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STIM-TRP Pathways

The STIM1/Orai/TRPC Channels Multiple Ca2+ Influx Complexes

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Store-operated Ca2+ entry (SOCE) pathways

Abstract

Receptor-evoked Ca2+ influx is a central component of the Ca2+ signal. A ubiquitous form of Ca2+ influx is activated by depletion of endoplasmic Ca2+ stores, the SOC channels. The two established Ca2+ influx channels that are activated by depletion of the endoplasmic reticulum Ca2+ store are the TRPC channels and the newly discovered Orai channels. The two channels can function independently and are gated by different STIM1 domains. Yet, the two channels also affect the function of each other by competition for STIM1 and by yet unresolved mechanism in which their function is required for their mutual activity. This chapter will discuss the evidence for the regulation of the Orai and TRPC channels by STIM1 and the interrelations between the two activities. The function and properties of the Orai channels and their regulation by STIM1 is extensively covered in other chapters and will only be briefly discussed here as they relate to the function of TRPC channels.

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References

  • Abdullaev IF, Bisaillon JM, Potier M, Gonzalez JC, Motiani RK, Trebak M (2008) Stim1 and Orai1 mediate CRAC currents and store-operated calcium entry important for endothelial cell proliferation. Circ Res 103:1289–1299

    Article  PubMed  CAS  Google Scholar 

  • Alicia S, Angelica Z, Carlos S, Alfonso S, 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

    Article  PubMed  CAS  Google Scholar 

  • Ambudkar IS, Ong HL, Liu X, Bandyopadhyay BC, Cheng KT (2007) TRPC1: the link between functionally distinct store-operated calcium channels. Cell Calcium 42:213–223

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Beech DJ, Xu SZ, McHugh D, Flemming R (2003) TRPC1 store-operated cationic channel subunit. Cell Calcium 33:433–440

    Article  PubMed  CAS  Google Scholar 

  • Berridge MJ (2006) Calcium microdomains: organization and function. Cell Calcium 40:405–412

    Article  PubMed  CAS  Google Scholar 

  • Berridge MJ, Bootman MD, Roderick HL (2003) Calcium signalling: dynamics, homeostasis and remodelling. Nat Rev Mol Cell Biol 4:517–529

    Article  PubMed  CAS  Google Scholar 

  • Brini M, Carafoli E (2009) Calcium pumps in health and disease. Physiol Rev 89:1341–1378

    Article  PubMed  CAS  Google Scholar 

  • Chen X, Yang D, Ma S, He H, Luo Z, Feng X, Cao T, Ma L, Yan Z, Liu D, Tepel M, Zhu Z (2010) Increased rhythmicity in hypertensive arterial smooth muscle is linked to transient receptor potential canonical channels. J Cell Mol Med 14:2483–2494

    Article  PubMed  CAS  Google Scholar 

  • DeHaven WI, Smyth JT, Boyles RR, Bird GS, Putney JW Jr (2008) Complex actions of 2-aminoethyldiphenyl borate on store-operated calcium entry. J Biol Chem 283:19265–19273

    Article  PubMed  CAS  Google Scholar 

  • DeHaven WI, Jones BF, Petranka JG, Smyth JT, Tomita T, Bird GS, Putney JW Jr (2009) TRPC channels function independently of STIM1 and Orai1. J Physiol 587:2275–2298

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Feske S, Gwack Y, Prakriya M, Srikanth S, Puppel SH, Tanasa B, Higan PG, Lewis RS, Daly M, Rao A (2006) A mutation in Orai1 causes immune deficiency by abrogating CRAC channel function. Nature 441:179–85

    Article  PubMed  CAS  Google Scholar 

  • Feske S, Picard C, Fischer A (2010) Immunodeficiency due to mutations in ORAI1 and STIM1. Clin Immunol 135:169–182

    Article  PubMed  CAS  Google Scholar 

  • Freichel M, Suh SH, Pfeifer A, Schweig U, Trost C, Weissgerber P, Biel M, Philipp S, Freise D, Droogmans G, Hofmann F, Flockerzi V, Nilius B (2001) Lack of an endothelial store-operated Ca2+ current impairs agonist-dependent vasorelaxation in TRP4−/− mice. Nat Cell Biol 3:121–127

