Abstract
Store-operated Ca2+ entry (SOCE) is an ubiquitous and major mechanism for Ca2+ influx in mammalian cells with important physiological relevance. Since the discovery of SOCE in 1986 both, the mechanism that communicates the amount of Ca2+ accumulated in the intracellular Ca2+ stores to the plasma membrane channels and the nature of the capacitative channels, have been a matter of intense investigation. During the last decade, two of the major elements of SOCE, STIM1, the Ca2+ sensor of the intracellular Ca2+ compartments, and Orai1, the protein forming the channel that conducts the capacitative Ca2+ release-activated current I CRAC, were identified. Together with these proteins, different homologues, including STIM2, Orai2 and Orai3, were identified, although their relevance in SOCE has not been fully characterized yet. Before the identification of STIM1 and Orai1, TRPC proteins were found to be involved in SOCE in different cell types, more likely conducting the non-selective capacitative current described as I SOC. Current evidence indicates that STIM1, Orai1 and TRPC proteins dynamically interact forming a ternary complex that mediates SOCE in a number of cellular models. The dynamic interaction of STIM1 with Orai1, TRPCs or both might provide an explanation to the distinct capacitative currents described in different cell types.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Abbreviations
- [Ca2+]i :
-
intracellular free Ca2+ concentration
- CAD:
-
CRAC-activating domain
- CMD:
-
CRAC modulatory domain
- CRAC:
-
Ca2+ release-activated Ca2+ channel
- ER:
-
endoplasmic reticulum
- IP3 :
-
inositol 3,4,5-trisphosphate
- OASF:
-
Orai-activating small fragment
- PM:
-
plasma membrane
- PMCA:
-
plasma membrane Ca2+-ATPase
- RACK1:
-
receptor for activated C-kinase-1
- ROC:
-
receptor-operated Ca2+ channels
- ROCE:
-
receptor-operated Ca2+ entry
- SCID:
-
severe combined immune deficiency
- SERCA:
-
sarcoplasmic/endoplasmic-reticulum Ca2+-ATPase
- SMOC:
-
second messenger-operated Ca2+ channels
- SOC:
-
store-operated Ca2+ channel
- SOAR:
-
STIM1 Orai-activating region
- SOCE:
-
store-operated Ca2+ entry
- STIM1:
-
stromal interaction molecule 1
- TRP:
-
transient receptor potential
- VOC:
-
voltage-operated channels
References
Bootman MD, Lipp P, Berridge MJ (2001) The organisation and functions of local Ca2+ signals. J Cell Sci 114:2213–2222
O’Neill SC, Miller L, Hinch R, Eisner DA (2004) Interplay between SERCA and sarcolemmal Ca2+ efflux pathways controls spontaneous release of Ca2+ from the sarcoplasmic reticulum in rat ventricular myocytes. J Physiol 559:121–128
Van Coppenolle F, Vanden Abeele F, Slomianny C, Flourakis M, Hesketh J, Dewailly E, Prevarskaya N (2004) Ribosome-translocon complex mediates calcium leakage from endoplasmic reticulum stores. J Cell Sci 117:4135–4142
Patel S, Docampo R (2010) Acidic calcium stores open for business: expanding the potential for intracellular Ca2+ signaling. Trends Cell Biol 20:277–286
Meldolesi J, Pozzan T (1998) The endoplasmic reticulum Ca2+ store: a view from the lumen. Trends Biochem Sci 23:10–14
Cancela JM, Charpentier G, Petersen OH (2003) Co-ordination of Ca2+ signalling in mammalian cells by the new Ca2+-releasing messenger NAADP. Pflugers Arch 446:322–327
Patel S, Churchill GC, Galione A (2001) Coordination of Ca2+ signalling by NAADP. Trends Biochem Sci 26:482–489
Streb H, Irvine RF, Berridge MJ, Schulz I (1983) Release of Ca2+ from a nonmitochondrial intracellular store in pancreatic acinar cells by inositol-1,4,5-trisphosphate. Nature 306:67–69
Galione A, Lee HC, Busa WB (1991) Ca2+-induced Ca2+ release in sea urchin egg homogenates: modulation by cyclic ADP-ribose. Science 253:1143–1146
Sher E, Biancardi E, Passafaro M, Clementi F (1991) Physiopathology of neuronal voltage-operated calcium channels. FASEB J 5:2677–2683
Alexander SP, Mathie A, Peters JA (2006) Guide to receptors and channels, 2nd edition. Br J Pharmacol 147(Suppl 3):S1–S168
Kyrozis A, Goldstein PA, Heath MJ, MacDermott AB (1995) Calcium entry through a subpopulation of AMPA receptors desensitized neighbouring NMDA receptors in rat dorsal horn neurons. J Physiol 485:373–381
Matsuda K, Fletcher M, Kamiya Y, Yuzaki M (2003) Specific assembly with the NMDA receptor 3B subunit controls surface expression and calcium permeability of NMDA receptors. J Neurosci 23:10064–10073
McKemy DD, Neuhausser WM, Julius D (2002) Identification of a cold receptor reveals a general role for TRP channels in thermosensation. Nature 416:52–58
Caterina MJ, Rosen TA, Tominaga M, Brake AJ, Julius D (1999) A capsaicin-receptor homologue with a high threshold for noxious heat. Nature 398:436–441
Valente P, Garcia-Sanz N, Gomis A, Fernandez-Carvajal A, Fernandez-Ballester G, Viana F, Belmonte C, Ferrer-Montiel A (2008) Identification of molecular determinants of channel gating in the transient receptor potential box of vanilloid receptor I. FASEB J 22:3298–3309
Jardin I, Gomez LJ, Salido GM, Rosado JA (2009) Dynamic interaction of hTRPC6 with the Orai1/STIM1 complex or hTRPC3 mediates its role in capacitative or non-capacitative Ca2+ entry pathways. Biochem J 420:267–276
Hofmann T, Obukhov AG, Schaefer M, Harteneck C, Gudermann T, Schultz G (1999) Direct activation of human TRPC6 and TRPC3 channels by diacylglycerol. Nature 397:259–263
Vazquez G, Wedel BJ, Kawasaki BT, Bird GS, Putney JW Jr (2004) Obligatory role of Src kinase in the signaling mechanism for TRPC3 cation channels. J Biol Chem 279:40521–40528
Moneer Z, Pino I, Taylor EJ, Broad LM, Liu Y, Tovey SC, Staali L, Taylor CW (2005) Different phospholipase-C-coupled receptors differentially regulate capacitative and non-capacitative Ca2+ entry in A7r5 cells. Biochem J 389:821–829
Soboloff J, Spassova M, Xu W, He LP, Cuesta N, Gill DL (2005) Role of endogenous TRPC6 channels in Ca2+ signal generation in A7r5 smooth muscle cells. J Biol Chem 280:39786–39794
Chakrabarti R, Chakrabarti R (2006) Calcium signaling in non-excitable cells: Ca2+ release and influx are independent events linked to two plasma membrane Ca2+ entry channels. J Cell Biochem 99:1503–1516
Vazquez G, Bird GS, Mori Y, Putney JW Jr (2006) Native TRPC7 channel activation by an inositol trisphosphate receptor-dependent mechanism. J Biol Chem 281:25250–25258
Berra-Romani R, Mazzocco-Spezzia A, Pulina MV, Golovina VA (2008) Ca2+ handling is altered when arterial myocytes progress from a contractile to a proliferative phenotype in culture. Am J Physiol Cell Physiol 295:C779–C790
Wang Y, Deng X, Hewavitharana T, Soboloff J, Gill DL (2008) Stim, orai and trpc channels in the control of calcium entry signals in smooth muscle. Clin Exp Pharmacol Physiol 35:1127–1133
Rosado JA, Sage SO (2000) Protein kinase C activates non-capacitative calcium entry in human platelets. J Physiol 529(Pt 1):159–169
