Abstract
Activation of phospholipase C (PLC)-linked signaling cascades in nonexcitable cells stimulates Ca2+ release from inositol-1,4,5-trisphosphate (IP3)-sensitive intracellular Ca2+ stores and activation of Ca2+ entry via plasma membrane Ca2+ channels. The attention of investigators is currently focused on the properties and molecular basis of channels involved in Ca2+ entry into nonexcitable cells. According to current views, mammalian TRP proteins are involved in receptor-and store-dependent influx of Ca2+; however, little is known about the linkage between specific TRP proteins and endogenous channels responsible for Ca2+ entry. The aim of the present study was to elucidate the role of TRPC3 in the formation of store-dependent or receptor-operated pathways of Ca2+ entry into A431 cells. Registration of Ca2+ influx based on fluorescence measurements of intracellular Ca2+ concentrations and analysis of integral membrane currents revealed that partial inhibition of TRPC3 expression by small interfering RNA (siRNA) results in suppression of store-dependent Ca2+ entry without any effect on receptor-operated Ca2+ influx. In-depth studies of single channels revealed that TRPC3 suppression in A431 cells results in the disappearance of one type of store-operated channels and formation of a novel type of store-independent Ca2+-permeable channels. This, in turn, testifies to the crucial role of TRPC3 in normal functioning of store-operated Ca2+ channels in A431 cells.
Similar content being viewed by others
References
Parekh, A.B. and Penner R., Store depletion and calcium influx, Physiol Rev., 1997, vol. 77(4), pp. 901–930.
Putney, J.W., Jr., Broad, L.M., Braun, F.J., Lievremont, J.P., and Bird, G.S., Mechanisms of capacitative calcium entry, J. Cell Sci., 2001, vol. 114, pp. 2223–2229.
Venkatachalam, K., van Rossum, D.B., Patterson, R.L., Ma, H.T., and Gill, D.L., The cellular and molecular basis of store-operated calcium entry, Nature Cell Biol., 2002, vol. 4, pp. E263–E272.
Lewis, R.S. and Cahalan, M.D., Mitogen-induced oscillations of cytosolic Ca2+ and transmembrane Ca2+ current in human leukemic T cells, Cell Regul., 1989, vol. 1, pp. 99–112.
Hoth, M. and Penner, R., Depletion of intracellular calcium stores activates a calcium current in mast cells, Nature, 1992, vol. 355(6358), pp. 353–356.
Zweifach, A. and Lewis, R.S., Mitogen-regulated Ca2+ current of T lymphocytes is activated by depletion of intracellular Ca2+ stores, Proc. Natl. Acad. Sci. USA, 1993, vol. 90, pp. 6295–6299.
Krause, E., Pfeiffer, F., Schmid, A., and Schulz, I., Depletion of intracellular calcium stores activates a calcium conducting nonselective cation current in mouse pancreatic acinar cells, J. Biol. Chem., 1996, vol. 271, pp. 32 523–32 528.
Roe, M.W., Worley, J.F. III, Qian, F., Tamarina, N., Mittal, A.A., Dralyuk, F., Blair, N.T., Mertz, R.J., Philipson, L.H., and Dukes, I.D., Characterization of a Ca2+ release-activated nonselective cation current regulating membrane potential and [Ca2+]i oscillations in transgenically derived beta-cells, J. Biol. Chem., 1998, vol. 273, pp. 10 402–10 410.
Montell, C., Birnbaumer, L., and Flockerzi, V., The TRP channels, a remarkably functional family, Cell, 2002, vol. 108, pp. 595–598.
Montell, C., Physiology, Phylogeny, and Functions of the TRP Superfamily of Cation Channels, Science’s STKE, http://stke.sciencemag.org/cgi/content/full/OC_sigtrans;2001/90/re1.
Okada, T., Inoue, R., Yamazaki, K., Maeda, A., Kurosaki, T., Yamakuni, T., Tanaka, I., Shimizu, S., Ikenaka, K., Imoto, K., and Mori, Y., Molecular and functional characterization of a novel mouse transient receptor potential protein homologue TRP7. Ca2+-permeable cation channel that is constitutively activated and enhanced by stimulation of G protein-coupled receptor, J. Biol. Chem., 1999, vol. 274(39), pp. 27 359–27 370.