    Article  PubMed  CAS  Google Scholar 

  • Gross SA, Guzman GA, Wissenbach U, Philipp SE, Zhu MX, Bruns D, Cavalie A (2009) TRPC5 is a Ca2+-activated channel functionally coupled to Ca2+-selective ion channels. J Biol Chem 284:34423–34432

    Article  PubMed  CAS  Google Scholar 

  • Hamilton SL, Serysheva II (2009) Ryanodine receptor structure: progress and challenges. J Biol Chem 284:4047–4051

    Article  PubMed  CAS  Google Scholar 

  • Hawkins BJ, Irrinki KM, Mallilankaraman K, Lien YC, Wang Y, Bhanumathy CD, Subbiah R, Ritchie MF, Soboloff J, Baba Y, Kurosaki T, Joseph SK, Gill DL, Madesh M (2010) S-glutathionylation activates STIM1 and alters mitochondrial homeostasis. J Cell Biol 190:391–405

    Article  PubMed  CAS  Google Scholar 

  • Hong JH, Li Q, Kim MS, Shin DM, Feske S, Birnbaumer L, Cheng KT, Ambudkar IS, Muallem S (2010) Polarized but differential localization and recruitment of STIM1, Orai1 and TRPC channels in secretory cells. Traffic 12(2):232–45

    Article  PubMed  CAS  Google Scholar 

  • Hong et al (2011) Polarized but differential localization and recruitment of STIM1, Orai1 and TRPC channels in secretory cells. Traffic 12:232–245

    Google Scholar 

  • Hoth M, Penner R (1992) Depletion of intracellular calcium stores activates a calcium current in mast cells. Nature 355:353–356

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Kim JY, Zeng W, Kiselyov K, Yuan JP, Dehoff MH, Mikoshiba K, Worley PF, Muallem S (2006) Homer 1 mediates store- and inositol 1,4,5-trisphosphate receptor-dependent translocation and retrieval of TRPC3 to the plasma membrane. J Biol Chem 281:32540–32549

    Article  PubMed  CAS  Google Scholar 

  • Kim MS, Hong JH, Li Q, Shin DM, Abramowitz J, Birnbaumer L, Muallem S (2009a) Deletion of TRPC3 in mice reduces store-operated Ca2+ influx and the severity of acute pancreatitis. Gastroenterology 137:1509–1517

    Article  PubMed  CAS  Google Scholar 

  • Kim MS, Zeng W, Yuan JP, Shin DM, Worley PF, Muallem S (2009b) Native Store-operated Ca2+ influx requires the channel function of Orai1 and TRPC1. J Biol Chem 284:9733–9741

    Article  PubMed  CAS  Google Scholar 

  • Kiselyov K, Wang X, Shin DM, Zang W, Muallem S (2006) Calcium signaling complexes in microdomains of polarized secretory cells. Cell Calcium 40:451–459

    Article  PubMed  CAS  Google Scholar 

  • Kiselyov K, Shin DM, Kim JY, Yuan JP, Muallem S (2007) TRPC channels: interacting proteins. Handb Exp Pharmacol 179:559–574

    Article  PubMed  CAS  Google Scholar 

  • Kiyonaka S, Kato K, Nishida M, Mio K, Numaga T, Sawaguchi Y, Yoshida T, Wakamori M, Mori E, Numata T, Ishii M, Takemoto H, Ojida A, Watanabe K, Uemura A, Kurose H, Morii T, Kobayashi T, Sato Y, Sato C, Hamachi I, Mori Y (2009) Selective and direct inhibition of TRPC3 channels underlies biological activities of a pyrazole compound. Proc Natl Acad Sci USA 106:5400–5405

    Article  PubMed  CAS  Google Scholar 

  • Korzeniowski MK, Manjarres IM, Varnai P, Balla T (2010) Activation of STIM1-Orai1 involves an intramolecular switching mechanism. Sci Signal 3:ra82

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Lee KP, Yuan JP, Hong JH, So I, Worley PF, Muallem S (2010a) An endoplasmic reticulum/plasma membrane junction: STIM1/Orai1/TRPCs. FEBS Lett 584:2022–2027

    Article  PubMed  CAS  Google Scholar 

  • Lee KP, Yuan JP, So I, Worley PF, Muallem S (2010b) STIM1-dependent and STIM1-independent function of transient receptor potential canonical (TRPC) channels tunes their store-operated mode. J Biol Chem 285:38666–38673

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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 U S A 106:3202–3206

