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Store-Operated Ca²⁺ Entry (SOCE) Pathways pp 189–210Cite as

STIM-TRP Pathways and Microdomain Organization: Auxiliary Proteins of the STIM/Orai Complex

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Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 993))

Abstract

The basic paradigm of a mechanism for calcium influx triggered after a reduction on calcium store content implies a sensor of calcium concentration on the endoplasmic reticulum (the stores) and a calcium channel immersed on the plasma membrane. These two basic components are STIM and Orai, the most fundamental and minimal molecular constituents of the store-operated calcium entry mechanism. However, even when minimal components can be reduced to these two proteins, the intricate process involved in approximating two cellular membranes (endoplasmic reticulum, ER and plasma membrane, PM) require the participation of several other components, many of which remain unidentified to this date. Here we review several of the proteins identified as constituents of the so-called store-operated calcium influx complex (SOCIC) and discuss their role in modulating this complex phenomenon.

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References

  • Albarran L, Lopez JJ, Amor NB, Martin-Cano FE, Berna-Erro A, Smani T, Salido GM, Rosado JA (2016) Dynamic interaction of SARAF with STIM1 and Orai1 to modulate store-operated calcium entry. Sci Rep 6:24452

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Asanov A, Sherry R, Sampieri A, Vaca L (2013) A relay mechanism between EB1 and APC facilitate STIM1 puncta assembly at endoplasmic reticulum-plasma membrane junctions. Cell Calcium 54(3):246–256

    Article  CAS  PubMed  Google Scholar 

  • Bakowski D, Glitsch MD, Parekh AB (2001) An examination of the secretion-like coupling model for the activation of the Ca2+ release-activated Ca2+ current I(CRAC) in RBL-1 cells. J Physiol 532(Pt 1):55–71

    Article  CAS  PubMed  PubMed Central  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(23):6089–6091

    Article  CAS  PubMed  Google Scholar 

  • Berridge MJ (1993) Inositol trisphosphate and calcium signalling. Nature 361(6410):315–325

    Article  CAS  PubMed  Google Scholar 

  • Berridge MJ, Irvine RF (1984) Inositol trisphosphate, a novel second messenger in cellular signal transduction. Nature 312(5992):315–321

    Article  CAS  PubMed  Google Scholar 

  • Bertin A, McMurray MA, Thai L, Garcia G 3rd, Votin V, Grob P, Allyn T, Thorner J, Nogales E (2010) Phosphatidylinositol-4,5-bisphosphate promotes budding yeast septin filament assembly and organization. J Mol Biol 404(4):711–731

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bird GS, Hwang SY, Smyth JT, Fukushima M, Boyles RR, Putney JW Jr (2009) STIM1 is a calcium sensor specialized for digital signaling. Curr Biol 19(20):1724–1729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bogeski I, Kilch T, Niemeyer BA (2012) ROS and SOCE: recent advances and controversies in the regulation of STIM and Orai. J Physiol 590(17):4193–4200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carrasco S, Meyer T (2011) STIM proteins and the endoplasmic reticulum-plasma membrane junctions. Annu Rev Biochem 80:973–1000

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chang LF, Chen S, Liu CC, Pan X, Jiang J, Bai XC, Xie X, Wang HW, Sui SF (2012) Structural characterization of full-length NSF and 20S particles. Nat Struct Mol Biol 19(3):268–275

    Article  CAS  PubMed  Google Scholar 

  • Chang CL, Hsieh TS, Yang TT, Rothberg KG, Azizoglu DB, Volk E, Liao JC, Liou J (2013) Feedback regulation of receptor-induced Ca2+ signaling mediated by E-Syt1 and Nir2 at endoplasmic reticulum-plasma membrane junctions. Cell Rep 5(3):813–825

    Article  PubMed  CAS  Google Scholar 

  • Cheng JP, Nichols BJ (2016) Caveolae: one function or many? Trends Cell Biol 26(3):177–189

    Article  CAS  PubMed  Google Scholar 

  • Cooper DM (2015) Store-operated Ca(2)(+)-entry and adenylyl cyclase. Cell Calcium 58(4):368–375

