excitation‐contraction coupling in mammalian smooth muscle. J. Cell Biol. 52: 690-718, 1972.
 26. Downes, C. P., and M. M. Wusteman. Breakdown of polyphosphoinositides and not phosphatidylinositol accounts for muscarinic agonist‐stimulated inositol phospholipid metabolism in rat parotid glands. Biochem. J. 216: 633-640, 1983.
 27. Exton, J. H. Mechanisms involved in α‐adrenergic phenomena. Am. J. Physiol. 248 (Endocrinol. Metab.11): E633-E647, 1985.
 28. Fairhurst, A. S., M. L. Whittaker, and F. J. Ehlert. Interactions of D‐600 (methoxyverapamil) and local anesthetics with rat brain α‐adrenergic and muscarinic receptors. Biochem. Pharmacol. 29: 155-162, 1980.
 29. Gallacher, D. V., and O. H. Petersen. Substance P increases membrane conductance in parotid acinar cells. Nature Lond. 283: 393-395, 1980.
 30. Gardos, G. The function of calcium in the potassium permeability of human erythrocytes. Biochim. Biophys. Acta 30: 653-654, 1958.
 31. Godfraind, J. M., H. Kawamura, K. Krnjević, and R. Pumain. Actions of dinitrophenol and some other metabolic inhibitors on cortical neurones. J. Physiol. Lond. 215: 199-222, 1971.
 32. Godfraind, J. M., K. Krnjević, and R. Pumain. Unexpected features of the action of dinitrophenol on cortical neurones. Nature Lond. 228: 562-564, 1970.
 33. Henriques, V., and S. L. Orskov. Untersuchungen über die Schwankungen des Kationengehalts der roten Blutkörperchen. II. Änderung des Kaliumgehaltz der Blutkörperchen bei Bleiv‐ergiftung. Skand. Arch. Physiol. 74: 78-85, 1936.
 34. Heslop, J. P., R. F. Irvine, A. H. Tashjian, and M. J. Berridge. Inositol tetrakis‐ and pentakisphosphates in GH4 cells. J. Exp. Biol. 119: 395-401, 1985.
 35. Hokin, L. E. Effects of calcium omission on acetylcholine‐stimulated amylase secretion and phospholipid synthesis in pigeon pancreas slices. Biochim. Biophys. Acta 115: 219-221, 1966.
 36. Hokin, L. E. Receptors and phosphoinositide‐generated second messengers. Annu. Rev. Biochem. 54: 205-235, 1985.
 37. Hokin, L. E., and A. L. Sherwin. Protein secretion and phosphate turnover in the phospholipids in salivary glands in vitro. J. Physiol. Lond. 135: 18-29, 1957.
 38. Hokin, M. R., and L. E. Hokin. Effects of acetylcholine on phospholipids in the pancreas. J. Biol. Chem. 209: 549-558, 1954.
 39. Irvine, R. F., E. A. Anggård, A. J. Letcher, and C. P. Downes. Metabolism of inositol 1,4,5‐trisphosphate and inositol 1,3,4‐trisphosphate in rat parotid glands. Biochem. J. 229: 505-511, 1985.
 40. Irvine, R. F., A. J. Letcher, D. J. Lander, and C. P. Downes. Inositol trisphosphates in carbachol‐stimulated rat parotid glands. Biochem. J. 223: 237-243, 1984.
 41. Iwatsuki, N., and O. H. Petersen. Does exocytosis influence membrane resistance in mouse parotid acini? J. Physiol. Lond. 292: 81P-82P, 1979.
 42. Kanagasuntheram, P., and P.J. Randle. Calcium metabolism and amylase release in rat parotid acinar cells. Biochem. J. 160: 547-564, 1976.
 43. Kirk, C. J., J. A. Creba, C. P. Downes, and R. H. Michell. Hormone‐stimulated metabolism of inositol lipids and its relationship to hepatic receptor function. Biochem. Soc. Trans. 9: 377-379, 1981.
