Advertisement

The Journal of Membrane Biology

, Volume 112, Issue 2, pp 159–167 | Cite as

Intestinal secretagogues increase cytosolic free Ca2+ concentration and K+ conductance in a human intestinal epithelial cell line

  • Toshihiko Yada
  • Shigetoshi Oiki
  • Shunji Ueda
  • Yasunobu Okada
Articles

Summary

A human intestinal epithelial cell line (Intestine 407) is known to retain receptors for intestinal secretagogues such as acetylcholine (ACh), histamine, serotonin (5-HT) and vasoactive intestinal peptide (VIP). The cells were also found to possess separate receptors for secretin and ATP, the stimulation of which elicited transient hyperpolarizations coupled to decreased membrane resistances. These responses were reversed in polarity at the K+ equilibrium potential. The hyperpolarizing responses to six agonists were reversibly inhibited by quinine or quinidine. By means of Ca2+-selective microelectrodes, increases in the cytosolic free Ca2+ concentration were observed in response to individual secretagogues. The time course of Ca2+ responses coincided with that of hyperpolarizing responses. The responses to ACh and 5-HT were abolished by a reduction in the extracellular Ca2+ concentration down to pCa 7 or by application of Co2+. Thus, in Intestine 407 cells, not only the intestinal secretagogues, which are believed to act via increased cytosolic Ca2+ (ACh, 5-HT and histamine), but also those which elevate cyclic AMP (VIP, secretin and ATP) induce increases in cytosolic Ca2+, thereby activating the K+ conductance. It is likely that the origin of increased cytosolic Ca2+ is mainly extracellular for ACh- and 5-HT-induced responses, whereas histamine, VIP, secretin and ATP mobilize Ca2+ from the internal compartment.