    Article  PubMed  CAS  Google Scholar 

  • 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 287:C1709–C1716

    Article  CAS  Google Scholar 

  • Liou J, Kim ML, Heo WD, Jones JT, Myers JW, Ferrell JE, Meyer T (2005) STIM is a Ca2+ sensor essential for Ca2+-store-depletion-triggered Ca2+ influx. Curr Biol 15:1235–1241

    Article  PubMed  CAS  Google Scholar 

  • Liou J, Fivaz M, Inoue T, Meyer T (2007) Live-cell imaging reveals sequential oligomerization and local plasma membrane targeting of stromal interaction molecule 1 after Ca2+ store depletion. Proc Natl Acad Sci U S A 104:9301–9306

    Article  PubMed  CAS  Google Scholar 

  • Lis A, Peinelt C, Beck A, Parvez S, Monteilh-Zoller M, Fleig A, Penner R (2007) CRACM1, CRACM2, and CRACM3 are store-operated Ca(2+) channels with distinct functional properties. Curr Biol 17:794–800

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Liu X, Cheng KT, Bandyopadhyay BC, Pani B, Dietrich A, Paria BC, Swaim WD, Beech D, Yildrim E, Singh BB, Birnbaumer L, Ambudkar IS (2007) Attenuation of store-operated Ca2+ current impairs salivary gland fluid secretion in TRPC1(−/−) mice. Proc Natl Acad Sci USA 104:17542–17547

    Article  PubMed  CAS  Google Scholar 

  • Lur et al. (2011) InsP3receptors and Orai channels in pancreatic acinar cells: co-localization and its consequences Biochem J 1;436(2):231–9

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Luik RM, Wang B, Prakriya M, Wu MM, Lewis RS (2008) Oligomerization of STIM1 couples ER calcium depletion to CRAC channel activation. Nature 454:538–542

    Article  PubMed  CAS  Google Scholar 

  • Ma HT, Peng Z, Hiragun T, Iwaki S, Gilfillan AM, Beaven MA (2008) Canonical transient receptor potential 5 channel in conjunction with Orai1 and STIM1 allows Sr2+ entry, optimal influx of Ca2+, and degranulation in a rat mast cell line. J Immunol 180:2233–2239

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Mikoshiba K (2007) IP3 receptor/Ca2+ channel: from discovery to new signaling concepts. J Neurochem 102:1426–1446

    Article  PubMed  CAS  Google Scholar 

  • Montell C (2005) The TRP superfamily of cation channels. Sci STKE 2005:re3

    Article  PubMed  Google Scholar 

  • Muallem S, Fimmel CJ, Pandol SJ, Sachs G (1986) Regulation of free cytosolic Ca2+ in the peptic and parietal cells of the rabbit gastric gland. J Biol Chem 261:2660–2667

    PubMed  CAS  Google Scholar 

  • Muallem S, Schoeffield MS, Fimmel CJ, Pandol SJ (1988) Agonist-sensitive calcium pool in the pancreatic acinar cell. II. Characterization of reloading. Am J Physiol 255:G229–G235

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Ng LC, Airey JA, Hume JR (2010) The contribution of TRPC1 and STIM1 to capacitative Ca(2+) entry in pulmonary artery. Adv Exp Med Biol 661:123–135

    Article  PubMed  CAS  Google Scholar 

  • Nilius B, Owsianik G, Voets T (2008) Transient receptor potential channels meet phosphoinositides. EMBO J 27:2809–2816

    Article  PubMed  CAS  Google Scholar 

  • 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 SOC and CRAC channel components. J Biol Chem 282:9105–9116

    Article  PubMed  CAS  Google Scholar 

  • Pandol SJ, Schoeffield MS, Fimmel CJ, Muallem S (1987) The agonist-sensitive calcium pool in the pancreatic acinar cell. Activation of plasma membrane Ca2+ influx mechanism. J Biol Chem 262:16963–16968

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Pani B, Ong HL, Brazer SC, Liu X, Rauser K, Singh BB, Ambudkar IS (2009) Activation of TRPC1 by STIM1 in ER-PM microdomains involves release of the channel from its scaffold caveolin-1. Proc Natl Acad Sci U S A 106:20087–20092

    Article  PubMed  CAS  Google Scholar 

  • Parekh AB, Putney JW Jr (2005) Store-operated calcium channels. Phys Rev 85:757–810