    Article  CAS  PubMed  Google Scholar 

  • Cross BM, Hack A, Reinhardt TA, Rao R (2013) SPCA2 regulates Orai1 trafficking and store independent Ca2+ entry in a model of lactation. PLoS One 8(6):e67348

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dionisio N, Smani T, Woodard GE, Castellano A, Salido GM, Rosado JA (2015) Homer proteins mediate the interaction between STIM1 and Cav1.2 channels. Biochim Biophys Acta 1853(5):1145–1153

    Article  CAS  PubMed  Google Scholar 

  • Dolmetsch RE, Xu K, Lewis RS (1998) Calcium oscillations increase the efficiency and specificity of gene expression. Nature 392(6679):933–936

    Article  CAS  PubMed  Google Scholar 

  • Feng JM, Fernandes AO, Campagnoni CW, Hu YH, Campagnoni AT (2004) The golli-myelin basic protein negatively regulates signal transduction in T lymphocytes. J Neuroimmunol 152(1–2):57–66

    Article  CAS  PubMed  Google Scholar 

  • Feng JM, YK H, Xie LH, Colwell CS, Shao XM, Sun XP, Chen B, Tang H, Campagnoni AT (2006) Golli protein negatively regulates store depletion-induced calcium influx in T cells. Immunity 24(6):717–727

    Article  CAS  PubMed  Google Scholar 

  • Feng M, Grice DM, Faddy HM, Nguyen N, Leitch S, Wang Y, Muend S, Kenny PA, Sukumar S, Roberts-Thomson SJ, Monteith GR, Rao R (2010) Store-independent activation of Orai1 by SPCA2 in mammary tumors. Cell 143(1):84–98

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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(7090):179–185

    Article  CAS  PubMed  Google Scholar 

  • Fierro L, Parekh AB (1999) Fast calcium-dependent inactivation of calcium release-activated calcium current (CRAC) in RBL-1 cells. J Membr Biol 168(1):9–17

    Article  CAS  PubMed  Google Scholar 

  • Frischauf I, Schindl R, Derler I, Bergsmann J, Fahrner M, Romanin C (2008) The STIM/Orai coupling machinery. Channels 2(4):261–268

    Article  PubMed  Google Scholar 

  • Frischauf I, Zayats V, Deix M, Hochreiter A, Jardin I, Muik M, Lackner B, Svobodova B, Pammer T, Litvinukova M, Sridhar AA, Derler I, Bogeski I, Romanin C, Ettrich RH, Schindl R (2015) A calcium-accumulating region, CAR, in the channel Orai1 enhances Ca2+ permeation and SOCE-induced gene transcription. Sci Signal 8(408):ra131

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Fujii Y, Shiota M, Ohkawa Y, Baba A, Wanibuchi H, Kinashi T, Kurosaki T, Baba Y (2012) Surf4 modulates STIM1-dependent calcium entry. Biochem Biophys Res Commun 422(4):615–620

    Article  CAS  PubMed  Google Scholar 

  • Galan C, Dionisio N, Smani T, Salido GM, Rosado JA (2011) The cytoskeleton plays a modulatory role in the association between STIM1 and the Ca2+ channel subunits Orai1 and TRPC1. Biochem Pharmacol 82(4):400–410

    Article  CAS  PubMed  Google Scholar 

  • Galjart N (2010) Plus-end-tracking proteins and their interactions at microtubule ends. Curr Biol 20(12):R528–R537

    Article  CAS  PubMed  Google Scholar 

  • Giordano F, Saheki Y, Idevall-Hagren O, Colombo SF, Pirruccello M, Milosevic I, Gracheva EO, Bagriantsev SN, Borgese N, De Camilli P (2013) PI(4,5)P(2)-dependent and Ca(2+)-regulated ER-PM interactions mediated by the extended synaptotagmins. Cell 153(7):1494–1509

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grigoriev I, Gouveia SM, van der Vaart B, Demmers J, Smyth JT, Honnappa S, Splinter D, Steinmetz MO, Putney JW Jr, Hoogenraad CC, Akhmanova A (2008) STIM1 is a MT-plus-end-tracking protein involved in remodeling of the ER. Curr Biol 18(3):177–182