Venkatachalam, K., Zheng, F., and Gill, D.L., Regulation of canonical transient receptor potential (TRPC) channel function by diacylglycerol and protein kinase C, J. Biol. Chem., 2003, vol. 278, pp. 29 031–29 040.
Zhu, X., Jiang, M., and Birnbaumer, L., Receptor-activated Ca2+ influx via human Trp3 stably expressed in human embryonic kidney (HEK)293 cells. Evidence for a non-capacitative Ca2+ entry, J. Biol. Chem., 1998, vol. 273, pp. 133–142.
Hurst, R.S., Zhu, X., Boulay, G., Birnbaumer, L., and Stefani, E., Ionic currents underlying HTRP3 mediated agonist-dependent Ca2+ influx in stably transfected HEK293 cells, FEBS Lett., 1998, vol. 422, pp. 333–338.
Kamouchi, M., Philipp, S., Flockerzi, V., Wissenbach, U., Mamin, A., Raeymaekers, L., Eggermont, J., Droogmans, G., and Nilius, B., Properties of heterologously expressed hTRP3 channels in bovine pulmonary artery endothelial cells, J. Physiol., 1999, vol. 518, pp. 345–358.
Kiselyov, K., Xu, X., Mozhayeva, G., Kuo, T., Pessah, I., Mignery, G., Zhu, X., Birnbaumer, L., and Muallem, S., Functional interaction between InsP3 receptors and store-operated Htrp3 channels, Nature, 1998, vol. 396, pp. 478–482.
Boulay, G., Brown, D.M., Qin, N., Jiang, M., Dietrich, A., Zhu, M.X., Chen, Z., Birnbaumer, M., Mikoshiba, K., and Birnbaumer, L., Modulation of Ca2+ entry by polypeptides of the inositol 1,4,5-trisphosphate receptor (IP3R) that bind transient receptor potential (TRP): evidence for roles of TRP and IP3R in store depletion-activated Ca2+ entry, Proc. Natl. Acad. Sci. USA, 1999, vol. 96, pp. 14955–14960.
Vazquez, G., Wedel, B.J., Trebak, M., St. John Bird, G., and Putney, J.W., Jr., Expression level of the canonical transient receptor potential 3 (TRPC3) channel determines its mechanism of activation, J. Biol. Chem., 2003, vol. 278, pp. 21 649–21 654.
Vazquez, G., Lievremont, J.P., St. J., Bird, G., and Putney, J.W., Jr., Human Trp3 forms both inositol trisphosphate receptor-dependent and receptor-independent store-operated cation channels in DT40 avian B lymphocytes, Proc. Natl. Acad. Sci. USA, 2001, vol. 98, pp. 11 777–11 782.
Venkatachalam, K., Ma, H.T., Ford, D.L., and Gill, D.L., Expression of functional receptor-coupled TRPC3 channels in DT40 triple receptor InsP3 knockout cells, J. Biol. Chem., 2001, vol. 276, pp. 33 980–33 985.
Hofmann, T., Schaefer, M., Schultz, G., and Gudermann, T., Subunit composition of mammalian transient receptor potential channels in living cells, Proc. Natl. Acad. Sci. USA, 2002, vol. 99, pp. 7461–7466.
Wu, X., Babnigg, G., and Villereal, M.L., Functional significance of human Trp1 and Trp3 in store-operated Ca2+ entry in HEK-293 cells, Am. J. Physiol., 2000, vol. 278, pp. 526–536.
Zagranichnaya, T., Wu, X., and Villereal, M.L., Endogenous TRPC1, TRPC3, and TRPC7 Proteins combine to form native store-operated channels in HEK-293 Cells, J. Biol. Chem., 2005, vol. 280, pp. 29 559–29 569.