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Patel S, Marchant JS, Brailoiu E (2010) Two-pore channels: regulation by NAADP and customized roles in triggering calcium signals. Cell Calcium 47:480–490

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Petersen OH, Tepikin AV (2008) Polarized calcium signaling in exocrine gland cells. Annu Rev Physiol 70:273–299

    Article  PubMed  CAS  Google Scholar 

  • Petersen OH, Sutton R, Criddle DN (2006) Failure of calcium microdomain generation and pathological consequences. Cell Calcium 40:593–600

    Article  PubMed  CAS  Google Scholar 

  • Pozo-Guisado E, Campbell DG, Deak M, Alvarez-Barrientos A, Morrice NA, Alvarez IS, Alessi DR, Martín-Romero FJ (2010) Phosphorylation of STIM1 at ERK1/2 target sites modulates store-operated calcium entry. J Cell Sci 123:3084–3093

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Puertollano R, Kiselyov K (2009) TRPMLs: in sickness and in health. Am J Physiol Renal Physiol 296:F1245–F1254

    Article  PubMed  CAS  Google Scholar 

  • Putney JW Jr (1986) A model for receptor-regulated calcium entry. Cell Calcium 7:1–12

    Article  PubMed  CAS  Google Scholar 

  • Rao JN, Rathor N, Zou T, Liu L, Xiao L, Yu TX, Cui YH, Wang JY (2010) STIM1 translocation to the plasma membrane enhances intestinal epithelial restitution by inducing TRPC1-mediated Ca2+ signaling after wounding. Am J Physiol 299:C579–C588

    Article  CAS  Google Scholar 

  • Rizzuto R, Pozzan T (2006) Microdomains of intracellular Ca2+: molecular determinants and functional consequences. Physiol Rev. Jan;86(1):369–408.

    Google Scholar 

  • Roos J, DiGregorio PJ, Yeromin AV, Ohlsen K, Lioudyno M, Zhang S, Safrina O, Kozak JA, Wagner SL, Cahalan MD, Veliçelebi G, Stauderman KA (2005) STIM1, an essential and conserved component of store-operated Ca2+ channel function. J Cell Biol 169:435–445

    Article  PubMed  CAS  Google Scholar 

  • Saleh SN, Albert AP, Peppiatt-Wildman CM, Large WA (2008) Diverse properties of store-operated TRPC channels activated by protein kinase C in vascular myocytes. J Physiol 586:2463–2476

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Shirakawa H, Sakimoto S, Nakao K, Sugishita A, Konno M, Iida S, Kusano A, Hashimoto E, Nakagawa T, Kaneko S (2010) Transient receptor potential canonical 3 (TRPC3) mediates thrombin-induced astrocyte activation and upregulates its own expression in cortical astrocytes. J Neurosci 30:13116–12129

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Soboloff J, Spassova MA, Dziadek MA, Gill DL (2006a) Calcium signals mediated by STIM and Orai proteins – a new paradigm in inter-organelle communication. Biochim Biophys Acta 1763:1161–1168

    Article  PubMed  CAS  Google Scholar 

  • Soboloff J, Spassova MA, Tang XD, Hewavitharana T, Xu W, Gill DL (2006b) Orai1 and STIM reconstitute store-operated calcium channel function. J Biol Chem 281:20661–20665

    Article  PubMed  CAS  Google Scholar 

  • Sours-Brothers S, Ding M, Graham S, Ma R (2009) Interaction between TRPC1/TRPC4 assembly and STIM1 contributes to store-operated Ca2+ entry in mesangial cells. Exp Biol Med 234:673–682

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Strubing C, Krapivinsky G, Krapivinsky L, Clapham DE (2003) Formation of novel TRPC channels by complex subunit interactions in embryonic brain. J Biol Chem 278:39014–39019

    Article  PubMed  Google Scholar 

  • Takahashi Y, Watanabe H, Murakami M, Ono K, Munehisa Y, Koyama T, Nobori K, Iijima T, Ito H (2007) Functional role of stromal interaction molecule 1 (STIM1) in vascular smooth muscle cells. Biochem Biophys Res Commun 361:934–940

    Article  PubMed  CAS  Google Scholar 

  • Takemura H, Hughes AR, Thastrup O, Putney JW Jr (1989) Activation of calcium entry by the tumor promoter thapsigargin in parotid acinar cells. Evidence that an intracellular calcium pool and not an inositol phosphate regulates calcium fluxes at the plasma membrane. J Biol Chem 264:12266–12271