Togashi K, Hara Y, Tominaga T, Higashi T, Konishi Y, Mori Y, Tominaga M (2006) TRPM2 activation by cyclic ADP-ribose at body temperature is involved in insulin secretion. EMBO J 25:1804–1815
Redondo PC, Salido GM, Pariente JA, Rosado JA (2004) Dual effect of hydrogen peroxide on store-mediated calcium entry in human platelets. Biochem Pharmacol 67:1065–1076
Rosado JA, Redondo PC, Salido GM, Gomez-Arteta E, Sage SO, Pariente JA (2004) Hydrogen peroxide generation induces pp 60src activation in human platelets: evidence for the involvement of this pathway in store-mediated calcium entry. J Biol Chem 279:1665–1675
Zhang W, Tong Q, Conrad K, Wozney J, Cheung JY, Miller BA (2007) Regulation of TRP channel TRPM2 by the tyrosine phosphatase PTPL1. Am J Physiol Cell Physiol 292: C1746–C1758
Amor NB, Redondo PC, Bartegi A, Pariente JA, Salido GM, Rosado JA (2006) A role for 5,6-epoxyeicosatrienoic acid in calcium entry by de novo conformational coupling in human platelets. J Physiol 570:309–323
Loot AE, Popp R, Fisslthaler B, Vriens J, Nilius B, Fleming I (2008) Role of cytochrome P450-dependent transient receptor potential V4 activation in flow-induced vasodilatation. Cardiovasc Res 80:445–452
Rohacs T, Nilius B (2007) Regulation of transient receptor potential (TRP) channels by phosphoinositides. Pflugers Arch 455:157–168
Jardin I, Redondo PC, Salido GM, Rosado JA (2008) Phosphatidylinositol 4,5-bisphosphate enhances store-operated calcium entry through hTRPC6 channel in human platelets. Biochim Biophys Acta 1783:84–97
Putney JW Jr (1986) A model for receptor-regulated calcium entry. Cell Calcium 7:1–12
Lee C, Xu DZ, Feketeova E, Kannan KB, Fekete Z, Deitch EA, Livingston DH, Hauser CJ (2005) Store-operated calcium channel inhibition attenuates neutrophil function and postshock acute lung injury. J Trauma 59:56–63
Leung FP, Yung LM, Yao X, Laher I, Huang Y (2008) Store-operated calcium entry in vascular smooth muscle. Br J Pharmacol 153:846–857
Berridge MJ (1995) Capacitative calcium entry. Biochem J 312(Pt 1):1–11
Redondo PC, Harper MT, Rosado JA, Sage SO (2006) A role for cofilin in the activation of store-operated calcium entry by de novo conformational coupling in human platelets. Blood 107:973–979
Galan C, Zbidi H, Bartegi A, Salido GM, Rosado JA (2009) STIM1, Orai1 and hTRPC1 are important for thrombin- and ADP-induced aggregation in human platelets. Arch Biochem Biophys 490:137–144
Feske S (2007) Calcium signalling in lymphocyte activation and disease. Nat Rev Immunol 7:690–702
Wedel B, Boyles RR, Putney JW Jr, Bird GS (2007) Role of the store-operated calcium entry proteins Stim1 and Orai1 in muscarinic cholinergic receptor-stimulated calcium oscillations in human embryonic kidney cells. J Physiol 579:679–689
Yan X, Xing J, Lorin-Nebel C, Estevez AY, Nehrke K, Lamitina T, Strange K (2006) Function of a STIM1 homologue in C. elegans: evidence that store-operated Ca2+ entry is not essential for oscillatory Ca2+ signaling and ER Ca2+ homeostasis. J Gen Physiol 128:443–459
Randriamampita C, Tsien RY (1993) Emptying of intracellular Ca2+ stores releases a novel small messenger that stimulates Ca2+ influx. Nature 364:809–814
Pandol SJ, Schoeffield-Payne MS (1990) Cyclic GMP mediates the agonist-stimulated increase in plasma membrane calcium entry in the pancreatic acinar cell. J Biol Chem 265:12846–12853
Sargeant P, Farndale RW, Sage SO (1993) ADP- and thapsigargin-evoked Ca2+ entry and protein-tyrosine phosphorylation are inhibited by the tyrosine kinase inhibitors genistein and methyl-2,5-dihydroxycinnamate in fura-2-loaded human platelets. J Biol Chem 268: 18151–18156
Sargeant P, Farndale RW, Sage SO (1994) Calcium store depletion in dimethyl BAPTA-loaded human platelets increases protein tyrosine phosphorylation in the absence of a rise in cytosolic calcium. Exp Physiol 79:269–272
Rosado JA, Graves D, Sage SO (2000) Tyrosine kinases activate store-mediated Ca2+ entry in human platelets through the reorganization of the actin cytoskeleton. Biochem J 351: 429–437
Alvarez J, Montero M, Garcia-Sancho J (1992) Cytochrome P450 may regulate plasma membrane Ca2+ permeability according to the filling state of the intracellular Ca2+ stores. FASEB J 6:786–792
Bird GS, Putney JW Jr (1993) Inhibition of thapsigargin-induced calcium entry by microinjected guanine nucleotide analogues. Evidence for the involvement of a small G-protein in capacitative calcium entry. J Biol Chem 268:21486–21488
Rosado JA, Sage SO (2000) Farnesylcysteine analogues inhibit store-regulated Ca2+ entry in human platelets: evidence for involvement of small GTP-binding proteins and actin cytoskeleton. Biochem J 347(Pt 1):183–192
Fasolato C, Hoth M, Penner R (1993) A GTP-dependent step in the activation mechanism of capacitative calcium influx. J Biol Chem 268:20737–20740
Yao Y, Ferrer-Montiel AV, Montal M, Tsien RY (1999) Activation of store-operated Ca2+ current in Xenopus oocytes requires SNAP-25 but not a diffusible messenger. Cell 98:475–485
Muallem S, Kwiatkowska K, Xu X, Yin HL (1995) Actin filament disassembly is a sufficient final trigger for exocytosis in nonexcitable cells. J Cell Biol 128:589–598
Patterson RL, van Rossum DB, Gill DL (1999) Store-operated Ca2+ entry: evidence for a secretion-like coupling model. Cell 98:487–499
Bezzerides VJ, Ramsey IS, Kotecha S, Greka A, Clapham DE (2004) Rapid vesicular translocation and insertion of TRP channels. Nat Cell Biol 6:709–720
Cayouette S, Lussier MP, Mathieu EL, Bousquet SM, Boulay G (2004) Exocytotic insertion of TRPC6 channel into the plasma membrane upon Gq protein-coupled receptor activation. J Biol Chem 279:7241–7246
Singh BB, Lockwich TP, Bandyopadhyay BC, Liu X, Bollimuntha S, Brazer SC, Combs C, Das S, Leenders AG, Sheng ZH, Knepper MA, Ambudkar SV, Ambudkar IS (2004) VAMP2-dependent exocytosis regulates plasma membrane insertion of TRPC3 channels and contributes to agonist-stimulated Ca2+ influx. Mol Cell 15:635–646
Woodard GE, Salido GM, Rosado JA (2008) Enhanced exocytotic-like insertion of Orai1 into the plasma membrane upon intracellular Ca2+ store depletion. Am J Physiol Cell Physiol 294:C1323–C1331
Irvine RF (1990) ‘Quantal’ Ca2+ release and the control of Ca2+ entry by inositol phosphates – a possible mechanism. FEBS Lett 263:5–9
Block BA, Imagawa T, Campbell KP, Franzini-Armstrong C (1988) Structural evidence for direct interaction between the molecular components of the transverse tubule/sarcoplasmic reticulum junction in skeletal muscle. J Cell Biol 107:2587–2600
Kiselyov K, Mignery GA, Zhu MX, Muallem S (1999) The N-terminal domain of the IP3 receptor gates store-operated hTrp3 channels. Mol Cell 4:423–429
Boulay G, Brown DM, Qin N, Jiang M, Dietrich A, Zhu MX, Chen Z, Birnbaumer M, Mikoshiba K, Birnbaumer L (1999) 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 96:14955–14960
