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Abstract: The activation of Ca²⁺ entry through store-operated channels by agonists that deplete Ca²⁺ from the endoplasmic reticulum (ER) is a ubiquitous signaling mechanism, the molecular basis of which has remained elusive for the past two decades. Store-operated Ca²⁺-release-activated Ca²⁺ (CRAC) channels constitute the sole pathway for Ca²⁺ entry following antigen-receptor engagement. In a set of breakthrough studies over the past two years, stromal interaction molecule 1 (STIM1, the ER Ca²⁺ sensor) and orai1 (a pore-forming subunit of the CRAC channel) have been identified. Here we review these recent studies and the insights they provide into the mechanism of store-operated Ca²⁺ channels (SOCCs).

[1] Aires, V., Adote, S., Hichami, A., Moutairou, K., Boustani, E.S., Khan, N.A., 2004. Modulation of intracellular calcium concentrations and T cell activation by prickly pear polyphenols. Mol. Cell. Biochem., 260(1-2):103-110.

[2] Alfonso, S., Benito, O., Alicia, S., Angélica, Z., Patricia, G., Diana, K., Luis, V., 2008. Regulation of the cellular localization and function of human transient receptor potential channel 1 by other members of the TRPC family. Cell Calcium., 43(4):375-387.

[3] Ambudkar, I.S., Ong, H.L., Liu, X., Bandyopadhyay, B., Cheng, K.T., 2007. TRPC1: the link between functionally distinct store-operated calcium channels. Cell Calcium., 42(2):213-223.

[4] Baba, Y., Hayashi, K., Fujii, Y., Mizushima, A., Watarai, H., Wakamori, M., Numaga, T., Mori, Y., Iino, M., Hikida, M., Kurosaki, T., 2006. Coupling of STIM1 to store-operated Ca²⁺ entry through its constitutive and inducible movement in the endoplasmic reticulum. Proc. Natl. Acad. Sci. USA, 103(45):16704-16709.

[5] Bollimuntha, S., Cornatzer, E., Singh, B.B., 2005. Plasma membrane localization and function of TRPC1 is dependent on its interaction with beta-tubulin in retinal epithelium cells. Vis. Neurosci., 22(2):163-170.

[6] Bugaj, V., Alexeenko, V., Zubov, A., Glushankova, L., Nikolaev, A., Wang, Z., Kaznacheyeva, E., Bezprozvanny, I., Mozhayeva, G.N., 2005. Functional properties of endogenous receptor- and store-operated calcium influx channels in HEK293 cells. J. Biol. Chem., 280(17):16790-16797.

[7] DeHaven, W.I., Smyth, J.T., Boyles, R.R., Putney, J.W.Jr., 2007. Calcium inhibition and calcium potentiation of Orai1, Orai2 and Orai3 calcium release-activated calcium channels. J. Biol. Chem., 282(24):17548-17556.

[8] Demaurex, N., Arnaudeau, S., Opas, M., 2002. Measurement of intracellular Ca²⁺ concentration. Methods Cell Biol., 70:453-474.

[9] Dziadek, M.A., Johnstone, L.S., 2007. Biochemical properties and cellular localisation of STIM proteins. Cell Calcium., 42(2):123-132.

[10] Felix, R., 2005. Molecular regulation of voltage-gated Ca²⁺ channels. J. Recept. Signal Transduct., 25(2):57-71.

[11] Feske, S., Gwack, Y., Prakriya, M., Srikanth, S., Puppel, S.H., Tanasa, B., Hogan, P.G., Lewis, R.S., Daly, M., Rao, A., 2006. A mutation in Orai1 causes immune deficiency by abrogating CRAC channel function. Nature, 441(7090):179-185.