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Groden J, Thliveris A, Samowitz W, Carlson M, Gelbert L, Albertsen H, Joslyn G, Stevens J, Spirio L, Robertson M et al (1991) Identification and characterization of the familial adenomatous polyposis coli gene. Cell 66(3):589–600

    Article  CAS  PubMed  Google Scholar 

  • Hajkova Z, Bugajev V, Draberova E, Vinopal S, Draberova L, Janacek J, Draber P, Draber P (2011) STIM1-directed reorganization of microtubules in activated mast cells. J Immunol 186(2):913–923

    Article  CAS  PubMed  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(3):391–405

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Honnappa S, Gouveia SM, Weisbrich A, Damberger FF, Bhavesh NS, Jawhari H, Grigoriev I, van Rijssel FJ, Buey RM, Lawera A, Jelesarov I, Winkler FK, Wuthrich K, Akhmanova A, Steinmetz MO (2009) An EB1-binding motif acts as a microtubule tip localization signal. Cell 138(2):366–376

    Article  CAS  PubMed  Google Scholar 

  • Hoth M, Penner R (1993) Calcium release-activated calcium current in rat mast cells. J Physiol 465:359–386

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hou X, Pedi L, Diver MM, Long SB (2012) Crystal structure of the calcium release-activated calcium channel Orai. Science 338(6112):1308–1313

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jardin I, Albarran L, Bermejo N, Salido GM, Rosado JA (2012) Homers regulate calcium entry and aggregation in human platelets: a role for Homers in the association between STIM1 and Orai1. Biochem J 445(1):29–38

    Article  CAS  PubMed  Google Scholar 

  • Jha A, Ahuja M, Maleth J, Moreno CM, Yuan JP, Kim MS, Muallem S (2013) The STIM1 CTID domain determines access of SARAF to SOAR to regulate Orai1 channel function. J Cell Biol 202(1):71–79

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jing J, He L, Sun A, Quintana A, Ding Y, Ma G, Tan P, Liang X, Zheng X, Chen L, Shi X, Zhang SL, Zhong L, Huang Y, Dong MQ, Walker CL, Hogan PG, Wang Y, Zhou Y (2015) Proteomic mapping of ER-PM junctions identifies STIMATE as a regulator of Ca influx. Nat Cell Biol 17(10):1339–1347

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kar P, Parekh AB (2015) Distinct spatial Ca2+ signatures selectively activate different NFAT transcription factor isoforms. Mol Cell 58(2):232–243

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kar P, Nelson C, Parekh AB (2011) Selective activation of the transcription factor NFAT1 by calcium microdomains near Ca2+ release-activated Ca2+ (CRAC) channels. J Biol Chem 286(17):14795–14803

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Korzeniowski MK, Popovic MA, Szentpetery Z, Varnai P, Stojilkovic SS, Balla T (2009) Dependence of STIM1/Orai1-mediated calcium entry on plasma membrane phosphoinositides. J Biol Chem 284(31):21027–21035

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Krapivinsky G, Krapivinsky L, Stotz SC, Manasian Y, Clapham DE (2011) POST, partner of stromal interaction molecule 1 (STIM1), targets STIM1 to multiple transporters. Proc Natl Acad Sci U S A 108(48):19234–19239

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Laude AJ, Prior IA (2004) Plasma membrane microdomains: organization, function and trafficking. Mol Membr Biol 21(3):193–205

    Article  CAS  PubMed  PubMed Central  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 U S A 106(34):14687–14692

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Levental I, Grzybek M, Simons K (2010) Greasing their way: lipid modifications determine protein association with membrane rafts. Biochemistry 49(30):6305–6316

    Article  CAS  PubMed  Google Scholar 

  • Lindquist JA, Jensen ON, Mann M, Hammerling GJ (1998) ER-60, a chaperone with thiol-dependent reductase activity involved in MHC class I assembly. EMBO J 17(8):2186–2195

    Article  CAS  PubMed  PubMed Central  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(13):1235–1241

    Article  CAS  PubMed  PubMed Central  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(22):9301–9306

    Article  CAS  PubMed  PubMed Central  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 Ca2+ channels with distinct functional properties. Curr Biol 17(9):794–800