Birnbaumer L, Boulay G, Brown D, Jiang M, Dietrich A, Mikoshiba K, Zhu X, Qin N (2000) Mechanism of capacitative Ca2+ entry (CCE): interaction between IP3 receptor and TRP links the internal calcium storage compartment to plasma membrane CCE channels. Recent Prog Horm Res 55:127–161
Treves S, Franzini-Armstrong C, Moccagatta L, Arnoult C, Grasso C, Schrum A, Ducreux S, Zhu MX, Mikoshiba K, Girard T, Smida-Rezgui S, Ronjat M, Zorzato F (2004) Junctate is a key element in calcium entry induced by activation of InsP3 receptors and/or calcium store depletion. J Cell Biol 166:537–548
Rosado JA, Jenner S, Sage SO (2000) A role for the actin cytoskeleton in the initiation and maintenance of store-mediated calcium entry in human platelets. Evidence for conformational coupling. J Biol Chem 275:7527–7533
Rosado JA, Sage SO (2001) Activation of store-mediated calcium entry by secretion-like coupling between the inositol 1,4,5-trisphosphate receptor type II and human transient receptor potential (hTrp1) channels in human platelets. Biochem J 356:191–198
Rosado JA, Sage SO (2002) The ERK cascade, a new pathway involved in the activation of store-mediated calcium entry in human platelets. Trends Cardiovasc Med 12:229–234
Redondo PC, Harper AG, Sage SO, Rosado JA (2007) Dual role of tubulin-cytoskeleton in store-operated calcium entry in human platelets. Cell Signal 19:2147–2154
Xie Q, Zhang Y, Zhai C, Bonanno JA (2002) Calcium influx factor from cytochrome P-450 metabolism and secretion-like coupling mechanisms for capacitative calcium entry in corneal endothelial cells. J Biol Chem 277:16559–16566
Rosado JA, Sage SO (2000) Coupling between inositol 1,4,5-trisphosphate receptors and human transient receptor potential channel 1 when intracellular Ca2+ stores are depleted. Biochem J 350(Pt 3):631–635
Brownlow SL, Sage SO (2003) Rapid agonist-evoked coupling of type II Ins(1,4,5)P3 receptor with human transient receptor potential (hTRPC1) channels in human platelets. Biochem J 375:697–704
Roos J, DiGregorio PJ, Yeromin AV, Ohlsen K, Lioudyno M, Zhang S, Safrina O, Kozak JA, Wagner SL, Cahalan MD, Velicelebi G, Stauderman KA (2005) STIM1, an essential and conserved component of store-operated Ca2+ channel function. J Cell Biol 169:435–445
Zhang SL, Yu Y, Roos J, Kozak JA, Deerinck TJ, Ellisman MH, Stauderman KA, Cahalan MD (2005) STIM1 is a Ca2+ sensor that activates CRAC channels and migrates from the Ca2+ store to the plasma membrane. Nature 437:902–905
Feske S, Gwack Y, Prakriya M, Srikanth S, Puppel SH, Tanasa B, Hogan PG, Lewis RS, Daly M, Rao A (2006) A mutation in Orai1 causes immune deficiency by abrogating CRAC channel function. Nature 441:179–185
Mercer JC, Dehaven WI, Smyth JT, Wedel B, Boyles RR, Bird GS, Putney JW 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 281:24979–24990
Jardin I, Lopez JJ, Salido GM, Rosado JA (2008) Functional relevance of the de novo coupling between hTRPC1 and type II IP3 receptor in store-operated Ca2+ entry in human platelets. Cell Signal 20:737–747
Bandyopadhyay BC, Ong HL, Lockwich TP, Liu X, Paria BC, Singh BB, Ambudkar IS (2008) TRPC3 controls agonist-stimulated intracellular Ca2+ release by mediating the interaction between inositol 1,4,5-trisphosphate receptor and RACK1. J Biol Chem 283: 32821–32830
Woodard GE, Lopez JJ, Jardin I, Salido GM, Rosado JA (2010) TRPC3 regulates agonist-stimulated Ca2+ mobilization by mediating the interaction between type I inositol 1,4,5-trisphosphate receptor, RACK1, and Orai1. J Biol Chem 285:8045–8053
Zbidi H, Jardin I, Woodard GE, Lopez JJ, Berna-Erro A, Salido GM, Rosado JA (2011) STIM1 and STIM2 are located in the acidic Ca2+ stores and associates with Orai1 upon depletion of the acidic stores in human platelets. J Biol Chem 286:12257–12270
Liou J, Kim ML, Heo WD, Jones JT, Myers JW, Ferrell JE Jr, Meyer T (2005) STIM is a Ca2+ sensor essential for Ca2+-store-depletion-triggered Ca2+ influx. Curr Biol 15:1235–1241
Lopez JJ, Salido GM, Pariente JA, Rosado JA (2006) Interaction of STIM1 with endogenously expressed human canonical TRP1 upon depletion of intracellular Ca2+ stores. J Biol Chem 281:28254–28264
Spassova MA, Soboloff J, He LP, Xu W, Dziadek MA, Gill DL (2006) STIM1 has a plasma membrane role in the activation of store-operated Ca2+ channels. Proc Natl Acad Sci USA 103:4040–4045
Schultz J, Ponting CP, Hofmann K, Bork P (1997) SAM as a protein interaction domain involved in developmental regulation. Protein Sci 6:249–253
Brandman O, Liou J, Park WS, Meyer T (2007) STIM2 is a feedback regulator that stabilizes basal cytosolic and endoplasmic reticulum Ca2+ levels. Cell 131:1327–1339
Huang Y, Zhou Y, Wong HC, Chen Y, Wang S, Castiblanco A, Liu A, Yang JJ (2009) A single EF-hand isolated from STIM1 forms dimer in the absence and presence of Ca2+. FEBS J 276:5589–5597
Soboloff J, Spassova MA, Dziadek MA, Gill DL (2006) Calcium signals mediated by STIM and Orai proteins – a new paradigm in inter-organelle communication. Biochim Biophys Acta 1763:1161–1168
Schindl R, Muik M, Fahrner M, Derler I, Fritsch R, Bergsmann J, Romanin C (2009) Recent progress on STIM1 domains controlling Orai activation. Cell Calcium 46:227–232
Soboloff J, Spassova MA, Tang XD, Hewavitharana T, Xu W, Gill DL (2006) Orai1 and STIM reconstitute store-operated calcium channel function. J Biol Chem 281:20661–20665
Jardin I, Lopez JJ, Redondo PC, Salido GM, Rosado JA (2009) Store-operated Ca2+ entry is sensitive to the extracellular Ca2+ concentration through plasma membrane STIM1. Biochim Biophys Acta 1793:1614–1622
Dionisio N, Galan C, Jardin I, Salido GM, Rosado JA (2011) Lipid rafts are essential for the regulation of SOCE by plasma membrane resident STIM1 in human platelets. Biochim Biophys Acta 1813:431–437
Pani B, Ong HL, Liu X, Rauser K, Ambudkar IS, Singh BB (2008) Lipid rafts determine clustering of STIM1 in endoplasmic reticulum-plasma membrane junctions and regulation of store-operated Ca2+ entry (SOCE). J Biol Chem 283:17333–17340
Luik RM, Wu MM, Buchanan J, Lewis RS (2006) The elementary unit of store-operated Ca2+ entry: local activation of CRAC channels by STIM1 at ER-plasma membrane junctions. J Cell Biol 174:815–825
Peinelt C, Vig M, Koomoa DL, Beck A, Nadler MJ, Koblan-Huberson M, Lis A, Fleig A, Penner R, Kinet JP (2006) Amplification of CRAC current by STIM1 and CRACM1 (Orai1). Nat Cell Biol 8:771–773
Yuan JP, Zeng W, Huang GN, Worley PF, Muallem S (2007) STIM1 heteromultimerizes TRPC channels to determine their function as store-operated channels. Nat Cell Biol 9:636–645
Park CY, Shcheglovitov A, Dolmetsch R (2010) The CRAC channel activator STIM1 binds and inhibits L-type voltage-gated calcium channels. Science 330:101–105
Wang Y, Deng X, Mancarella S, Hendron E, Eguchi S, Soboloff J, Tang XD, Gill DL (2010) The calcium store sensor, STIM1, reciprocally controls Orai and CaV1.2 channels. Science 330:105–109
