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The Journal of Membrane Biology

, Volume 124, Issue 2, pp 113–126 | Cite as

Variety of Ca2+-permeable channels in human carcinoma A431 cells

  • G. N. Mozhayeva
  • A. P. Naumov
  • Yu A. Kuryshev
Articles

Summary

Patch-clamp methods were used to search for and characterize channels that mediate calcium influx through the plasma membrane of human carcinoma A431 cells. Here we present four Ca2+-permeable channel types referred to as SG, G, I and BI. With 105mm Ca2+ as the charge carrier, at 30–33°C their mean unitary conductances (in pS) are: 1.3 (SG), 2.4 (G), 3.7 (I) and 12.8 (BI). SG and G channels are activated by nonhydrolyzable analogues of guanosine 5-triphosphate (GTP) applied to the inside of the membrane, suggesting an involvement of G-proteins in the control of their activity. I and BI channels are activated by inositol 1,4,5-trisphosphate (InsP3). G, I, BI and possibly SG channels are activated from the extracellular side of the membrane by epidermal growth factor (EGF) and histamine. It is assumed that all identified Ca2+ channels take part in the generation of the agonist-induced intracellular Ca2+ signal. The variety of Ca-channel types seems to be necessary to tune cell responses according to the respective type and level of an external signal, on the one hand, and to the functional state of the cell, on the other.

Key Words

Patch clamp carcinoma cell receptor-operated calcium-permeable channels guanine nucleotide inositol trisphosphate 