[12] Fleming, I., Rueben, A., Popp, R., Fisslthaler, B., Schrodt, S., Sander, A., Haendeler, J., Falck, J.R., Morisseau, C., Hammock, B.D., Busse, R., 2007. Epoxyeicosatrienoic acids regulate Trp channel dependent Ca²⁺ signaling and hyperpolarization in endothelial cells. Arterioscler. Thromb. Vasc. Biol., 27(12):2612-2618.

[13] Gross, S.A., Wissenbach, U., Philipp, S.E., Freichel, M., Cavalié, A., Flockerzi, V., 2007. Murine ORAI2 splice variants form functional Ca²⁺ release-activated Ca²⁺ (CRAC) channels. J. Biol. Chem., 282(27):19375-19384.

[14] Gwack, Y., Srikanth, S., Feske, S., Cruz-Guilloty, F., Oh-hora, M., Neems, D.S., Hogan, P.G., Rao, A., 2007. Biochemical and functional characterization of Orai proteins. J. Biol. Chem., 282(22):16232-16243.

[15] He, L.L., Zhang, Y., Chen, Y.H., Yamada, Y., Yang, J., 2007. Functional modularity of the beta-subunit of voltage-gated Ca²⁺ channels. Biophys. J., 93(3):834-845.

[16] Hewavitharana, T., Deng, X., Soboloff, J., Gill, D.L., 2007. Role of STIM and Orai proteins in the store-operated calcium signaling pathway. Cell Calcium., 42(2):173-182.

[17] Homann, V., Kinne-Saffran, E., Arnold, W.H., Gaengler, P., Kinne, R.K., 2006. Calcium transport in human salivary glands: a proposed model of calcium secretion into saliva. Histochem. Cell Biol., 125(5):583-591.

[18] Hoth, M., Penner, R., 1992. Depletion of intracellular calcium stores activates a calcium current in mast cells. Nature, 355(6358):353-356.

[19] Huang, G.N., Zeng, W., Kim, J.Y., Yuan, J.P., Han, L., Muallem, S., Worley, P.F., 2006. STIM1 carboxyl-terminus activates native SOC, I(crac) and TRPC1 channels. Nat. Cell Biol., 8(9):1003-1010.

[20] Jiang, Q.J., Xu, G., Mao, F.F., Zhu, Y.F., 2006. Effects of combination of irbesartan and perindopril on calcineurin expression and sarcoplasmic reticulum Ca²⁺-ATPase ativity in rat cardiac pressure-overload hypertrophy. J. Zhejiang. Univ. Sci. B., 7(3):228-234.

[21] Laporte, R., Hui, A., Laher, I., 2004. Pharmacological modulation of sarcoplasmic reticulum function in smooth muscle. Pharmacol. Rev., 56(4):439-513.

[22] Lepage, P.K., Boulay, G., 2007. Molecular determinants of TRP channel assembly. Biochem. Soc. Trans., 35(Pt 1):81-83.

[23] Lewis, R.S., 2007. The molecular choreography of a store-operated calcium channel. Nature, 446(7133):284-287.

[24] Lewis, R.S., Cahalan, M.D., 1989. Mitogen-induced oscillations of cytosolic Ca²⁺ and transmembrane Ca²⁺ current in human leukemic T cells. Cell Regul., 1:99-112.

[25] Li, Z., Lu, J., Xu, P., Xie, X., Chen, L., Xu, T., 2007. Mapping the interacting domains of STIM1 and Orai1 in Ca²⁺ release-activated Ca²⁺ channel activation. J. Biol. Chem., 282(40):29448-29456.

[26] Liou, J., Kim, M.L., Heo, W.D., Jones, J.T., Myers, J.W., Ferrell, J.E.Jr., Meyer, T., 2005. STIM is a Ca²⁺ sensor essential for Ca²⁺-store-depletion-triggered Ca²⁺ influx. Curr. Biol., 15(13):1235-1241.

[27] Liu, L., Li, Y., Wang, R., Yin, C., Dong, Q., Hing, H., Kim, C., Welsh, M.J., 2007. Drosophila hygrosensation requires the TRP channels water witch and nanchung. Nature, 450(7167):294-298.