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Zheng X, Mueller GA, Sobhany M, DeRose EF, Zhang Y, London RE, Birnbaumer L (2012) Crystal structure of calmodulin binding domain of orai1 in complex with Ca2+ calmodulin displays a unique binding mode. J Biol Chem 287(51):43030–43041

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Macian F (2005) NFAT proteins: key regulators of T-cell development and function. Nat Rev Immunol 5(6):472–484

    Article  CAS  PubMed  Google Scholar 

  • Maleth J, Choi S, Muallem S, Ahuja M (2014) Translocation between PI(4,5)P2-poor and PI(4,5)P2-rich microdomains during store depletion determines STIM1 conformation and Orai1 gating. Nat Commun 5:5843

    Article  PubMed  PubMed Central  Google Scholar 

  • Mangolini A, de Stephanis L, Aguiari G (2016) Role of calcium in polycystic kidney disease: from signaling to pathology. World J Nephrol 5(1):76–83

    Article  PubMed  PubMed Central  Google Scholar 

  • Maurice T, Su TP (2009) The pharmacology of sigma-1 receptors. Pharmacol Ther 124(2):195–206

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miao Y, Miner C, Zhang L, Hanson PI, Dani A, Vig M (2013) An essential and NSF independent role for alpha-SNAP in store-operated calcium entry. elife 2:e00802

    Article  PubMed  PubMed Central  Google Scholar 

  • Miederer AM, Alansary D, Schwar G, Lee PH, Jung M, Helms V, Niemeyer BA (2015) A STIM2 splice variant negatively regulates store-operated calcium entry. Nat Commun 6:6899

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mitrovic S, Ben-Tekaya H, Koegler E, Gruenberg J, Hauri HP (2008) The cargo receptors Surf4, endoplasmic reticulum-Golgi intermediate compartment (ERGIC)-53, and p25 are required to maintain the architecture of ERGIC and Golgi. Mol Biol Cell 19(5):1976–1990

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Molinari M, Helenius A (1999) Glycoproteins form mixed disulphides with oxidoreductases during folding in living cells. Nature 402(6757):90–93

    Article  CAS  PubMed  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(12):8014–8022

    Article  CAS  PubMed  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(9):1678–1689

    Article  CAS  PubMed  PubMed Central  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 U S A 106(36):15495–15500

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mullins FM, Yen M, Lewis RS (2016) Orai1 pore residues control CRAC channel inactivation independently of calmodulin. J Gen Physiol 147(2):137–152

    Article  PubMed  PubMed Central  Google Scholar 

  • Na SS, Aldonza MB, Sung HJ, Kim YI, Son YS, Cho S, Cho JY (2015) Stanniocalcin-2 (STC2): a potential lung cancer biomarker promotes lung cancer metastasis and progression. Biochim Biophys Acta 1854(6):668–676

    Article  CAS  PubMed  Google Scholar 

  • Nathke IS (2004) The adenomatous polyposis coli protein: the Achilles heel of the gut epithelium. Annu Rev Cell Dev Biol 20:337–366

    Article  PubMed  CAS  Google Scholar 

  • Nilius B, Owsianik G (2011) The transient receptor potential family of ion channels. Genome Biol 12(3):218

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oliver JD, van der Wal FJ, Bulleid NJ, High S (1997) Interaction of the thiol-dependent reductase ERp57 with nascent glycoproteins. Science 275(5296):86–88

    Article  CAS  PubMed  Google Scholar 

  • Oliver JD, Roderick HL, Llewellyn DH, High S (1999) ERp57 functions as a subunit of specific complexes formed with the ER lectins calreticulin and calnexin. Mol Biol Cell 10(8):2573–2582

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Palty R, Raveh A, Kaminsky I, Meller R, Reuveny E (2012) SARAF inactivates the store operated calcium entry machinery to prevent excess calcium refilling. Cell 149(2):425–438

    Article  CAS  PubMed  Google Scholar 

  • Pani B, Singh BB (2009) Lipid rafts/caveolae as microdomains of calcium signaling. Cell Calcium 45(6):625–633

    Article  CAS  PubMed  PubMed Central  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(47):20087–20092