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References

  1. Avdonin, P.V., Cheglakov, I.B., Tkachuk, V.A. 1990. Ionic permeability and regulation of human platelet membrane receptor-operated channels.Biol. Membrany 7:12–22 (in Russian)Google Scholar
  2. Berridge, M.J., Irvin, R.F. 1989. Inositol phosphates and cell signalling.Nature 341:197–205PubMedGoogle Scholar
  3. Bers, D.M., MacLeod, K.T. 1988. Calcium chelators and calcium ionophoes.In: Calcium in Drug Actions. P.F. Baker, editor. pp. 492–507. Springer-Verlag, Berlin-TokyoGoogle Scholar
  4. Bochkov, V.N., Feoktistov, I.A., Avdonin, P.V., Tkachuk, V.A. 1989. The phorbol ester blocks the coupling between the GTP-binding protein and the receptor-operating calcium channels.Biochimya 54:1533–1542 (in Russian)Google Scholar
  5. Colquhoun, D., Sigworth, F.J. 1983. Fitting and statistical analysis of single channel records.In: Single-Channel Recording. B. Sakmann and E. Neher, editors. Plenum, New York-LondonGoogle Scholar
  6. Ehrlich, B.E., Finkelstein, A., Forte, M., Kung, C. 1984. Voltage dependent calcium channels fromParamecium cilia incorporated into planar lipid bilayers.Science 225:427–428Google Scholar
  7. Ehrlich, B.E., Watras, J. 1988. Inositol 1,4,5-trisphosphate activates a channel from smooth muscle sarcoplasmic reticulum.Nature 336:583–586PubMedGoogle Scholar
  8. Ewald, D.A., Sternweis, P.C., Miller, R.J. 1988. Guanine nucleotide-binding protein Go-induced coupling of neuropeptide Y receptors to Ca2+ channels in sensory neurons.Proc. Natl. Acad. Sci. USA 85:3633–3637PubMedGoogle Scholar
  9. Gilman, A.G. 1987. G-proteins: Transducers of receptor generated signal.Annu. Rev. Biochem. 56:615–649PubMedGoogle Scholar
  10. Gonzales, F.A., Gross, D.J., Heppel, L.A., Webb, W.W. 1988. Studies on the increase in cytosolic free calcium induced by epidermal growth factor, serum and nucleotides in individual A431 cells.J. Cell. Physiol. 135:269–276PubMedGoogle Scholar
  11. Hallam, T.J., Rink, T.J. 1989. Receptor-mediated Ca2+ entry: Diversity of function and mechanism.Trends Pharmacol. Sci. 10:8–10PubMedGoogle Scholar
  12. Hamill, O.P., Marty, A., Neher, E., Sakmann, B., Sigworth, F.J. 1981. Improved patch-clamp technique for high-resolution current recording from cells and cell-free membrane patches.Pfluegers Arch. 391:85–100CrossRefGoogle Scholar
  13. Hepler, J.R., Nakahata, N., Lovenberg, T., DiGuiseppi, J., Herman, B., Earp, H.S., Harden, T.K. 1987. Epidermal growth factor stimulates the rapid accumulation of inositol (1,4,5)-trisphosphate and a rise in cytosolic calcium mobilized from intracellular stores in A431 cells.J. Biol. Chem. 262:2951–2956PubMedGoogle Scholar
  14. Hescheler, J., Rosental, W., Hinsch, K., Wulfren, M., Trautwein, W., Schultz, G. 1988. Angiotensin II-induced stimulation of voltage-dependent Ca2+ currents in an adrenal cortical cell line.EMBO J. 7:619–624PubMedGoogle Scholar
  15. Hess, P., Lansman, J.B., Tsien, R.W. 1986. Calcium channel selectivity for divalent and monovalent ions. Voltage and concentration dependence of single channel current in ventricular cells.J. Gen. Physiol. 88:293–319PubMedGoogle Scholar
  16. Holz, G.G., Rane, S.G., Dunlap, K. 1986. GTP-binding proteins mediate transmitter inhibition of voltage-dependent calcium channels.Nature 319:670–672CrossRefGoogle Scholar
  17. Hosoi, K., Edidin, M. 1989. Exogenous ATP and other nucleotide phosphates modulate epidermal growth factor receptors of A431 epidermoid carcinoma cells.Proc. Natl. Acad. Sci. USA 86:4510–4514PubMedGoogle Scholar
  18. Jacob, R. 1990. Calcium oscillations in electrically non-excitable cells.Biochim. Biophys. Acta 1052:427–438PubMedGoogle Scholar
  19. Johns, A., Lategan, T.W., Lodge, N.J., Ryan, U.S., van Breemen, C., Adams, D.J. 1987. Calcium entry through receptoroperated channels in bovine pulmonary artery endothelial cells.Tissue Cell 19:733–745PubMedGoogle Scholar
  20. Kato, K., Nakanishi, M., Arata, Y., Teshima, R., Terao, T., Miyamoto, H. 1987. Calcium influx in a single rat basophilic leukemia cell as releated with a digital imaging fluorescence microscope.J. Biol. Chem. 102:1–4Google Scholar
  21. Kostyuk, P.G., Shuba, Ya.M., Savchenko, A.N. 1988. Three types of calcium channels in the membrane of mouse sensory neurons.Pfluegers Arch. 411:661–669Google Scholar
  22. Kuno, M., Gardner, P. 1987. Ion channels activated by inositol 1,4,5-trisphosphate in plasma membrane of human T-lymphocytes.Nature 326:301–304PubMedGoogle Scholar
  23. Kuno, M., Goronzy, J., Weyand, C.M., Gardner, P. 1986. Single channel and whole-cell recordings of mitogen-regulated inward currents in human cloned helper T-lymphocites.Nature 323:269–272PubMedGoogle Scholar
  24. Kuno, M., Okada, T., Shibata, T. 1989. A patch-clamp study: Secretagogue-induced currents in rat peritoneal mast cells.Am. J. Physiol. 256:6560–6568Google Scholar
  25. Macara, I.G. 1986. Activation of Ca2+ influx and22Na/H+ exchange by epidermal growth factor and vanadate in A431 cells is independent of phosphatidylinositol turnover and is inhibited by phorbol ester and diacyglycerol.J. Biol. Chem. 262:9321–9327Google Scholar