Key Words

intestinal secretagogues receptor cytosolic Ca · K channel intestinal epithelial cell 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Armstrong, C.M. 1971. Interaction of tetraethylammonium ion derivatives with the potassium channels of giant axons.J. Gen. Physiol. 55:413–437Google Scholar
  2. Baker, P.F., Meves, H., Ridgway, E.B. 1973. Effects of manganese and other agents on the calcium uptake that follows depolarization of squid axons.J. Physiol. (LOndon) 231:511–526Google Scholar
  3. Binder, H.J., Lemp, G.F., Gardner, J.D. 1980. Receptors for vasoactive intestinal peptide and secretin on small intestinal epithelial cells.Am. J. Physiol. 238:G190-G196PubMedGoogle Scholar
  4. Bolton, J.E., Field, M. 1977. Ca ionophore-stimulated ion secretion in rabbit ileal mucosa: Relation to actions of cyclic 3′,5′-AMP and carbamylcholine.J. Membrane Biol. 35:159–174Google Scholar
  5. Cartwright, C.A., McRoberts, J.A., Mandel, K.G., Dharmsathaphorn, K. 1985. Synergistic action of cyclic adenosine monophosphate- and calcium-mediated chloride secretion in a colonic epithelial cell line.J. Clin. Invest. 76:1837–1842PubMedGoogle Scholar
  6. Chang, E.B., Brown, D.R., Wang, N.S., Field, M. 1986. Secretagogue-induced changes in membrane calcium permeability in chicken and chinchilla ileal mucosa.J. Clin. Invest. 78:281–287PubMedGoogle Scholar
  7. Cooke, H.J. 1987. Neural and humoral regulation of small intestinal electrolyte transport.In: Physiology of Gastrointestinal Tract. L.R. Johnson, editor. pp. 1307–1350. Raven, New YorkGoogle Scholar
  8. DeRiemer, S.A., Strong, J.A., Albert, K.A., Greengard, P., Kaczmarek, L.K. 1985. Enhancement of calcium current inAplysia neurones by phorbol ester and protein kinase C.Nature (London) 313:313–316Google Scholar
  9. Dharmsathaphorn, K., Harms, V., Yamashiro, D.H., Hughes, R.J., Binder, H.J., Wright, E.M. 1983. Preferential binding of vasoactive intestinal polypeptide to basolateral membrane of rat and rabbit enterocytes.J. Clin. Invest. 71:27–35PubMedGoogle Scholar
  10. Dharmsathaphorn, K., Pandol, S.J. 1986. Mechanism of chloride secretion induced by carbachol in a colonic epithelial cell line.J. Clin. Invest. 77:348–354PubMedGoogle Scholar
  11. Donowitz, M. 1983. Ca2+ in the control of active Na and Cl transport: Involvement in neurohumoral action.Am. J. Physiol. 245:G165-G177Google Scholar
  12. Donowitz, M., Welsh, M.J. 1987. Regulation of mammalian small intestinal electrolyte secretion.In: Physiology of Gastrointestinal Tract. L.R. Johnson, editor. pp. 1351–1388 Raven, New YorkGoogle Scholar
  13. Endo, M. 1975. Mechanisms of action of caffeine on the sarcoplasmic reticulum of skeletal muscle.Proc. Jpn. Acad. 51:479–484Google Scholar
  14. Findlay, I., Dunne, M.J., Ullrich, S., Wollheim, C.B., Petersen, O.H. 1985. Quinine inhibits Ca2+-independent K+ channels whereas tetraethylammonium inhibits Ca2+-activated K+ channels in insulin-secreting cells.FEBS Lett. 185:4–8PubMedGoogle Scholar
  15. Frizzell, R.A. 1977. Active chloride secretion by rabbit colon: Calcium dependent stimulation by ionophore A23187.J. Membrane Biol. 35:175–187Google Scholar
  16. Gaginella, T.S., Phillips, S.F., Dozois, R.R., Go, V.L.W. 1978. Stimulation of adenylate cyclase in homogenates of isolated intestinal epithelial cells from hamsters. Effects of gastrointestinal hormones, prostaglandins, and deoxycholic and ricinoleic acids.Gastroenterology 74:11–15PubMedGoogle Scholar
  17. Hagiwara, S., Takahashi, K. 1967. Surface density of calcium ions and calcium spikes on the barnacle muscle fiber membrane.J. Gen. Physiol. 50:583–601PubMedGoogle Scholar