 44. Koelz, H. R., S. Kondo, A. L. Blum, and I. Schulz. Calcium ion uptake induced by cholinergic and α‐adrenergic stimulation in isolated cells of rat salivary glands. Pfluegers Arch. 370: 37-44, 1977.
 45. Krnjević, K., and A. Lisiewicz. Injections of calcium ions into spinal motoneurones. J. Physiol. Lond. 225: 363-390, 1972.
 46. Landis, C. A., and J. W. Putney,Jr. Calcium and receptor regulation of radiosodium uptake by dispersed rat parotid acinar cells. J. Physiol. Lond. 297: 369-377, 1979.
 47. Lew, V. L., and H. G. Ferreira. Ca transport and the properties of a Ca‐sensitive K channel in red cell membranes. Cur. Top. Membr. Transp. 10: 217-277, 1978.
 48. Lew, V. L. (editor). Ca‐activated K+ channels. Cell Calcium 4: 321-517, 1983.
 49. Mangos, J. A. Role of cGMP in isolated rat parotid acinar cells. J. Dent. Res. 57: 989-994, 1978.
 50. Marier, S. H., J. W. Putney, Jr., and C. M. Van de Walle. Control of calcium channels by membrane receptors in the rat parotid gland. J. Physiol. Lond. 279: 141-151, 1978.
 51. Martinez, J. R., and D. O. Quissel. Potassium release from the rat submaxillary gland in vitro. II. Induction by parasympathomimetic secretagogues. J. Pharmacol. Exp. Ther. 199: 518-525, 1976.
 52. Martinez, J. R., D. O. Quissel, and M. Giles. Potassium release from the rat submaxillary gland in vitro. I. Induction by catecholamines. J. Pharmacol. Exp. Ther. 198: 385-394, 1976.
 53. Meech, R. W. Intracellular calcium and the control of membrane permeability. In: Calcium in Biological Systems, edited by C. J. Duncan. Cambridge, UK: Cambridge Univ. Press, 1976, p. 161-191.
 54. Meech, R. W. Calcium‐dependent potassium activation in nervous tissues. Annu. Rev. Biophys. Bioeng. 7: 1-18, 1978.
 55. Michell, R. H. Inositol phospholipids and cell surface receptor function. Biochim. Biophys. Acta 415: 81-147, 1975.
 56. Miller, B. E., and D. L. Nelson. Calcium fluxes in isolated acinar cells from rat parotid: the effect of adrenergic and cholinergic stimulation. J. Biol. Chem. 252: 3629-3636, 1977.
 57. Miller, B., D. L. Nelson, and F. R. Butcher. Tetracaine blocks the responses of isolated acinar cells from rat parotid to carbachol but not to substance P. Biochim. Biophys. Acta 587: 446-454, 1979.
 58. Oron, Y., M. Lowe, and Z. Selinger. Involvement of the α‐adrenergic receptor in the phospholipid effect in rat parotid. FEBS Lett. 34: 198-200, 1973.
 59. Pedersen, G. L., and O. H. Petersen. Membrane potential measurement in parotid acinar cells. J. Physiol. Lond. 234: 217-227, 1973.
 60. Petersen, O. H., and G. L. Pedersen. Membrane effects mediated by alpha‐ and beta‐adrenoceptors in mouse parotid acinar cells. J. Membr. Biol. 16: 353-362, 1974.
 61. Poggioli, J., and J. W. Putney,Jr. Net calcium fluxes in rat parotid acinar cells: Evidence for a hormone‐sensitive calcium pool in or near the plasma membrane. Pfluegers Arch. 392: 239-243, 1982.
 62. Putney, J. W.,Jr. Biphasic modulation of potassium release in rat parotid gland by carbachol and phenylephrine. J. Pharmacol. Exp. Ther. 198: 375-384, 1976.