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Parekh AB (1998) Slow feedback inhibition of calcium release-activated calcium current by calcium entry. J Biol Chem 273(24):14925–14932

    Article  CAS  PubMed  Google Scholar 

  • Pike LJ (2004) Lipid rafts: heterogeneity on the high seas. Biochem J 378(Pt 2):281–292

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pozo-Guisado E, Casas-Rua V, Tomas-Martin P, Lopez-Guerrero AM, Alvarez-Barrientos A, Martin-Romero FJ (2013) Phosphorylation of STIM1 at ERK1/2 target sites regulates interaction with the microtubule plus-end binding protein EB1. J Cell Sci 126(Pt 14):3170–3180

    Article  CAS  PubMed  Google Scholar 

  • Prakriya M, Lewis RS (2015) Store-operated calcium channels. Physiol Rev 95(4):1383–1436

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Preston SF, Sha’afi RI, Berlin RD (1991) Regulation of Ca2+ influx during mitosis: Ca2+ influx and depletion of intracellular Ca2+ stores are coupled in interphase but not mitosis. Cell Regul 2(11):915–925

    CAS  PubMed  PubMed Central  Google Scholar 

  • Prins D, Groenendyk J, Touret N, Michalak M (2011) Modulation of STIM1 and capacitative Ca2+ entry by the endoplasmic reticulum luminal oxidoreductase ERp57. EMBO Rep 12(11):1182–1188

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Quintana A, Pasche M, Junker C, Al-Ansary D, Rieger H, Kummerow C, Nunez L, Villalobos C, Meraner P, Becherer U, Rettig J, Niemeyer BA, Hoth M (2011) Calcium microdomains at the immunological synapse: how ORAI channels, mitochondria and calcium pumps generate local calcium signals for efficient T-cell activation. EMBO J 30(19):3895–3912

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Quintana A, Rajanikanth V, Farber-Katz S, Gudlur A, Zhang C, Jing J, Zhou Y, Rao A, Hogan PG (2015) TMEM110 regulates the maintenance and remodeling of mammalian ER-plasma membrane junctions competent for STIM-ORAI signaling. Proc Natl Acad Sci U S A 112(51):E7083–E7092

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ribeiro CM, Reece J, Putney JW Jr (1997) Role of the cytoskeleton in calcium signaling in NIH 3T3 cells. An intact cytoskeleton is required for agonist-induced [Ca2+]i signaling, but not for capacitative calcium entry. J Biol Chem 272(42):26555–26561

    Article  CAS  PubMed  Google Scholar 

  • Ritchie MF, Samakai E, Soboloff J (2012) STIM1 is required for attenuation of PMCA-mediated Ca2+ clearance during T-cell activation. EMBO J 31(5):1123–1133

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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(3):435–445

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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(11):7527–7533

    Article  CAS  PubMed  Google Scholar 

  • Sampieri A, Zepeda A, Asanov A, Vaca L (2009) Visualizing the store-operated channel complex assembly in real time: identification of SERCA2 as a new member. Cell Calcium 45(5):439–446

    Article  CAS  PubMed  Google Scholar 

  • Sathish V, Abcejo AJ, Thompson MA, Sieck GC, Prakash YS, Pabelick CM (2012) Caveolin-1 regulation of store-operated Ca(2+) influx in human airway smooth muscle. Eur Respir J 40(2):470–478

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sharma S, Quintana A, Findlay GM, Mettlen M, Baust B, Jain M, Nilsson R, Rao A, Hogan PG (2013) An siRNA screen for NFAT activation identifies septins as coordinators of store-operated Ca2+ entry. Nature 499(7457):238–242

    Article  CAS  PubMed  Google Scholar 

  • Smyth JT, DeHaven WI, Bird GS, Putney JW 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

    Article  CAS  PubMed  PubMed Central  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(12):1465–1472

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Soboloff J, Rothberg BS, Madesh M, Gill DL (2012) STIM proteins: dynamic calcium signal transducers. Nat Rev Mol Cell Biol 13(9):549–565

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Srikanth S, Gwack Y (2013) Orai1-NFAT signalling pathway triggered by T cell receptor stimulation. Mol Cell 35(3):182–194