  18. Hardcastle, J., Hardcastle, P.T. 1986. The involvement of basolateral potassium channels in the intestinal response to secretagogues in the rat.J. Physiol. (London) 379:331–345Google Scholar
  19. Hardcastle, J., Hardcastle, P.T. 1987. The secretory actions of histamine in rat small intestine.J. Physiol. (London) 388:521–532Google Scholar
  20. Hardcastle, J., Hardcastle, P.T., Redfern, J.S. 1981. Action of 5-hydroxytryptamine on intestinal ion transport in the rat.J. Physiol. (London) 320:41–55Google Scholar
  21. Hazama, A., Okada, Y. 1988. Ca2+ sensitivity of volume-regulatory K+ and Cl channels in cultured human epithelial cells.J. Physiol. (London) 402:687–702Google Scholar
  22. Hazama, A., Yada, T., Okada, Y. 1985. HeLa cells have histamine H1-receptors which mediate activation of the K+ conductance.Biochim. Biophys. Acta 845:249–253CrossRefPubMedGoogle Scholar
  23. Henle, G., Deinhardt, F. 1957. The establishment of strains of human cells in tissue culture.J. Immunol. 79:54–59PubMedGoogle Scholar
  24. Hughes, J.M., Murad, F., Chang, B., Guerrant, R.L. 1978. Role of cyclic GMP in the action of heat-stable enterotoxin ofEscherichia coli.Nature (London) 271:755–756Google Scholar
  25. Ilundain, A., O'Brien, J.A., Burton, K.A., Sepulveda, F.V. 1987. Inositol trisphosphate and calcium mobilisation in permeabilised enterocytes.Biochim. Biophys. Acta 896:113–116PubMedGoogle Scholar
  26. Itoh, A., Ueda, S., Okada, Y. 1989. Chloride current activation induced by intestinal secretagogues in an intestinal epithelial cell line.Jpn. J. Physiol. (Abstr.) (in press) Google Scholar
  27. Juzu, H.A., Holdsworth, E.S. 1980. New evidence for the role of cyclic AMP in the release of mitochondrial calcium.J. Membrane Biol. 52:185–186Google Scholar
  28. Kelepouris, E., Agus, Z.S., Civan, M.M. 1985. Intracellular calcium activity in split frog skin epithelium: Effect of cAMP.J. Membrane Biol. 88:113–121Google Scholar
  29. Klaeveman, H.L., Conlon, T.P., Levy, A.G., Garoner, J.D. 1975. Effects of gastrointestinal hormones on adenylate cyclase activity in human jejunal mucosa.Gastroenterology 68:667–675PubMedGoogle Scholar
  30. Korman, L.Y., Lemp, G.F., Jackson, M.J., Gardner, J.D. 1982. Mechanism of action of ATP on intestinal epithelial cells. Cyclic AMP-mediated stimulation of active ion transport.Biochim. Biophys. Acta 721:47–54PubMedGoogle Scholar
  31. Kuno, M., Gardner, P. 1987. Ion channels activated by inositol 1,4,5-trisphosphate in plasma membrane of human T-lymphocytes.Nature (London) 326:301–304Google Scholar
  32. Laburthe, M., Mangeat, P., Marchis-Mouren, G., Rosselin, G. 1979a. Activation of cyclic AMP-dependent protein kinases by vasoactive intestinal peptide (VIP) in isolated intestinal epithelial cells from rat.Life Sci. 25:1931–1938PubMedGoogle Scholar
  33. Laburthe, M., Prieto, J.C., Amiranoff, B., Dupont, C., Hui Bon Hoa, D., Rosselin, G. 1979b. Interaction of vasoactive intestinal peptide with isolated intestinal epithelial cells from rat. 2. Characterization and structural requirements of the stimulatory effect of vasoactive intestinal peptide on production of 3′:5′-monophosphate.Eur. J. Biochem. 96:239–248PubMedGoogle Scholar
  34. Lee, C.O., Taylor, A., Windhager, E.E. 1980. Cytosolic calcium ion activity in epithelial cells ofNecturus, kidney.Nature (London) 287:859–861Google Scholar
  35. Mandel, K.G., McRoberts, J.A., Beuerlein, G., Foster, E.S., Dharmsathaphorn, K., 1986. Ba2+ inhibition of VIP- and A23187-stimulated Cl secretion by T84 cell monolayer.Am. J. Physiol. 250:C486-C494PubMedGoogle Scholar