Williams RT, Manji SS, Parker NJ, Hancock MS, Van Stekelenburg L, Eid JP, Senior PV, Kazenwadel JS, Shandala T, Saint R, Smith PJ, Dziadek MA (2001) Identification and characterization of the STIM (stromal interaction molecule) gene family: coding for a novel class of transmembrane proteins. Biochem J 357:673–685
Huang GN, Zeng W, Kim JY, Yuan JP, Han L, Muallem S, Worley PF (2006) STIM1 carboxyl-terminus activates native SOC, I(crac) and TRPC1 channels. Nat Cell Biol 8:1003–1010
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 282:29448–29456
Pozo-Guisado E, Campbell DG, Deak M, Alvarez-Barrientos A, Morrice NA, Alvarez IS, Alessi DR, Martin-Romero FJ (2010) Phosphorylation of STIM1 at ERK1/2 target sites modulates store-operated calcium entry. J Cell Sci 123:3084–3093
Smyth JT, Petranka JG, Boyles RR, DeHaven WI, Fukushima M, Johnson KL, Williams JG, Putney JW Jr (2009) Phosphorylation of STIM1 underlies suppression of store-operated calcium entry during mitosis. Nat Cell Biol 11:1465–1472
Berna-Erro A, Braun A, Kraft R, Kleinschnitz C, Schuhmann MK, Stegner D, Wultsch T, Eilers J, Meuth SG, Stoll G, Nieswandt B (2009) STIM2 regulates capacitive Ca2+ entry in neurons and plays a key role in hypoxic neuronal cell death. Sci Signal 2:ra67
Cordeiro S, Strauss O (2011) Expression of Orai genes and I(CRAC) activation in the human retinal pigment epithelium. Graefes Arch Clin Exp Ophthalmol 249:47–54
Gao YD, Hanley PJ, Rinne S, Zuzarte M, Daut J (2010) Calcium-activated K+ channel (K(Ca)3.1) activity during Ca2+ store depletion and store-operated Ca2+ entry in human macrophages. Cell Calcium 48:19–27
Schuhmann MK, Stegner D, Berna-Erro A, Bittner S, Braun A, Kleinschnitz C, Stoll G, Wiendl H, Meuth SG, Nieswandt B (2010) Stromal interaction molecules 1 and 2 are key regulators of autoreactive T cell activation in murine autoimmune central nervous system inflammation. J Immunol 184:1536–1542
Oh-hora M, Yamashita M, Hogan PG, Sharma S, Lamperti E, Chung W, Prakriya M, Feske S, Rao A (2008) Dual functions for the endoplasmic reticulum calcium sensors STIM1 and STIM2 in T cell activation and tolerance. Nat Immunol 9:432–443
Darbellay B, Arnaudeau S, Ceroni D, Bader CR, Konig S, Bernheim L (2010) Human muscle economy myoblast differentiation and excitation-contraction coupling use the same molecular partners, STIM1 and STIM2. J Biol Chem 285:22437–22447
Matsumoto M, Fujii Y, Baba A, Hikida M, Kurosaki T, Baba Y (2011) The calcium sensors STIM1 and STIM2 control B cell regulatory function through interleukin-10 production. Immunity 34:703–714
Soboloff J, Spassova MA, Hewavitharana T, He LP, Xu W, Johnstone LS, Dziadek MA, Gill DL (2006) STIM2 is an inhibitor of STIM1-mediated store-operated Ca2+ Entry. Curr Biol 16:1465–1470
Manji SS, Parker NJ, Williams RT, Van SL, Pearson RB, Dziadek M, Smith PJ (2000) STIM1: a novel phosphoprotein located at the cell surface. Biochim Biophys Acta 1481: 147–155
Williams RT, Senior PV, Van SL, Layton JE, Smith PJ, Dziadek MA (2002) Stromal interaction molecule 1 (STIM1), a transmembrane protein with growth suppressor activity, contains an extracellular SAM domain modified by N-linked glycosylation. Biochim Biophys Acta 1596:131–137
Kim CA, Bowie JU (2003) SAM domains: uniform structure, diversity of function. Trends Biochem Sci 28:625–628
Stathopulos PB, Zheng L, Li GY, Plevin MJ, Ikura M (2008) Structural and mechanistic insights into STIM1-mediated initiation of store-operated calcium entry. Cell 135: 110–122
Stathopulos PB, Li GY, Plevin MJ, Ames JB, 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 281:35855–35862
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 103:16704–16709
Zheng L, Stathopulos PB, Schindl R, Li GY, Romanin C, Ikura M (2011) Auto-inhibitory role of the EF-SAM domain of STIM proteins in store-operated calcium entry. Proc Natl Acad Sci USA 108:1337–1342
Stathopulos PB, Zheng L, Ikura M (2009) Stromal interaction molecule (STIM) 1 and STIM2 calcium sensing regions exhibit distinct unfolding and oligomerization kinetics. J Biol Chem 284:728–732
Barrero MJ, Montero M, Alvarez J (1997) Dynamics of [Ca2+] in the endoplasmic reticulum and cytoplasm of intact HeLa cells. A comparative study. J Biol Chem 272:27694–27699
Demaurex N, Frieden M (2003) Measurements of the free luminal ER Ca2+ concentration with targeted “cameleon” fluorescent proteins. Cell Calcium 34:109–119
Yu R (2000) Hinkle PM: rapid turnover of calcium in the endoplasmic reticulum during signaling. Studies with cameleon calcium indicators. J Biol Chem 275:23648–23653
Parry DA, Fraser RD, Squire JM (2008) Fifty years of coiled-coils and alpha-helical bundles: a close relationship between sequence and structure. J Struct Biol 163:258–269
Bauer MC, O’Connell D, Cahill DJ, Linse S (2008) Calmodulin binding to the polybasic C-termini of STIM proteins involved in store-operated calcium entry. Biochemistry 47: 6089–6091
Parvez S, Beck A, Peinelt C, Soboloff J, Lis A, Monteilh-Zoller M, Gill DL, Fleig A, Penner R (2008) STIM2 protein mediates distinct store-dependent and store-independent modes of CRAC channel activation. FASEB J 22:752–761
McAndrew D, Grice DM, Peters AA, Davis FM, Stewart T, Rice M, Smart CE, Brown MA, Kenny PA, Roberts-Thomson SJ, Monteith GR (2011) ORAI1-mediated calcium influx in lactation and in breast cancer. Mol Cancer Ther 10:448–460
Motiani RK, Abdullaev IF, Trebak M (2010) A novel native store-operated calcium channel encoded by Orai3: selective requirement of Orai3 versus Orai1 in estrogen receptor-positive versus estrogen receptor-negative breast cancer cells. J Biol Chem 285: 19173–19183
Lu W, Wang J, Peng G, Shimoda LA, Sylvester JT (2009) Knockdown of stromal interaction molecule 1 attenuates store-operated Ca2+ entry and Ca2+ responses to acute hypoxia in pulmonary arterial smooth muscle. Am J Physiol Lung Cell Mol Physiol 297:L17–L25
Varga-Szabo D, Braun A, Kleinschnitz C, Bender M, Pleines I, Pham M, Renne T, Stoll G, Nieswandt B (2008) The calcium sensor STIM1 is an essential mediator of arterial thrombosis and ischemic brain infarction. J Exp Med 205:1583–1591
Braun A, Gessner JE, Varga-Szabo D, Syed SN, Konrad S, Stegner D, Vogtle T, Schmidt RE, Nieswandt B (2009) STIM1 is essential for Fcgamma receptor activation and autoimmune inflammation. Blood 113:1097–1104
Gilio K, van Kruchten R, Braun A, Berna-Erro A, Feijge MA, Stegner D, van der Meijden PE, Kuijpers MJ, Varga-Szabo D, Heemskerk JW, Nieswandt B (2010) Roles of platelet STIM1 and Orai1 in glycoprotein VI- and thrombin-dependent procoagulant activity and thrombus formation. J Biol Chem 285:23629–23638
Brechard S, Plancon S, Melchior C, Tschirhart EJ (2009) STIM1 but not STIM2 is an essential regulator of Ca2+ influx-mediated NADPH oxidase activity in neutrophil-like HL-60 cells. Biochem Pharmacol 78:504–513