 63. Putney, J. W.,Jr. Stimulation of 45Ca influx in rat parotid gland by carbachol. J. Pharmacol. Exp. Ther. 199: 526-537, 1976.
 64. Putney, J. W.,Jr. Muscarinic, α‐adrenergic and peptide receptors regulate the same calcium influx sites in the parotid gland. J. Physiol. Lond. 268: 139-149, 1977.
 65. Putney, J. W.,Jr. Stimulus‐permeability coupling: role of calcium in the receptor regulation of membrane permeability. Pharmacol. Rev. 30: 209-245, 1978.
 66. Putney, J. W.,Jr. Identification of cellular activation mechanisms associated with salivary secretion. Annu. Rev. Physiol. 48: 75-88, 1986.
 67. Putney, J. W.,Jr. A model for receptor‐regulated calcium entry. Cell Calcium 7: 1-12, 1986.
 68. Putney, J. W.,Jr., G. M. Burgess, S. P. Halenda, J. S. McKinney, and R. P. Rubin. Effects of secretagogues on [32P]phosphatidylinositol 4,5‐bisphosphate metabolism in the exocrine pancreas. Biochem. J. 212: 483-488, 1983.
 69. Putney, J. W.,Jr., B. A. Leslie, and S. H. Marier. Calcium and the control of potassium efflux in the sublingual gland. Am. J. Physiol. 235 (Cell Physiol. 4): C128-C135, 1978.
 70. Putney, J. W.,Jr., and R. J. Parod. Calcium‐mediated effects of carbachol on cation pumping and Na uptake in rat parotid gland slices. J. Pharmacol. Exp. Ther. 205: 449-458, 1978.
 71. Putney, J. W.,Jr., and C. M. Van de Walle. The relationship between muscarinic receptor binding and ion movements in the rat parotid gland. J. Physiol. Lond. 299: 521-531, 1980.
 72. Putney, J. W.,Jr., C. M. Van de Walle, and B. A. Leslie. Receptor control of calcium influx in parotid acinar cells. Mol. Pharmacol. 14: 1046-1053, 1978.
 73. Putney, J. W.,Jr., and S. J. Weiss. Relationship between receptors, calcium channels and responses in exocrine gland cells. In: Methods in Cell Biology. Basic Mechanisms of Cellular Secretion, edited by D. Prescott and A. R. Hand. New York: Academic, 1981, vol. 23, p. 503-511.
 74. Quissell, D. O. Secretory response of dispersed rat submandibular cells. I. Potassium release. Am. J. Physiol. 238 (Cell Physiol.7): C90-C98, 1980.
 75. Ringer, S. A further contribution regarding the influence of the different constituents of the blood on the contraction of the heart. J. Physiol. Lond. 4: 29-42, 1883.
 76. Roberts, M. L., N. Iwatsuki, and O. H. Petersen. Parotid acinar cells: ionic dependence of acetylcholine‐evoked membrane potential changes. Pfluegers Arch. 376: 159-167, 1978.
 77. Roberts, M. L., and O. H. Petersen. Membrane potential and resistance changes induced in salivary gland acinar cells by microiontophoretic application of acetylcholine and adrenergic agonists. J. Membr. Biol. 39: 297-312, 1978.
 78. Rubin, R. P. Calcium and Cellular Secretion. New York: Plenum, 1982.
 79. Rudich, L., and F. R. Butcher. Effect of substance P and eledoisin on K+ efflux, amylase release and cyclic nucleotide levels in slices of rat parotid gland. Biochim. Biophys. Acta 444: 704-711, 1976.
 80. Sandow, A. Excitation‐contraction coupling in skeletal muscle. Pharmacol. Rev. 17: 265-320, 1965.
 81. Schramm, M., and Z. Selinger. The functions of cyclic AMP and calcium as alternative second messengers in parotid gland and pancreas. J. Cyclic Nucleotide Res. 1: 181-192, 1975.