[28] Liu, X., Bandyopadhyay, B.C., Singh, B.B., Groschner, K., Ambudkar, I.S., 2005. Molecular analysis of a store-operated and 2-acetyl-sn-glycerol-sensitive non-selective cation channel. Heteromeric assembly of TRPC1-TRPC3. J. Biol. Chem., 280(22):21600-21606.

[29] López, J.J., Salido, G.M., Pariente, J.A., Rosado, J.A., 2006. Interaction of STIM1 with endogenously expressed human canonical TRP1 upon depletion of intracellular Ca²⁺ stores. J. Biol. Chem., 281(38):28254-28264.

[30] Luik, R.M., Wu, M.M., Buchanan, J., Lewis, R.S., 2006. The elementary unit of store-operated Ca²⁺ entry: local activation of CRAC channels by STIM1 at ER-plasma membrane junctions. J. Cell Biol., 174(6):815-825.

[31] Mercer, J.C., Dehaven, W.I., Smyth, J.T., Wedel, B., Boyles, R.R., Bird, G.S., Putney, J.W.Jr., 2006. Large store-operated calcium selective currents due to co-expression of Orai1 or Orai2 with the intracellular calcium sensor, STIM1. J. Biol. Chem., 281(34):24979-24990.

[32] Mignen, O., Thompson, J.L., Shuttleworth, T.J., 2007. STIM1 regulates Ca²⁺ entry via arachidonate-regulated Ca²⁺-selective (ARC) channels without store depletion or translocation to the plasma membrane. J. Physiol., 579(Pt 3):703-715.

[33] Mueller, P., Quintana, A., Griesemer, D., Hoth, M., Pieters, J., 2007. Disruption of the cortical actin cytoskeleton does not affect store operated Ca²⁺ channels in human T-cells. FEBS Lett., 581(18):3557-3562.

[34] Parekh, A.B., 2003. Store-operated Ca²⁺ entry: dynamic interplay between endoplasmic reticulum, mitochondria and plasma membrane. J. Physiol., 547(Pt 2):333-348.

[35] Pigozzi, D., Ducret, T., Tajeddine, N., Gala, J.L., Tombal, B., Gailly, P., 2006. Calcium store contents control the expression of TRPC1, TRPC3 and TRPV6 proteins in LNCaP prostate cancer cell line. Cell Calcium., 39(5):401-415.

[36] Prakriya, M., Feske, S., Gwack, Y., Srikanth, S., Rao, A., Hogan, P.G., 2006. Orai1 is an essential pore subunit of the CRAC channel. Nature, 443(7108):230-233.

[37] Putney, J.W.Jr., 2005. Capacitative calcium entry: sensing the calcium stores. J. Cell. Biol., 169(3):381-389.

[38] Roos, J., DiGregorio, P.J., Yeromin, A.V., Ohlsen, K., Lioudyno, M., Zhang, S., Safrina, O., Kozak, J.A., Wagner, S.L., Cahalan, M.D., et al., 2005. STIM1, an essential and conserved component of store-operated Ca²⁺ channel function. J. Cell Biol., 169(3):435-445.

[39] Ross, K., Whitaker, M., Reynolds, N.J., 2007. Agonist-induced calcium entry correlates with STIM1 translocation. J. Cell. Physiol., 211(3):569-576.

[40] Smyth, J.T., DeHaven, W.I., Bird, G.S., Putney, J.W.Jr., 2007. Role of the microtubule cytoskeleton in the function of the store-operated Ca²⁺ channel activator STIM1. J. Cell Sci., 120(Pt 21):3762-3771.

[41] Soboloff, J., Spassova, M.A., Tang, X.D., Hewavitharana, T., Xu, W., Gill, D.L., 2006a. Orai1 and STIM reconstitute store-operated calcium channel function. J. Biol. Chem., 281(30):20661-20665.