Peel SE, Liu B, Hall IP (2006) A key role for STIM1 in store operated calcium channel activation in airway smooth muscle. Respir Res 7:119
Decuypere JP, Monaco G, Kiviluoto S, Oh-hora M, Luyten T, De Smedt H, Parys JB, Missiaen L, Bultynck G (2010) STIM1, but not STIM2, is required for proper agonist-induced Ca2+ signaling. Cell Calcium 48:161–167
Bandyopadhyay BC, Pingle SC, Ahern GP (2011) Store-operated Ca2+ signaling in dendritic cells occurs independently of STIM1. J Leukoc Biol 89:57–62
El Boustany C, Katsogiannou M, Delcourt P, Dewailly E, Prevarskaya N, Borowiec AS, Capiod T (2010) Differential roles of STIM1, STIM2 and Orai1 in the control of cell proliferation and SOCE amplitude in HEK293 cells. Cell Calcium 47:350–359
Darbellay B, Arnaudeau S, Konig S, Jousset H, Bader C, Demaurex N, Bernheim L (2009) STIM1- and Orai1-dependent store-operated calcium entry regulates human myoblast differentiation. J Biol Chem 284:5370–5380
Zhou Y, Mancarella S, Wang Y, Yue C, Ritchie M, Gill DL, Soboloff J (2009) The short N-terminal domains of STIM1 and STIM2 control the activation kinetics of Orai1 channels. J Biol Chem 284:19164–19168
Vig M, Peinelt C, Beck A, Koomoa DL, Rabah D, Koblan-Huberson M, Kraft S, Turner H, Fleig A, Penner R, Kinet JP (2006) CRACM1 is a plasma membrane protein essential for store-operated Ca2+ entry. Science 312:1220–1223
Zhang SL, Yeromin AV, Zhang XH, Yu Y, Safrina O, Penna A, Roos J, Stauderman KA, Cahalan MD (2006) Genome-wide RNAi screen of Ca2+ influx identifies genes that regulate Ca2+ release-activated Ca2+ channel activity. Proc Natl Acad Sci USA 103:9357–9362
DeHaven WI, Smyth JT, Boyles RR, Putney JW Jr (2007) Calcium inhibition and calcium potentiation of Orai1, Orai2, and Orai3 calcium release-activated calcium channels. J Biol Chem 282:17548–17556
Maruyama Y, Ogura T, Mio K, Kato K, Kaneko T, Kiyonaka S, Mori Y, Sato C (2009) Tetrameric Orai1 is a teardrop-shaped molecule with a long, tapered cytoplasmic domain. J Biol Chem 284:13676–13685
Mullins FM, Park CY, Dolmetsch RE, Lewis RS (2009) STIM1 and calmodulin interact with Orai1 to induce Ca2+-dependent inactivation of CRAC channels. Proc Natl Acad Sci USA 106:15495–15500
Fierro L, Lund PE, Parekh AB (2000) Comparison of the activation of the Ca2+ release-activated Ca2+ current ICRAC to InsP3 in Jurkat T-lymphocytes, pulmonary artery endothelia and RBL-1 cells. Pflugers Arch 440:580–587
Zweifach A, Lewis RS (1995) Rapid inactivation of depletion-activated calcium current (ICRAC) due to local calcium feedback. J Gen Physiol 105:209–226
Muik M, Frischauf I, Derler I, Fahrner M, Bergsmann J, Eder P, Schindl R, Hesch C, Polzinger B, Fritsch R, Kahr H, Madl J, Gruber H, Groschner K, Romanin C (2008) Dynamic coupling of the putative coiled-coil domain of ORAI1 with STIM1 mediates ORAI1 channel activation. J Biol Chem 283:8014–8022
Frischauf I, Muik M, Derler I, Bergsmann J, Fahrner M, Schindl R, Groschner K, Romanin C (2009) Molecular determinants of the coupling between STIM1 and Orai channels: differential activation of Orai1-3 channels by a STIM1 coiled-coil mutant. J Biol Chem 284:21696–21706
Lis A, Peinelt C, Beck A, Parvez S, Monteilh-Zoller M, Fleig A, Penner R (2007) CRACM1, CRACM2, and CRACM3 are store-operated Ca2+ channels with distinct functional properties. Curr Biol 17:794–800
Peinelt C, Lis A, Beck A, Fleig A, Penner R (2008) 2-Aminoethoxydiphenyl borate directly facilitates and indirectly inhibits STIM1-dependent gating of CRAC channels. J Physiol 586:3061–3073
Prakriya M, Feske S, Gwack Y, Srikanth S, Rao A, Hogan PG (2006) Orai1 is an essential pore subunit of the CRAC channel. Nature 443:230–233
Schindl R, Bergsmann J, Frischauf I, Derler I, Fahrner M, Muik M, Fritsch R, Groschner K, Romanin C (2008) 2-aminoethoxydiphenyl borate alters selectivity of Orai3 channels by increasing their pore size. J Biol Chem 283:20261–20267
Vig M, Beck A, Billingsley JM, Lis A, Parvez S, Peinelt C, Koomoa DL, Soboloff J, Gill DL, Fleig A, Kinet JP, Penner R (2006) CRACM1 multimers form the ion-selective pore of the CRAC channel. Curr Biol 16:2073–2079
Yeromin AV, Zhang SL, Jiang W, Yu Y, Safrina O, Cahalan MD (2006) Molecular identification of the CRAC channel by altered ion selectivity in a mutant of Orai. Nature 443:226–229
Srikanth S, Jung HJ, Ribalet B, Gwack Y (2010) The intracellular loop of Orai1 plays a central role in fast inactivation of Ca2+ release-activated Ca2+ channels. J Biol Chem 285:5066–5075
Lee KP, Yuan JP, Zeng W, So I, Worley PF, Muallem S (2009) Molecular determinants of fast Ca2+-dependent inactivation and gating of the Orai channels. Proc Natl Acad Sci USA 106:14687–14692
Yamashita M, Navarro-Borelly L, McNally BA, Prakriya M (2007) Orai1 mutations alter ion permeation and Ca2+-dependent fast inactivation of CRAC channels: evidence for coupling of permeation and gating. J Gen Physiol 130:525–540
Derler I, Fahrner M, Muik M, Lackner B, Schindl R, Groschner K, Romanin C (2009) A Ca2+ release-activated Ca2+ (CRAC) modulatory domain (CMD) within STIM1 mediates fast Ca2+-dependent inactivation of ORAI1 channels. J Biol Chem 284:24933–24938
Frischauf I, Schindl R, Bergsmann J, Derler I, Fahrner M, Muik M, Fritsch R, Lackner B, Groschner K, Romanin C (2011) Cooperativeness of Orai cytosolic domains tunes subtype-specific gating. J Biol Chem 286:8577–8584
Vig M, DeHaven WI, Bird GS, Billingsley JM, Wang H, Rao PE, Hutchings AB, Jouvin MH, Putney JW, Kinet JP (2008) Defective mast cell effector functions in mice lacking the CRACM1 pore subunit of store-operated calcium release-activated calcium channels. Nat Immunol 9:89–96
Gross SA, Wissenbach U, Philipp SE, Freichel M, Cavalie A, Flockerzi V (2007) Murine ORAI2 splice variants form functional Ca2+ release-activated Ca2+ (CRAC) channels. J Biol Chem 282:19375–19384
Ohana L, Newell EW, Stanley EF, Schlichter LC (2009) The Ca2+ release-activated Ca2+ current (ICRAC) mediates store-operated Ca2+ entry in rat microglia. Channels (Austin) 3:129–139
Gwack Y, Srikanth S, Feske S, Cruz-Guilloty F, Oh-hora M, Neems DS, Hogan PG, Rao A (2007) Biochemical and functional characterization of Orai proteins. J Biol Chem 282:16232–16243
Su AI, Wiltshire T, Batalov S, Lapp H, Ching KA, Block D, Zhang J, Soden R, Hayakawa M, Kreiman G, Cooke MP, Walker JR, Hogenesch JB (2004) A gene atlas of the mouse and human protein-encoding transcriptomes. Proc Natl Acad Sci USA 101:6062–6067
Wissenbach U, Philipp SE, Gross SA, Cavalie A, Flockerzi V (2007) Primary structure, chromosomal localization and expression in immune cells of the murine ORAI and STIM genes. Cell Calcium 42:439–446
Prakriya M (2009) The molecular physiology of CRAC channels. Immunol Rev 231:88–98
Thompson J, Mignen O, Shuttleworth TJ (2010) The N-terminal domain of Orai3 determines selectivity for activation of the store-independent ARC channel by arachidonic acid. Channels (Austin) 4:398–410