Gusev, K., Glouchankova, L., Zubov, A., Kaznacheyeva, E., Wang, Z., Bezprozvanny, I., and Mozhayeva G.N., The store-operated calcium entry pathways in human carcinoma A431 cells: functional properties and activation mechanisms, J. Gen. Physiol., 2003, vol. 122, pp. 81–94.
Mozhayeva, G.N., Naumov, A.P., and Kuryshev, Y.A., Calcium-permeable channels activated via guanine nucleotide-dependent mechanism in human carcinoma cells, FEBS Lett., 1990, vol. 277, pp. 233–234.
Kiselyov, K.I., Mamin, A.G., Semyonova, S.B., and Mozhayeva, G.N., Low-conductance high selective inositol (1,4,5)-trisphosphate activated Ca2+ channels in plasma membrane of A431 carcinoma cells, FEBS Lett., 1997, vol. 407, pp. 309–312.
Kiselyov, K.I., Semyonova, S.B., Mamin, A.G., and Mozhayeva, G.N., Miniature Ca2+ channels in excised plasma-membrane patches: activation by IP3, Pflugers Arch., 1999, vol. 437, pp. 305–314.
Zubov, A.I., Kaznacheeva, E.V., Nikolaev, A.V., Alexeenko, V.A., Kiselyov, K., Muallem, S., and Mozhayeva, G.N., Regulation of the miniature plasma membrane Ca2+ channel I(min) by inositol 1,4,5-trisphosphate receptors, J. Biol. Chem., 1999, vol. 274, pp. 25 983–25 985.
Kaznacheyeva, E., Zubov, A.N., Nikolaev, A., Alexeenko, V., Bezprozvanny, I., and Mozhayeva, G.N., Plasma membrane calcium channels in human carcinoma A431 cells are functionally coupled to inositol 1,4,5-trisphosphate receptor-phosphatidylinositol 4,5-bisphosphate complexes, J. Biol. Chem., 2000, vol. 275, pp. 4561–4564.
Kaznacheyeva, E., Zubov, A., Gusev, K., Bezprozvanny, I., and Mozhayeva, G.N., Activation of calcium entry in human carcinoma A431 cells by store depletion and phospholipase C-dependent mechanisms converge on ICRAC-like calcium channels, Proc. Natl. Acad. Sci. USA, 2001, vol. 98, pp. 148–153.
Brummelkamp, T.R., Bernards, R., and Agami R., A system for stable expression of short interfering RNAs in mammalian cells, Science, 2002, vol. 296(5567), pp. 550–553.
Grynkiewicz, G., Poenie, M., and Tsien, R.Y., A new generation of Ca2+ indicators with greatly improved fluorescence properties, J. Biol. Chem., 1985, vol. 260(6), pp. 3440–3450.
Hamill, O.P. and Sakmann, B., Multiple conductance states of single acetylcholine receptor channels in embryonic muscle cells, Nature, 1981, vol. 294(5840), pp. 462–464.
Bugaj, V., Alexeenko, V., Zubov, A., Glushankova, L., Nikolaev, A., Wang, Z., Kaznacheyeva, E., Bezprozvanny, I., and Mozhayeva, G.N., Functional properties of endogenous receptor-and store-operated calcium influx channels in HEK293 cells, J. Biol. Chem., 2005, vol. 280, pp. 16 790–16 797.
Author information
Authors and Affiliations
Additional information
Original Russian Text © E.V. Kaznacheyeva, L.N. Glushankova, V.V. Bugaj, O.A. Zimina, A.Yu. Skopin, V.A. Alexeenko, I.B. Bezprozvanny, and G.N. Mozhayeva, 2007, published in Biologicheskie Membrany, 2007, Vol. 24, No. 1, pp. 87–95.
Rights and permissions
About this article
Cite this article
Kaznacheyeva, E.V., Glushankova, L.N., Bugaj, V.V. et al. Role of TRPC3 in the formation of receptor-and store-operated calcium channels in carcinoma A431 cells. Biochem. Moscow Suppl. Ser. A 1, 79–87 (2007). https://doi.org/10.1134/S1990747807010096
Received:
Issue Date:
DOI: https://doi.org/10.1134/S1990747807010096