 82. Selinger, Z., S. Batzri, S. Eimerl, and M. Schramm. Calcium and energy requirements for K+ release mediated by the epinephrine α‐receptor in rat parotid slices. J. Biol. Chem. 248: 369-372, 1973.
 83. Selinger, Z., S. Eimerl, and M. Schramm. A calcium iono‐phore simulating the action of epinephrine on the α‐adrenergic receptor. Proc. Natl. Acad. Sci. USA 71: 128-131, 1974.
 84. Slack, B. E., J. E. Bell, and D. J. Benos. Inositol‐1,4,5‐trisphosphate injection mimics fertilization potentials in sea urchin eggs. Am. J. Physiol. 250 (Cell Physiol. 19): C340-C344, 1986.
 85. Spät, A., P. G. Bradford, J. S. McKinney, R. P. Rubin, and J. W. Putney,Jr. A saturable receptor for [32P]inositol‐,4,5)trisphosphate in hepatocytes and neutrophils. Nature Lond. 319: 514-516, 1986.
 86. Spearman, T. N., and E. T. Pritchard. Potassium release from submandibular salivary gland in vitro. Biochim. Biophys. Acta 466: 198-207, 1977.
 87. Storey, D. J., S. B. Shears, C. J. Kirk, and R. H. Michell. Stepwise enzymatic dephosphorylation of inositol‐1,4,5‐trisphosphate to inositol in liver. Nature Lond. 312: 374-376, 1984.
 88. Streb, H., E. Bayerdörffer, W. Haase, R. F. Irvine, and I. Schultz. Effect of inositol‐1,4,5‐trisphosphate on isolated subcellular fractions of rat pancreas. J. Membr. Biol. 81: 241-253, 1984.
 89. Streb, H., R. F. Irvine, M. J. Berridge, and I. Schulz. Release of Ca2+ from a nonmitochondrial intracellular store in pancreatic acinar cells by inositol‐1,4,5‐trisphosphate. Nature Lond. 306: 67-69, 1983.
 90. Takemura, H. Changes in cytosolic free calcium concentration in isolated rat parotid cells by cholinergic and α‐adrenergic agonists. Biochem. Biophys. Res. Commun. 131: 1048-1055, 1985.
 91. Tsien, R. Y., T. Pozzan, and T. J. Rink. Calcium homeostasis in intact lymphocytes: cytoplasmic free calcium monitored with a new, intracellularly trapped fluorescent indicator. J. Cell Biol. 94: 325-334, 1982.
 92. Ueda, T., S. H. Church, M. W. Noel, and D. L. Gill. Influence of inositol 1,4,5‐trisphosphate and guanine nucleotides on intracellular calcium release within the N1E‐115 neuronal cell line. J. Biol. Chem. 216: 3184-3192, 1986.
 93. Weiss, S. J., J. S. McKinney, and J. W. Putney,Jr. Receptor‐mediated net breakdown of phosphatidylinositol 4,5‐bisphosphate in parotid acinar cells. Biochem. J. 206: 555-560, 1982.
 94. Weiss, S. J., and J. W. Putney,Jr. The relationship of phosphatidylinositol turnover to receptors and calcium‐ion channels in rat parotid acinar cells. Biochem. J. 194: 463-468, 1981.
 95. Whittam, R. Control of membrane permeability to potassium in red blood cells (Abstract). Nature Lond. 219: 610, 1968.
 96. Wilbrandt, W. A relation between the permeability of the red cell and its metabolism. Trans. Faraday Soc. 33: 956-959, 1937.

Contact Editor

Submit a note to the editor about this article by filling in the form below.

* Required Field

Article Title: Calcium Signaling System in Salivary Glands
 

How to Cite

James W. Jr. Putney. Calcium Signaling System in Salivary Glands. Compr Physiol 2011, Supplement 18: Handbook of Physiology, The Gastrointestinal System, Salivary, Gastric, Pancreatic, and Hepatobiliary Secretion: 51-61. First published in print 1989. doi: 10.1002/cphy.cp060303