Mignen O, Thompson JL, Shuttleworth TJ (2009) The molecular architecture of the arachidonate-regulated Ca2+-selective ARC channel is a pentameric assembly of Orai1 and Orai3 subunits. J Physiol 587:4181–4197
Mignen O, Thompson JL, Shuttleworth TJ (2008) Both Orai1 and Orai3 are essential components of the arachidonate-regulated Ca2+-selective (ARC) channels. J Physiol 586:185–195
Lis A, Zierler S, Peinelt C, Fleig A, Penner R (2010) A single lysine in the N-terminal region of store-operated channels is critical for STIM1-mediated gating. J Gen Physiol 136:673–686
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 356:45–52
Baryshnikov SG, Pulina MV, Zulian A, Linde CI, Golovina VA (2009) Orai1, a critical component of store-operated Ca2+ entry, is functionally associated with Na+/Ca2+ exchanger and plasma membrane Ca2+ pump in proliferating human arterial myocytes. Am J Physiol Cell Physiol 297:C1103–C1112
Potier M, Gonzalez JC, Motiani RK, Abdullaev IF, Bisaillon JM, Singer HA, Trebak M (2009) Evidence for STIM1- and Orai1-dependent store-operated calcium influx through ICRAC in vascular smooth muscle cells: role in proliferation and migration. FASEB J 23:2425–2437
Bisaillon JM, Motiani RK, Gonzalez-Cobos JC, Potier M, Halligan KE, Alzawahra WF, Barroso M, Singer HA, Jourd’heuil D, Trebak M (2010) Essential role for STIM1/Orai1-mediated calcium influx in PDGF-induced smooth muscle migration. Am J Physiol Cell Physiol 298:C993–C1005
Faouzi M, Hague F, Potier M, Ahidouch A, Sevestre H, Ouadid-Ahidouch H (2011) Down-regulation of Orai3 arrests cell-cycle progression and induces apoptosis in breast cancer cells but not in normal breast epithelial cells. J Cell Physiol 226:542–551
Bogeski I, Kummerow C, Al-Ansary D, Schwarz EC, Koehler R, Kozai D, Takahashi N, Peinelt C, Griesemer D, Bozem M, Mori Y, Hoth M, Niemeyer BA (2010) Differential redox regulation of ORAI ion channels: a mechanism to tune cellular calcium signaling. Sci Signal 3:ra24
McCarl CA, Picard C, Khalil S, Kawasaki T, Rother J, Papolos A, Kutok J, Hivroz C, Ledeist F, Plogmann K, Ehl S, Notheis G, Albert MH, Belohradsky BH, Kirschner J, Rao A, Fischer A, Feske S (2009) ORAI1 deficiency and lack of store-operated Ca2+ entry cause immunodeficiency, myopathy, and ectodermal dysplasia. J Allergy Clin Immunol 124:1311–1318, e1317
Feske S (2009) ORAI1 and STIM1 deficiency in human and mice: roles of store-operated Ca2+ entry in the immune system and beyond. Immunol Rev 231:189–209
Montell C, Rubin GM (1989) Molecular characterization of the Drosophila trp locus: a putative integral membrane protein required for phototransduction. Neuron 2:1313–1323
Hardie RC, Minke B (1992) The trp gene is essential for a light-activated Ca2+ channel in Drosophila photoreceptors. Neuron 8:643–651
Phillips AM, Bull A, Kelly LE (1992) Identification of a Drosophila gene encoding a calmodulin-binding protein with homology to the trp phototransduction gene. Neuron 8:631–642
Hardie RC, Reuss H, Lansdell SJ, Millar NS (1997) Functional equivalence of native light-sensitive channels in the Drosophila trp301 mutant and TRPL cation channels expressed in a stably transfected Drosophila cell line. Cell Calcium 21:431–440
Hardie RC (2003) Regulation of TRP channels via lipid second messengers. Annu Rev Physiol 65:735–759
Wes PD, Chevesich J, Jeromin A, Rosenberg C, Stetten G, Montell C (1995) TRPC1, a human homolog of a Drosophila store-operated channel. Proc Natl Acad Sci USA 92:9652–9656
Zhu X, Chu PB, Peyton M, Birnbaumer L (1995) Molecular cloning of a widely expressed human homologue for the Drosophila trp gene. FEBS Lett 373:193–198
Petersen CC, Berridge MJ, Borgese MF, Bennett DL (1995) Putative capacitative calcium entry channels: expression of Drosophila trp and evidence for the existence of vertebrate homologues. Biochem J 311(Pt 1):41–44
Montell C, Birnbaumer L, Flockerzi V, Bindels RJ, Bruford EA, Caterina MJ, Clapham DE, Harteneck C, Heller S, Julius D, Kojima I, Mori Y, Penner R, Prawitt D, Scharenberg AM, Schultz G, Shimizu N, Zhu MX (2002) A unified nomenclature for the superfamily of TRP cation channels. Mol Cell 9:229–231
Pedersen SF, Owsianik G, Nilius B (2005) TRP channels: an overview. Cell Calcium 38:233–252
Zhu X, Jiang M, Peyton M, Boulay G, Hurst R, Stefani E, Birnbaumer L (1996) trp, a novel mammalian gene family essential for agonist-activated capacitative Ca2+ entry. Cell 85(5):661–671
Montell C (2003) The venerable inveterate invertebrate TRP channels. Cell Calcium 33:409–417
Montell C, Birnbaumer L, Flockerzi V (2002) The TRP channels, a remarkably functional family. Cell 108:595–598
Parekh AB, Putney JW Jr (2005) Store-operated calcium channels. Physiol Rev 85:757–810
Wedel BJ, Vazquez G, McKay RR, St JBG, Putney JW Jr (2003) A calmodulin/inositol 1,4,5-trisphosphate (IP3) receptor-binding region targets TRPC3 to the plasma membrane in a calmodulin/IP3 receptor-independent process. J Biol Chem 278:25758–25765
Vannier B, Zhu X, Brown D, Birnbaumer L (1998) The membrane topology of human transient receptor potential 3 as inferred from glycosylation-scanning mutagenesis and epitope immunocytochemistry. J Biol Chem 273:8675–8679
Vazquez G, Wedel BJ, Aziz O, Trebak M, Putney JW Jr (2004) The mammalian TRPC cation channels. Biochim Biophys Acta 1742:21–36
Montell C (2005) Drosophila TRP channels. Pflugers Arch 451:19–28
Liu X, Bandyopadhyay BC, Singh BB, Groschner K, Ambudkar IS (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 280:21600–21606
Thebault S, Zholos A, Enfissi A, Slomianny C, Dewailly E, Roudbaraki M, Parys J, Prevarskaya N (2005) Receptor-operated Ca2+ entry mediated by TRPC3/TRPC6 proteins in rat prostate smooth muscle (PS1) cell line. J Cell Physiol 204:320–328
Liu X, Wang W, Singh BB, Lockwich T, Jadlowiec J, O’Connell B, Wellner R, Zhu MX, Ambudkar IS (2000) Trp1, a candidate protein for the store-operated Ca2+ influx mechanism in salivary gland cells. J Biol Chem 275:3403–3411
Rosado JA, Brownlow SL, Sage SO (2002) Endogenously expressed Trp1 is involved in store-mediated Ca2+ entry by conformational coupling in human platelets. J Biol Chem 277:42157–42163
Zagranichnaya TK, Wu X, Villereal ML (2005) Endogenous TRPC1, TRPC3, and TRPC7 proteins combine to form native store-operated channels in HEK-293 cells. J Biol Chem 280:29559–29569
Ambudkar IS, Ong HL, Liu X, Bandyopadhyay B, Cheng KT (2007) TRPC1: the link between functionally distinct store-operated calcium channels. Cell Calcium 42:213–223
Fatherazi S, Presland RB, Belton CM, Goodwin P, Al-Qutub M, Trbic Z, Macdonald G, Schubert MM, Izutsu KT (2007) Evidence that TRPC4 supports the calcium selective ICRAC-like current in human gingival keratinocytes. Pflugers Arch 453:879–889