    Article  CAS  Google Scholar 

  • Srikanth S, Jung HJ, Kim KD, Souda P, Whitelegge J, Gwack Y (2010) A novel EF-hand protein, CRACR2A, is a cytosolic Ca2+ sensor that stabilizes CRAC channels in T cells. Nat Cell Biol 12(5):436–446

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Srikanth S, Jew M, Kim KD, Yee MK, Abramson J, Gwack Y (2012) Junctate is a Ca2+-sensing structural component of Orai1 and stromal interaction molecule 1 (STIM1). Proc Natl Acad Sci U S A 109(22):8682–8687

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Srivats S, Balasuriya D, Pasche M, Vistal G, Edwardson JM, Taylor CW, Murrell-Lagnado RD (2016) Sigma1 receptors inhibit store-operated Ca2+ entry by attenuating coupling of STIM1 to Orai1. J Cell Biol 213(1):65–79

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takeshima H, Hoshijima M, Song LS (2015) Ca(2)(+) microdomains organized by junctophilins. Cell Calcium 58(4):349–356

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Turano C, Gaucci E, Grillo C, Chichiarelli S (2011) ERp57/GRP58: a protein with multiple functions. Cell Mol Biol Lett 16(4):539–563

    Article  CAS  PubMed  Google Scholar 

  • Vaca L (2010) SOCIC: the store-operated calcium influx complex. Cell Calcium 47(3):199–209

    Article  CAS  PubMed  Google Scholar 

  • Vanoevelen J, Dode L, Van Baelen K, Fairclough RJ, Missiaen L, Raeymaekers L, Wuytack F (2005) The secretory pathway Ca2+/Mn2+-ATPase 2 is a Golgi-localized pump with high affinity for Ca2+ ions. J Biol Chem 280(24):22800–22808

    Article  CAS  PubMed  Google Scholar 

  • Vanoverberghe K, Lehen’kyi V, Thebault S, Raphael M, Vanden Abeele F, Slomianny C, Mariot P, Prevarskaya N (2012) Cytoskeleton reorganization as an alternative mechanism of store-operated calcium entry control in neuroendocrine-differentiated cells. PLoS One 7(9):e45615

    Article  CAS  PubMed  PubMed Central  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 (2006) CRACM1 is a plasma membrane protein essential for store-operated Ca2+ entry. Science 312(5777):1220–1223

    Article  CAS  PubMed  Google Scholar 

  • Vitre B, Coquelle FM, Heichette C, Garnier C, Chretien D, Arnal I (2008) EB1 regulates microtubule dynamics and tubulin sheet closure in vitro. Nat Cell Biol 10(4):415–421

    Article  CAS  PubMed  Google Scholar 

  • Volland S, Kugler W, Schweigerer L, Wilting J, Becker J (2009) Stanniocalcin 2 promotes invasion and is associated with metastatic stages in neuroblastoma. Int J Cancer 125(9):2049–2057

    Article  CAS  PubMed  Google Scholar 

  • Walsh CM, Chvanov M, Haynes LP, Petersen OH, Tepikin AV, Burgoyne RD (2010a) Role of phosphoinositides in STIM1 dynamics and store-operated calcium entry. Biochem J 425(1):159–168

    Article  CAS  Google Scholar 

  • Walsh CM, Doherty MK, Tepikin AV, Burgoyne RD (2010b) Evidence for an interaction between Golli and STIM1 in store-operated calcium entry. Biochem J 430(3):453–460

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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(6000):105–109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Willoughby D, Cooper DM (2007) Organization and Ca2+ regulation of adenylyl cyclases in cAMP microdomains. Physiol Rev 87(3):965–1010

    Article  CAS  PubMed  Google Scholar 

  • Willoughby D, Everett KL, Halls ML, Pacheco J, Skroblin P, Vaca L, Klussmann E, Cooper DM (2012) Direct binding between Orai1 and AC8 mediates dynamic interplay between Ca2+ and cAMP signaling. Sci Signal 5(219):ra29

    Article  PubMed  Google Scholar 

  • Winter U, Chen X, Fasshauer D (2009) A conserved membrane attachment site in alpha-SNAP facilitates N-ethylmaleimide-sensitive factor (NSF)-driven SNARE complex disassembly. J Biol Chem 284(46):31817–31826