  36. McRoberts, J.A., Beuerlein, G., Dharmsathaphorn, K. 1985. Cyclic AMP and Ca2+-activated K+ transport in a human colonic epithelial cell line.J. Biol. Chem. 260:14163–14172PubMedGoogle Scholar
  37. Moore, L., Pastan, I. 1977. Energy-dependent calcium uptake activity in cultured mouse fibroblast microsomes. Regulation of the uptake system by cell density.J. Biol. Chem. 252:6304–6309PubMedGoogle Scholar
  38. Morris, A.P., Gallacher, D.V., Lee, J.A.C. 1986. A large conductance, voltage- and calcium-activated K+ channel in the basolateral membrane of rat enterocytes.FEBS Lett. 206:87–92PubMedGoogle Scholar
  39. Nishizuka, Y. 1984. The role of protein kinase C in cell surface signal transduction and tumour promotion.Nature (London) 308:693–698Google Scholar
  40. O'Doherty, J., Stark, R.J. 1981. Transmembrane and transepithelial movement of calcium during stimulus-secretion coupling.Am. J. Physiol. 241:G150-G158PubMedGoogle Scholar
  41. O'Doherty, J., Stark, R.J., Crane, S.J., Brugge, K.L. 1983. Changes in cytosolic calcium during cholinergic and adrenergic stimulation of the parotid salivary gland.Pfluegers Arch. 398:241–246Google Scholar
  42. O'Doherty, J., Youmans, S.J., Armstrong, W.McD. 1980. Calcium regulation during stimulus-secretion coupling: Continuous measurement of intracellular calcium activities.Science 209:510–513PubMedGoogle Scholar
  43. Oiki, S., Okada, Y. 1988. Clq induces chemotaxis and K+ conductance activation coupled to increased cytosolic Ca2+ in mouse fibroblasts.J. Immunol. 141:3177–3185PubMedGoogle Scholar
  44. Okada, Y., Hazama, A., Yada, T. 1985. HeLa cells and Intestine 407 cell. Their differences in electrical membrane responses to secretagogues and in ecto-enzyme activities.Cell Struct. Funct. 10:515p (Abstr.)Google Scholar
  45. Osugi, T., Imaizumi, T., Mizushima, A., Uchida, S., Yoshida, H. 1986. 1-Oleoyl-2-acetyl-glycerol and phorbol diester stimulate Ca2+ influx through Ca2+ channels in neuroblastoma x glioma hybrid NG108-15 cells.Eur. J. Pharmacol. 126:47–51PubMedGoogle Scholar
  46. Parker, I., Miledi, R. 1987. Inositol trisphosphate activates a voltage-dependent calcium influx inXenopus oocytes.Proc. R. Soc. London B 231:27–36Google Scholar
  47. Penner, R., Matthews, G., Neher, E. 1988. Regulation of calcium influx by second messengers in rat mast cells.Nature (London) 334:499–504Google Scholar
  48. Petersen, O.H. 1986. Potassium channels and fluid secretion.News Physiol. Sci. 1:92–95Google Scholar
  49. Schwartz, C.J., Kimberg, D.V., Sheerin, H.E., Field, M., Said, S.I. 1974. Vasoactive intestinal peptide stimulation of adenylate cyclase and active electrolyte secretion in intestinal mucosa.J. Clin. Invest. 54:536–544PubMedGoogle Scholar
  50. Semrad, C.E., Chang, E.G. 1987. Calcium-mediated cyclic AMP inhibition of Na−H exchange in small intestine.Am. J. Physiol. 252:C315-C322PubMedGoogle Scholar
  51. Sepulveda, F.V., Smith, S.M. 1987. Calcium transport by permeabilised rabbit small intestinal epithelial cells.Pfluegers Arch. 408:231–238Google Scholar
  52. Sheppard, D.N., Giraldez, F., Sepúlveda, F.V. 1988. Kinetics of voltage- and Ca2+ activation and Ba2+ blockade of a largeconductance K+ channel fromNecturus enterocytes.J. Membrane Biol. 105:65–75Google Scholar
  53. Sjölander, A. 1988. Direct effects of wheat germ agglutinin on inositol phosphate formation and cytosolic-free calcium level in Intestine 407 cells.J. Cell. Physiol. 134:473–478PubMedGoogle Scholar