Jardin I, Lopez JJ, Salido GM, Rosado JA (2008) Orai1 mediates the interaction between STIM1 and hTRPC1 and regulates the mode of activation of hTRPC1-forming Ca2+ channels. J Biol Chem 283:25296–25304
Salido GM, Sage SO, Rosado JA (2008) TRPC channels and store-operated Ca2+ entry. Biochim Biophys Acta 1793:223–230
Olah T, Fodor J, Ruzsnavszky O, Vincze J, Berbey C, Allard B, Csernoch L (2011) Overexpression of transient receptor potential canonical type 1 (TRPC1) alters both store operated calcium entry and depolarization-evoked calcium signals in C2C12 cells. Cell Calcium 49(6):415–425
Xu SZ, Beech DJ (2001) TrpC1 is a membrane-spanning subunit of store-operated Ca2+ channels in native vascular smooth muscle cells. Circ Res 88:84–87
Vazquez G, Wedel BJ, Trebak M, St John Bird G, Putney JW Jr (2003) Expression level of the canonical transient receptor potential 3 (TRPC3) channel determines its mechanism of activation. J Biol Chem 278:21649–21654
Yildirim E, Kawasaki BT, Birnbaumer L (2005) Molecular cloning of TRPC3a, an N-terminally extended, store-operated variant of the human C3 transient receptor potential channel. Proc Natl Acad Sci USA 102:3307–3311
Philipp S, Cavalie A, Freichel M, Wissenbach U, Zimmer S, Trost C, Marquart A, Murakami M, Flockerzi V (1996) A mammalian capacitative calcium entry channel homologous to Drosophila TRP and TRPL. EMBO J 15:6166–6171
Brownlow SL, Sage SO (2005) Transient receptor potential protein subunit assembly and membrane distribution in human platelets. Thromb Haemost 94:839–845
Philipp S, Hambrecht J, Braslavski L, Schroth G, Freichel M, Murakami M, Cavalie A, Flockerzi V (1998) A novel capacitative calcium entry channel expressed in excitable cells. EMBO J 17:4274–4282
Brechard S, Melchior C, Plancon S, Schenten V, Tschirhart EJ (2008) Store-operated Ca2+ channels formed by TRPC1, TRPC6 and Orai1 and non-store-operated channels formed by TRPC3 are involved in the regulation of NADPH oxidase in HL-60 granulocytes. Cell Calcium 44:492–506
Lievremont JP, Bird GS, Putney JW Jr (2004) Canonical transient receptor potential TRPC7 can function as both a receptor- and store-operated channel in HEK-293 cells. Am J Physiol Cell Physiol 287:C1709–C1716
Singh BB, Liu X, Ambudkar IS (2000) Expression of truncated transient receptor potential protein 1alpha (Trp1alpha): evidence that the Trp1 C terminus modulates store-operated Ca2+ entry. J Biol Chem 275:36483–36486
Liu X, Singh BB, Ambudkar IS (2003) TRPC1 is required for functional store-operated Ca2+ channels. Role of acidic amino acid residues in the S5-S6 region. J Biol Chem 278:11337–11343
Brough GH, Wu S, Cioffi D, Moore TM, Li M, Dean N, Stevens T (2001) Contribution of endogenously expressed Trp1 to a Ca2+-selective, store-operated Ca2+ entry pathway. FASEB J 15:1727–1738
Varga-Szabo D, Authi KS, Braun A, Bender M, Ambily A, Hassock SR, Gudermann T, Dietrich A, Nieswandt B (2008) Store-operated Ca2+ entry in platelets occurs independently of transient receptor potential (TRP) C1. Pflugers Arch 457:377–387
Yuan JP, Zeng W, Dorwart MR, Choi YJ, Worley PF, Muallem S (2009) SOAR and the polybasic STIM1 domains gate and regulate Orai channels. Nat Cell Biol 11:337–343
Muik M, Fahrner M, Derler I, Schindl R, Bergsmann J, Frischauf I, Groschner K, Romanin C (2009) A cytosolic homomerization and a modulatory domain within STIM1 C terminus determine coupling to ORAI1 channels. J Biol Chem 284:8421–8426
Park CY, Hoover PJ, Mullins FM, Bachhawat P, Covington ED, Raunser S, Walz T, Garcia KC, Dolmetsch RE, Lewis RS (2009) STIM1 clusters and activates CRAC channels via direct binding of a cytosolic domain to Orai1. Cell 136:876–890
Kawasaki T, Lange I, Feske S (2009) A minimal regulatory domain in the C terminus of STIM1 binds to and activates ORAI1 CRAC channels. Biochem Biophys Res Commun 385:49–54
Wang Y, Deng X, Gill DL (2010) Calcium signaling by STIM and Orai: intimate coupling details revealed. Sci Signal 3:pe42
Muik M, Fahrner M, Schindl R, Stathopulos P, Frischauf I, Derler I, Plenk P, Lackner B, Groschner K, Ikura M, Romanin C (2011) STIM1 couples to ORAI1 via an intramolecular transition into an extended conformation. EMBO J 30:1678–1689
Xu P, Lu J, Li Z, Yu X, Chen L, Xu T (2006) Aggregation of STIM1 underneath the plasma membrane induces clustering of Orai1. Biochem Biophys Res Commun 350:969–976
Scrimgeour N, Litjens T, Ma L, Barritt GJ, Rychkov GY (2009) Properties of Orai1 mediated store-operated current depend on the expression levels of STIM1 and Orai1 proteins. J Physiol 587:2903–2918
Zeng W, Yuan JP, Kim MS, Choi YJ, Huang GN, Worley PF, Muallem S (2008) STIM1 gates TRPC channels, but not Orai1, by electrostatic interaction. Mol Cell 32:439–448
Ong HL, Cheng KT, Liu X, Bandyopadhyay BC, Paria BC, Soboloff J, Pani B, Gwack Y, Srikanth S, Singh BB, Gill DL, Ambudkar IS (2007) Dynamic assembly of TRPC1-STIM1-Orai1 ternary complex is involved in store-operated calcium influx. Evidence for similarities in store-operated and calcium release-activated calcium channel components. J Biol Chem 282:9105–9116
Cheng KT, Liu X, Ong HL, Ambudkar IS (2008) Functional requirement for Orai1 in store-operated TRPC1-STIM1 channels. J Biol Chem 283:12935–12940
Galan C, Woodard GE, Dionisio N, Salido GM, Rosado JA (2010) Lipid rafts modulate the activation but not the maintenance of store-operated Ca2+ entry. Biochim Biophys Acta 1803:1083–1093
Simons K, Toomre D (2000) Lipid rafts and signal transduction. Nat Rev Mol Cell Biol 1:31–39
Sampieri A, Zepeda A, Saldaña C, Salgado A, Vaca L (2008) STIM1 converts TRPC1 from a receptor-operated to a store-operated channel: moving TRPC1 in and out of lipid rafts. Cell Calcium 44:479–491
Jardin I, Salido GM, Rosado JA (2008) Role of lipid rafts in the interaction between hTRPC1, Orai1 and STIM1. Channels (Austin) 2:401–403
Liao Y, Erxleben C, Abramowitz J, Flockerzi V, Zhu MX, Armstrong DL, Birnbaumer L (2008) Functional interactions among Orai1, TRPCs, and STIM1 suggest a STIM-regulated heteromeric Orai/TRPC model for SOCE/Icrac channels. Proc Natl Acad Sci USA 105:2895–2900
Liao Y, Erxleben C, Yildirim E, Abramowitz J, Armstrong DL, Birnbaumer L (2007) Orai proteins interact with TRPC channels and confer responsiveness to store depletion. Proc Natl Acad Sci USA 104:4682–4687
Cheng KT, Liu X, Ong HL, Swaim W, Ambudkar IS (2011) Local Ca2+ entry via Orai1 regulates plasma membrane recruitment of TRPC1 and controls cytosolic Ca2+ signals required for specific cell functions. PLoS Biol 9:e1001025
Lorin-Nebel C, Xing J, Yan X, Strange K (2007) CRAC channel activity in C. elegans is mediated by Orai1 and STIM1 homologues and is essential for ovulation and fertility. J Physiol 580:67–85
Liao Y, Plummer NW, George MD, Abramowitz J, Zhu MX, Birnbaumer L (2009) A role for Orai in TRPC-mediated Ca2+ entry suggests that a TRPC:Orai complex may mediate store and receptor operated Ca2+ entry. Proc Natl Acad Sci USA 106:3202–3206