    PubMed  CAS  Google Scholar 

  • Tamarina NA, Kuznetsov A, Philipson LH (2008) Reversible translocation of EYFP-tagged STIM1 is coupled to calcium influx in insulin secreting beta-cells. Cell Calcium 44:533–544

    Article  PubMed  CAS  Google Scholar 

  • Tiruppathi C, Freichel M, Vogel SM, Paria BC, Mehta D, Flockerzi V, Malik AB (2002) Impairment of store-operated Ca2+ entry in TRPC4(−/−) mice interferes with increase in lung microvascular permeability. Circ Res 91:70–6

    Article  PubMed  CAS  Google Scholar 

  • Van Baelen K, Dode L, Vanoevelen J, Callewaert G, De Smedt H, Missiaen L, Parys JB, Raeymaekers L, Wuytack F (2004) The Ca2+/Mn2+ pumps in the Golgi apparatus. Biochim Biophys Acta 1742:103–112

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Vig M, Beck A, Billingsley JM, Lis A, Parvez S, Peinelt C, Koomoa DL, Soboloff J, Gill DL, Fleig A, Kinet JP, Penner R (2006a) CRACM1 multimers form the ion-selective pore of the CRAC channel. Curr Biol 16:2073–2079

    Article  PubMed  CAS  Google Scholar 

  • Vig M, Peinelt C, Beck A, Koomoa DL, Rabah D, Koblan-Huberson M, Kraft S, Turner H, Fleig A, Penner R, Kinet JP (2006b) CRACM1 is a plasma membrane protein essential for store-operated Ca2+ entry. Science 312:1220–1223

    Article  PubMed  CAS  Google Scholar 

  • Villereal ML (2006) Mechanism and functional significance of TRPC channel multimerization. Semin Cell Dev Biol 17:618–629

    Article  PubMed  CAS  Google Scholar 

  • Wuytack F, Raeymaekers L, Missiaen L (2002) Molecular physiology of the SERCA and SPCA pumps. Cell Calcium 32:279–305

    Article  PubMed  CAS  Google Scholar 

  • Xu SZ, Boulay G, Flemming R, Beech DJ (2006) E3-targeted anti-TRPC5 antibody inhibits store-operated calcium entry in freshly isolated pial arterioles. Am J Physiol Heart Circ Physiol 291:H2653–H2659

    Article  PubMed  CAS  Google Scholar 

  • Xu SZ, Sukumar P, Zeng F, Li J, Jairaman A, English A, Naylor J, Ciurtin C, Majeed Y, Milligan CJ, Bahnasi YM, Al-Shawaf E, Porter KE, Jiang LH, Emery P, Sivaprasadarao A, Beech DJ (2008) TRPC channel activation by extracellular thioredoxin. Nature 451:69–72

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Yu F, Sun L, Machaca K (2009) Orai1 internalization and STIM1 clustering inhibition modulate SOCE inactivation during meiosis. Proc Natl Acad Sci U S A 106:17401–17406

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Zhang SL, Yeromin AV, Zhang XH, Yu Y, Safrina O, Penna A, Roos J, Stauderman KA, Cahalan MD (2006) Genome-wide RNAi screen of Ca(2+) influx identifies genes that regulate Ca(2+) release-activated Ca(2+) channel activity. Proc Natl Acad Sci U S A 103:9357–9362

    Article  PubMed  CAS  Google Scholar 

  • Zhang ZY, Pan LJ, Zhang ZM (2010) Functional interactions among STIM1, Orai1 and TRPC1 on the activation of SOCs in HL-7702 cells. Amino Acids 39:195–204

    Article  PubMed  CAS  Google Scholar 

  • Zweifach A, Lewis RS (1995) Rapid inactivation of depletion-activated calcium current (ICRAC) due to local calcium feedback. J Gen Physiol 105:209–226

    Article  PubMed  CAS  Google Scholar 

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Correspondence to Shmuel Muallem .

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Hong, J.H., Kim, M.S., Lee, K.P., Yuan, J.P., Muallem, S. (2012). STIM-TRP Pathways. In: Groschner, K., Graier, W., Romanin, C. (eds) Store-operated Ca2+ entry (SOCE) pathways. Springer, Vienna. https://doi.org/10.1007/978-3-7091-0962-5_5

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