  54. Strong, J.A., Fox, A.P., Tsien, R.W., Kaczmarek, L.K. 1987. Stimulation of protein kinase C recruits convert calcium channels inAplysia bag cell neurons.Nature (London) 325:714–717Google Scholar
  55. Thomas, D.D., Knoop, F.C. 1983. Effect of heat-stable enterotoxin ofEscherichia coli on cultured mammalian cells.J. Infect. Dis. 147:450–459PubMedGoogle Scholar
  56. Trimble, E.R., Burzzone, R., Biden, T.J., Farese, R.V. 1986. Secretin induces rapid increases in inositol triphosphate, cytosolic Ca2+ and diacylglycerol as well as cyclic AMP in rat pancreatic acini.Biochem. J. 239:257–261PubMedGoogle Scholar
  57. Ueda, S., Loo, D.D.F., Sachs, G. 1987. Regulation of K+ channels in the basolateral membrane ofNecturus oxyntic cells.J. Membrane Biol. 97:31–41Google Scholar
  58. van Corven, E.J.J.M., Verbost, P.M., de Jong, M.D., van Os, C.H. 1987. Kinetics of ATP-dependent Ca2+ uptake by permeabilized rat enterocytes. Effects of inositol 1,4,5-trisphosphate.Cell Calcium 8:197–206PubMedGoogle Scholar
  59. Velasco, G., Shears, S.B., Michell, R.H., Lazo, P.S. 1986. Calcium uptake by intracellular compartments in permeabilised enterocytes. Effect of inositol 1,4,5 trisphosphate.Biochem. Biophys. Res. Commun. 139:612–618PubMedGoogle Scholar
  60. Vilven, J., Coronado, R. 1988. Opening of dihydropyridine calcium channels in skeletal muscle membranes by inositol trisphosphate.Nature (London) 336:587–589Google Scholar
  61. Wakelam, M.J.O., Murphy, G.J., Hruby, V.J., Houslay, M.D. 1986. Activation of two signal-transduction systems in hepatocytes by glucagon.Nature (London) 323:68–71Google Scholar
  62. Wasserman, S.I., Barrett, K.E., Huott, P.A., Beuerlein, G., Kagnoff, M.F., Dharmsathaphorn, K. 1988. Immune-related intestinal Cl secretion I. Effect of histamine on the T84 cell line.Am. J. Physiol. 254:C53-C62PubMedGoogle Scholar
  63. Weber, A. 1968. The mechanism of the action of caffeine on sarcoplasmic reticulum.J. Gen. Physiol. 52:760–772PubMedGoogle Scholar
  64. Welsh, M.J., Smith, P.L., Frizzell, R.A. 1982. Chloride secretion by canine tracheal epithelium: II. The cellular electrical potential profile.J. Membrane Biol. 70:227–238Google Scholar
  65. Welsh, M.J., Smith, P.L., Frizzell, R.A. 1983. Chloride secretion by canine tracheal epithelium: III. Membrane resistances and electromotive forces.J. Membrane Biol. 71:209–218Google Scholar
  66. Yada, T., Oiki, S., Ueda, S., Okada, Y. 1986. Synchronous oscillation of the cytoplasmic Ca2+ concentration and membrane potential in cultured epithelial cells (Intestine 407).Biochim. Biophys. Acta 887:105–112PubMedGoogle Scholar
  67. Yada, T., Okada, Y. 1984. Electrical activity of an intestinal epithelial cell line: Hyperpolarizing responses to intestinal secretagogues.J. Membrane Biol. 77:33–44Google Scholar
  68. Yada, T., Russo, L.L., Sharp, G.W.G. 1989. Phorbol ester-stimulated insulin secretion by RINm5F insulinoma cells is linked with depolarization and an increase in cytosolic free Ca2+ concentration.J. Biol. Chem. 264:2455–2462PubMedGoogle Scholar
  69. Yamaguchi, D.T., Kleeman, C.R., Muallem, S. 1987. Protein kinase C-activated calcium channel in the osteoblast-like clonal osteosarcoma cell line UMR-106.J. Biol. Chem. 262:14967–14973PubMedGoogle Scholar

Copyright information

© Springer-Verlag New York Inc 1989

Authors and Affiliations

  • Toshihiko Yada
    • 1
  • Shigetoshi Oiki
    • 1
  • Shunji Ueda
    • 1
  • Yasunobu Okada
    • 1
  1. 1.Department of PhysiologyKyoto University Faculty of MedicineKyotoJapan

Personalised recommendations