Partiseti M, Le Deist F, Hivroz C, Fischer A, Korn H, Choquet D (1994) The calcium current activated by T cell receptor and store depletion in human lymphocytes is absent in a primary immunodeficiency. J Biol Chem 269:32327–32335
Le Deist F, Hivroz C, Partiseti M, Thomas C, Buc HA, Oleastro M, Belohradsky B, Choquet D, Fischer A (1995) A primary T-cell immunodeficiency associated with defective transmembrane calcium influx. Blood 85:1053–1062
Picard C, McCarl CA, Papolos A, Khalil S, Luthy K, Hivroz C, LeDeist F, Rieux-Laucat F, Rechavi G, Rao A, Fischer A, Feske S (2009) STIM1 mutation associated with a syndrome of immunodeficiency and autoimmunity. N Engl J Med 360:1971–1980
Byun M, Abhyankar A, Lelarge V, Plancoulaine S, Palanduz A, Telhan L, Boisson B, Picard C, Dewell S, Zhao C, Jouanguy E, Feske S, Abel L, Casanova JL (2010) Whole-exome sequencing-based discovery of STIM1 deficiency in a child with fatal classic Kaposi sarcoma. J Exp Med 207:2307–2312
Feske S, Giltnane J, Dolmetsch R, Staudt LM, Rao A (2001) Gene regulation mediated by calcium signals in T lymphocytes. Nat Immunol 2:316–324
Feske S, Prakriya M, Rao A, Lewis RS (2005) A severe defect in CRAC Ca2+ channel activation and altered K+ channel gating in T cells from immunodeficient patients. J Exp Med 202:651–662
Feske S, Picard C, Fischer A (2010) Immunodeficiency due to mutations in ORAI1 and STIM1. Clin Immunol 135:169–182
Feske S (2010) CRAC channelopathies. Pflugers Arch 460:417–435
Feske S, Muller JM, Graf D, Kroczek RA, Drager R, Niemeyer C, Baeuerle PA, Peter HH, Schlesier M (1996) Severe combined immunodeficiency due to defective binding of the nuclear factor of activated T cells in T lymphocytes of two male siblings. Eur J Immunol 26:2119–2126
Maul-Pavicic A, Chiang SC, Rensing-Ehl A, Jessen B, Fauriat C, Wood SM, Sjoqvist S, Hufnagel M, Schulze I, Bass T, Schamel WW, Fuchs S, Pircher H, McCarl CA, Mikoshiba K, Schwarz K, Feske S, Bryceson YT, Ehl S (2011) ORAI1-mediated calcium influx is required for human cytotoxic lymphocyte degranulation and target cell lysis. Proc Natl Acad Sci USA 108:3324–3329
Chou YH, Juo SH, Chiu YC, Liu ME, Chen WC, Chang CC, Chang WP, Chang JG, Chang WC (2011) A polymorphism of the ORAI1 gene is associated with the risk and recurrence of calcium nephrolithiasis. J Urol 185:1742–1746
Bergmeier W, Oh-Hora M, McCarl CA, Roden RC, Bray PF, Feske S (2009) R93W mutation in Orai1 causes impaired calcium influx in platelets. Blood 113:675–678
Gwack Y, Srikanth S, Oh-Hora M, Hogan PG, Lamperti ED, Yamashita M, Gelinas C, Neems DS, Sasaki Y, Feske S, Prakriya M, Rajewsky K, Rao A (2008) Hair loss and defective T- and B-cell function in mice lacking ORAI1. Mol Cell Biol 28:5209–5222
Beyersdorf N, Braun A, Vogtle T, Varga-Szabo D, Galdos RR, Kissler S, Kerkau T, Nieswandt B (2009) STIM1-independent T cell development and effector function in vivo. J Immunol 182:3390–3397
Braun A, Varga-Szabo D, Kleinschnitz C, Pleines I, Bender M, Austinat M, Bosl M, Stoll G, Nieswandt B (2009) Orai1 (CRACM1) is the platelet SOC channel and essential for pathological thrombus formation. Blood 113:2056–2063
Ma J, McCarl CA, Khalil S, Luthy K, Feske S (2010) T-cell-specific deletion of STIM1 and STIM2 protects mice from EAE by impairing the effector functions of Th1 and Th17 cells. Eur J Immunol 40:3028–3042
Linde CI, Baryshnikov SG, Mazzocco-Spezzia A, Golovina VA (2011) Dysregulation of Ca2+ signaling in astrocytes from mice lacking amyloid precursor protein. Am J Physiol Cell Physiol 300:C1502–C1512
Leissring MA, Akbari Y, Fanger CM, Cahalan MD, Mattson MP, LaFerla FM (2000) Capacitative calcium entry deficits and elevated luminal calcium content in mutant presenilin-1 knockin mice. J Cell Biol 149:793–798
Bojarski L, Pomorski P, Szybinska A, Drab M, Skibinska-Kijek A, Gruszczynska-Biegala J, Kuznicki J (2009) Presenilin-dependent expression of STIM proteins and dysregulation of capacitative Ca2+ entry in familial Alzheimer’s disease. Biochim Biophys Acta 1793: 1050–1057
Zatti G, Ghidoni R, Barbiero L, Binetti G, Pozzan T, Fasolato C, Pizzo P (2004) The presenilin 2 M239I mutation associated with familial Alzheimer’s disease reduces Ca2+ release from intracellular stores. Neurobiol Dis 15:269–278
Giacomello M, Barbiero L, Zatti G, Squitti R, Binetti G, Pozzan T, Fasolato C, Ghidoni R, Pizzo P (2005) Reduction of Ca2+ stores and capacitative Ca2+ entry is associated with the familial Alzheimer’s disease presenilin-2 T122R mutation and anticipates the onset of dementia. Neurobiol Dis 18:638–648
Sorgato MC, Bertoli A (2009) From cell protection to death: may Ca2+ signals explain the chameleonic attributes of the mammalian prion protein? Biochem Biophys Res Commun 379:171–174
Lazzari C, Peggion C, Stella R, Massimino ML, Lim D, Bertoli A, Sorgato MC (2011) Cellular prion protein is implicated in the regulation of local Ca2+ movements in cerebellar granule neurons. J Neurochem 116:881–890
Jardin I, Lopez JJ, Zbidi H, Bartegi A, Salido GM, Rosado JA (2011) Attenuated store-operated divalent cation entry and association between STIM1, Orai1, hTRPC1 and hTRPC6 in platelets from type 2 diabetic patients. Blood Cells Mol Dis 15(46):252–260
Okon EB, Golbabaie A, Breemen C (2008) Paracrine effects of endothelial cells in a diabetic mouse model: capacitative calcium entry stimulated thromboxane release. Horm Metab Res 40:645–650
Sabbioni S, Veronese A, Trubia M, Taramelli R, Barbanti-Brodano G, Croce CM, Negrini M (1999) Exon structure and promoter identification of STIM1 (alias GOK), a human gene causing growth arrest of the human tumor cell lines G401 and RD. Cytogenet Cell Genet 86:214–218
Ruano Y, Mollejo M, Ribalta T, Fiano C, Camacho FI, Gomez E, de Lope AR, Hernandez-Moneo JL, Martinez P, Melendez B (2006) Identification of novel candidate target genes in amplicons of Glioblastoma multiforme tumors detected by expression and CGH microarray profiling. Mol Cancer 5:39
Acknowledgements
This work was supported by M.E.C. grants BFU2010-21043-C02-01 and Junta de Extremadura-FEDER (PRIBS10020 and GR10010). PCR is supported by MEC “Ramón y Cajal program” (RYC2007-00349) and AB held a contract from the University of Extremadura.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2012 Springer Science+Business Media B.V.
About this chapter
Cite this chapter
Berna-Erro, A., Redondo, P.C., Rosado, J.A. (2012). Store-Operated Ca2+ Entry. In: Islam, M. (eds) Calcium Signaling. Advances in Experimental Medicine and Biology, vol 740. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-2888-2_15
Download citation
DOI: https://doi.org/10.1007/978-94-007-2888-2_15
Published:
Publisher Name: Springer, Dordrecht
Print ISBN: 978-94-007-2887-5
Online ISBN: 978-94-007-2888-2
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)