[42] Soboloff, J., Spassova, M.A., Hewavitharana, T., He, L.P., Xu, W., Johnstone, L.S., Dziadek, M.A., Gill, D.L., 2006b. STIM2 is an inhibitor of STIM1-mediated store-operated Ca²⁺ entry. Curr. Biol., 16(14):1465-1470.

[43] Spassova, M.A., Soboloff, J., He, L.P., Xu, W., Dziadek, M.A., Gill, D.L., 2006. STIM1 has a plasma membrane role in the activation of store-operated Ca²⁺ channels. Proc. Natl. Acad. Sci. USA, 103(11):4040-4045.

[44] Stathopulos, P.B., Li, G.Y., Plevin, M.J., Ames, J.B., Ikura, M., 2006. Stored Ca²⁺ depletion-induced oligomerization of stromal interaction molecule 1 (STIM1) via the EF-SAM region: an initiation mechanism for capacitive Ca²⁺ entry. J. Biol. Chem., 281(47):35855-35862.

[45] Takahashi, Y., Murakami, M., Watanabe, H., Hasegawa, H., Ohba, T., Munehisa, Y., Nobori, K., Ono, K., Iijima, T., Ito, H., 2007. Essential role of the N-terminus of murine Orai1 in store-operated Ca²⁺ entry. Biochem. Biophys. Res. Commun., 356(1):45-52.

[46] Vanden Abeele, F., Shuba, Y., Roudbaraki, M., Lemonnier, L., Vanoverberghe, K., Mariot, P., Skryma, R., Prevarskaya, N., 2003. Store-operated Ca²⁺ channels in prostate cancer epithelial cells: function, regulation and role in carcinogenesis. Cell Calcium., 33(5-6):357-373.

[47] Venkatachalam, K., Zheng, F., Gill, D.L., 2003. Regulation of canonical transient receptor potential (TRPC) channel function by diacylglycerol and protein kinase C. J. Biol. Chem., 278(31):29031-29040.

[48] Vig, M., Beck, A., Billingsley, J.M., Lis, A., Parvez, S., Peinelt, C., Koomoa, D.L., Soboloff, J., Gill, D.L., Fleig, A., Kinet, J.P., Penner, R., 2006. CRACM1 multimers form the ion-selective pore of the CRAC channel. Curr. Biol., 16(20):2073-2079.

[49] Winslow, M.M., Neilson, J.R., Crabtree, G.R., 2003. Calcium signalling in lymphocytes. Curr. Opin. Immunol., 15(3):299-307.

[50] Wissenbach, U., Philipp, S.E., Gross, S.A., Cavalié, A., Flockerzi, V., 2007. Primary structure, chromosomal localization and expression in immune cells of the murine ORAI and STIM genes. Cell Calcium., 42(4-5):439-446.

[51] Worley, P.F., Zeng, W., Huang, G.N., Yuan, J.P., Kim, J.Y., Lee, M.G., Muallem, S., 2007. TRPC channels as STIM1-regulated store-operated channels. Cell Calcium., 42(2):205-211.

[52] Wu, M.M., Buchanan, J., Luik, R.M., Lewis, R.S., 2006. Ca²⁺ store depletion causes STIM1 to accumulate in ER regions closely associated with the plasma membrane. J. Cell Biol., 174(6):803-813.

[53] Yeromin, A.V., Zhang, S.L., Jiang, W., Yu, Y., Safrina, O., Cahalan, M.D., 2006. Molecular identification of the CRAC channel by altered ion selectivity in a mutant of Orai. Nature, 443(7108):226-229.

[54] Zhang, S.L., Yu, Y., Roos, J., Kozak, J.A., Deerinck, T.J., Ellisman, M.H., Stauderman, K.A., Cahalan, M.D., 2005. STIM1 is a Ca²⁺ sensor that activates CRAC channels and migrates from the Ca²⁺ store to the plasma membrane. Nature, 437(7060):902-905.