  26. MacDougall, S.L., Grinstein, S., Gelfand, E.W. 1988. Detection of ligand-activated conductive Ca2+ channels in human B lymphocytes.Cell 54:229–234PubMedGoogle Scholar
  27. Matsunaga, H., Nishimoto, I., Kojima, I., Yamashita, N., Kurokava, K., Ogata, E. 1988. Activation of calcium-permeable cation channel by insulin-like growth factor II in BALB/c3T3 cells.Am. J. Physiol. 255:442–446Google Scholar
  28. Matthews, G., Neher, E., Penner, R. 1989. Second messenger-activated calcium influx in rat pritoneal mast cells.J. Physiol. 418:105–130PubMedGoogle Scholar
  29. Merrit, J.E., Jacob, R., Hallam, T.J. 1989. Use of manganese to discriminate between calcium influx and mobilization from internal stores in stimulated human neutrophils.J. Biol. Chem. 264:1522–1527PubMedGoogle Scholar
  30. Moolenaar, W.H., Aerts, R.J., Tertoolen, L.G.J., de Laat, S.W. 1986. The epidermal growth factor-induced calcium signal in A431 cells.J. Biol. Chem. 261:279–284PubMedGoogle Scholar
  31. Morris, A.P., Gallacher, D.V., Irvine, R.F., Petersen, O.H. 1987. Synergism of inositol trisphosphate and tetrakisphosphate in activating of Ca2+-dependent K+ channels.Nature 330:653–655CrossRefGoogle Scholar
  32. Mozhayeva, G.N., Naumov, A.P., Kuryshev, Yu. A. 1989a. Activation of Ca2+-sensitive potassium channels in A431 cells by epidermal growth factor and histamine.Biol. Membrany 6:629–636 (in Russian)Google Scholar
  33. Mozhayeva, G.N., Naumov, A.P., Kuryshev, Yu.A. 1989b Ca2+-sensitive potassium channels in the epidermoid carcinoma A431 cells.Biol. Membrany 6:541–550 (in Russian)Google Scholar
  34. Mozhayeva, G.N., Naumov, A.P., Kuryshev, Yu.A. 1989c. Epidermal growth factor activates calcium-permeable channels in A431 cells.Biochim. Biophys. Acta 1011:171–175PubMedGoogle Scholar
  35. Narasimhan, V., Holowka, D., Fewtrell, C., Baird, B. 1988. Cholera toxin increases the rate of antigen-stimulated calcium influx in rat basophylic leukemia cells.J. Biol. Chem. 263:19626–19632PubMedGoogle Scholar
  36. Neer, E.J., Clapham, D.E. 1988. Roles of G protein subunits in transmembrane signalling.Nature 333:129–134CrossRefGoogle Scholar
  37. Nishimoto, I., Hata, Y., Ogata, E., Kojima, I. 1987. Insulinlike growth factor II stimulates calcium influx in competent BALB/c3T3 cells primed with epidermal growth factor.J. Biol. Chem. 262:12120–12126PubMedGoogle Scholar
  38. Pandiella, A., Magni, M., Lovisolo, D., Meldolesi, J. 1989. The effect of epidermal growth factor on membrane potential. Rapid hyperpolarization followed by persistent fluctuations.J. Biol. Chem. 264:12914–12921PubMedGoogle Scholar
  39. Penner, R., Matthews, G., Neher, E. 1988. Regulation of calcium influx by second messengers in rat mast cells.Nature 334:499–504PubMedGoogle Scholar
  40. Putney, J.W. 1987. Calcium-mobilizing receptors.Trends Pharmacol. Sci. 8:481–486Google Scholar
  41. Rasmussen, H., Barrett, P.Q. 1984. Calcium messenger system: An intergral view.Physiol. Rev. 64:938–984Google Scholar
  42. Reuter, H. 1986. Voltage-dependent mechanisms for raising intracellular free calcium concentration: Calcium channels.In: Calcium and the Cell. D. Everd and J. Whealan, editors. pp. 5–22. Ciba Found. Symp. 122Google Scholar
  43. Shapiro, D.N., Adams, B.S., Niederhuber, J.E. 1985. Antigenspecific activation results in an increase in cytoplasmic free calcium.J. Immunol. 135:2256–2261PubMedGoogle Scholar
  44. Sorkin, A.D., Teslenko, L.V., Nikolsky, N.N. 1988. The endocytosis of epidermal growth factor in A431 cells: pH of microenvironment and the dynamics of receptor complex dissociation.Exp. Cell. Res. 175:192–205PubMedGoogle Scholar
  45. Vilven, J., Coronado, R. 1988. Opening of dihydropyridine calcium channels in skeletal muscle membranes by inositol trisphosphate.Nature 336:587–589PubMedGoogle Scholar
  46. Volpi, M., Berlin, R.D. 1988. Intracellular elevations of free calcium induced by activation of histamine H1 receptors in interphase and mitotic HeLa cells: Hormone signal transduction is altered during mitosis.J. Cell. Biol. 107:2533–2539PubMedGoogle Scholar
  47. von Tscharner, V., Prod'hom, B., Baggiolini, M., Reuter, H., 1986. Ion channels in human neutrophils activated by a rise in free cytosolic calcium concentration.Nature 324:369–372PubMedGoogle Scholar
  48. Yatani, A., Codina, J., Imoto, Y., Roeves, J.P., Birnbaumer, L., Brown, A.M. 1987. A G-protein directly regulated mammalian cardiac calcium channels.Science 238:1228–1232Google Scholar
  49. Zschauer, A., Scott-Burden, T., Buhler, F.R., von Breemen, C. 1987. Vasopressor peptides and depolarization stimulated Ca2+-entry into cultured vascular smooth muscle.Biochem. Biophys. Res. Commun. 148:225–231PubMedGoogle Scholar

Copyright information

© Springer-Verlag New York Inc. 1991

Authors and Affiliations

  • G. N. Mozhayeva
    • 1
  • A. P. Naumov
    • 1
  • Yu A. Kuryshev
    • 1
  1. 1.Institute of CytologyAcademy of Sciences of the U.S.S.R.LeningradU.S.S.R.

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