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Woo JS, Srikanth S, Nishi M, Ping P, Takeshima H, Gwack Y (2016) Junctophilin-4, a component of the endoplasmic reticulum-plasma membrane junctions, regulates Ca2+ dynamics in T cells. Proc Natl Acad Sci U S A 113(10):2762–2767

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Woodward OM, Li Y, Yu S, Greenwell P, Wodarczyk C, Boletta A, Guggino WB, Qian F (2010) Identification of a polycystin-1 cleavage product, P100, that regulates store operated Ca entry through interactions with STIM1. PLoS One 5(8):e12305

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Wu J, Lai M, Shao C, Wang J, Wei JJ (2015) STC2 overexpression mediated by HMGA2 is a biomarker for aggressiveness of high-grade serous ovarian cancer. Oncol Rep 34(3):1494–1502

    Article  CAS  PubMed  Google Scholar 

  • Yeh YC, Parekh AB (2015) Distinct structural domains of caveolin-1 independently regulate Ca2+ release-activated Ca2+ channels and Ca2+ microdomain-dependent gene expression. Mol Cell Biol 35(8):1341–1349

    Article  CAS  PubMed  PubMed Central  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(41):17401–17406

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu F, Sun L, Machaca K (2010) Constitutive recycling of the store-operated Ca2+ channel Orai1 and its internalization during meiosis. J Cell Biol 191(3):523–535

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu F, Sun L, Hubrack S, Selvaraj S, Machaca K (2013) Intramolecular shielding maintains the ER Ca(2)(+) sensor STIM1 in an inactive conformation. J Cell Sci 126(Pt 11):2401–2410

    Article  CAS  PubMed  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(3):337–343

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yuan JP, Lee KP, Hong JH, Muallem S (2012) The closing and opening of TRPC channels by Homer1 and STIM1. Acta Physiol (Oxf) 204(2):238–247

    Article  CAS  Google Scholar 

  • Zeiger W, Ito D, Swetlik C, Oh-hora M, Villereal ML, Thinakaran G (2011) Stanniocalcin 2 is a negative modulator of store-operated calcium entry. Mol Cell Biol 31(18):3710–3722

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang J, Kong C, Xie H, McPherson PS, Grinstein S, Trimble WS (1999) Phosphatidylinositol polyphosphate binding to the mammalian septin H5 is modulated by GTP. Curr Biol 9(24):1458–1467

    Article  CAS  PubMed  Google Scholar 

  • Zheng L, Stathopulos PB, Li GY, Ikura M (2008) Biophysical characterization of the EF-hand and SAM domain containing Ca2+ sensory region of STIM1 and STIM2. Biochem Biophys Res Commun 369(1):240–246

    Article  CAS  PubMed  Google Scholar 

  • Zweifach A, Lewis RS (1996) Calcium-dependent potentiation of store-operated calcium channels in T lymphocytes. J Gen Physiol 107(5):597–610

    Article  CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. Instituto de Fisiología Celular, Universidad Nacional Autónoma de México, Ciudad Universitaria, México, DF, 04510, Mexico

    Jonathan Pacheco & Luis Vaca

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  1. Jonathan Pacheco
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  2. Luis Vaca
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Correspondence to Luis Vaca .

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Editors and Affiliations

  1. Institute of Biophysics, Medical University of Graz, Graz, Austria

    Klaus Groschner

  2. Institute of Molecular Biology and Biochemistry, Medical University of Graz, Graz, Austria

    Wolfgang F. Graier

  3. Institute of Biophysics, Johannes Kepler University Linz, Linz, Austria

    Christoph Romanin

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Pacheco, J., Vaca, L. (2017). STIM-TRP Pathways and Microdomain Organization: Auxiliary Proteins of the STIM/Orai Complex. In: Groschner, K., Graier, W., Romanin, C. (eds) Store-Operated Ca²⁺ Entry (SOCE) Pathways. Advances in Experimental Medicine and Biology, vol 993. Springer, Cham. https://doi.org/10.1007/978-3-319-57732-6_10

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