Cardiovascular system STIM1/Orai1-mediated store-operated Ca2+ entry in cardiovascular disease

Store-operated Ca2+ entry (SOCE) pathways: Emerging signaling concepts in human (patho)physiology

Volumn , Issue , 2012, Pages 301-325

  Motiani, Rajender K ^a   Trebak, Mohamed ^a  

^a ALBANY MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84930591518     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-3-7091-0962-5_20     Document Type: Chapter

References (129)

1. 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
2. Alexopoulos N, Raggi P (2009) Calcification in atherosclerosis. Nat Rev Cardiol 6:681-688
3. Aubart FC, Sassi Y, Coulombe A, Mougenot N, Vrignaud C, Leprince P, Lechat P, Lompre AM, Hulot JS (2009) RNA interference targeting STIM1 suppresses vascular smooth muscle cell proliferation and neointima formation in the rat. Mol Ther 17:455-462
4. Authi KS (2009) Orai1: a channel to safer antithrombotic therapy. Blood 113:1872-1873
5. 2+ entry through its constitutive and inducible movement in the endoplasmic reticulum. Proc Natl Acad Sci USA 103:16704-16709
6. 2+ pump in proliferating human arterial myocytes. Am J Physiol Cell Physiol 297:C1103-C1112
7. 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
8. 2+ entry in neurons and plays a key role in hypoxic neuronal cell death. Sci Signal 2(93):ra67
9. 2+ handling is altered when arterial myocytes progress from a contractile to a proliferative phenotype in culture. Am J Physiol Cell Physiol 295:C779-C790
10. Berridge MJ (1983) Rapid accumulation of inositol trisphosphate reveals that agonists hydrolyse polyphosphoinositides instead of phosphatidylinositol. Biochem J 212:849-858
11. Berridge MJ (1987) Inositol trisphosphate and diacylglycerol: two interacting second messengers. Annu Rev Biochem 56:159-193
12. Berridge MJ (1993) Inositol trisphosphate and calcium signalling. Nature 361:315-325
13. Berridge MJ (2003) Cardiac calcium signalling. Biochem Soc Trans 31:930-933
14. Berridge MJ, Irvine RF (1984) Inositol trisphosphate, a novel second messenger in cellular signal transduction. Nature 312:315-321
15. 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
16. 2+ levels. Cell 131:1327-1339
17. 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
18. Cahalan MD (2009) STIMulating store-operated Ca(2+) entry. Nat Cell Biol 11:669-677
19. Carrasco S, Meyer T (2010) Cracking CRAC. Nat Cell Biol 2010:416-418
20. Cheng H, Lederer WJ (2008) Calcium sparks. Physiol Rev 88:1491-1545
21. Cortes SF, Lemos VS, Stoclet JC (1997) Alterations in calcium stores in aortic myocytes from spontaneously hypertensive rats. Hypertension 29:1322-1328
22. de Groot D, Pasterkamp G, Hoefer IE (2009) Cardiovascular risk factors and collateral artery formation. Eur J Clin Invest 39:1036-1047
23. De Windt LJ, Lim HW, Bueno OF, Liang Q, Delling U, Braz JC, Glascock BJ, Kimball TF, del Monte F, Hajjar RJ, Molkentin JD (2001) Targeted inhibition of calcineurin attenuates cardiac hypertrophy in vivo. Proc Natl Acad Sci USA 98:3322-3327
24. 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
25. Devynck MA (2002) Gender and vascular smooth muscle cells: a direct influence on Ca2+ handling? J Hypertens 20:2139-2140
26. 2+ entry associated with metabolic syndrome and coronary atherosclerosis. Cardiovasc Res 85:631-640
27. Elezi S, Kastrati A, Neumann FJ, Hadamitzky M, Dirschinger J, Schomig A (1998) Vessel size and long-term outcome after coronary stent placement. Circulation 98:1875-1880
28. 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
29. Feske S (2010) CRAC channelopathies. Pflugers Arch 460:417-435
30. 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
31. Fischman DL, Leon MB, Baim DS, Schatz RA, Savage MP, Penn I, Detre K, Veltri L, Ricci D, Nobuyoshi M et al (1994) A randomized comparison of coronary-stent placement and balloon angioplasty in the treatment of coronary artery disease.Stent restenosis study investigators. N Engl J Med 331:496-501
32. Frey N, McKinsey TA, Olson EN (2000) Decoding calcium signals involved in cardiac growth and function. Nat Med 6:1221-1227
33. Frey N, Olson EN (2003) Cardiac hypertrophy: the good, the bad, and the ugly. Annu Rev Physiol 65:45-79
34. 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
35. Giachini FR, Chiao CW, Carneiro FS, Lima VV, Carneiro ZN, Dorrance AM, Tostes RC, Webb RC (2009) Increased activation of stromal interaction molecule-1/Orai-1 in aorta from hypertensive rats: a novel insight into vascular dysfunction. Hypertension 53:409-416
36. Giachini FR, Webb RC, Tostes RC (2010) STIM and Orai proteins: players in sexual differences in hypertension-associated vascular dysfunction? Clin Sci (Lond) 118:391-396
37. 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
38. Golovina VA (1999) Cell proliferation is associated with enhanced capacitative Ca(2+) entry in human arterial myocytes. Am J Physiol 277:C343-C349
39. Golovina VA, Platoshyn O, Bailey CL, Wang J, Limsuwan A, Sweeney M, Rubin LJ, Yuan JX (2001) Upregulated TRP and enhanced capacitative Ca(2+) entry in human pulmonary artery myocytes during proliferation. Am J Physiol Heart Circ Physiol 280:H746-H755
40. Grosse J, Braun A, Varga-Szabo D, Beyersdorf N, Schneider B, Zeitlmann L, Hanke P, Schropp P, Mühlstedt S, Zorn C, Huber M, Schmittwolf C, Jagla W, Yu P, Kerkau T, Schulze H, Nehls M, Nieswandt B (2007) An EF hand mutation in Stim1 causes premature platelet activation and bleeding in mice. J Clin Invest 117:3540-3550
41. Guo RW, Wang H, Gao P, Li MQ, Zeng CY, Yu Y, Chen JF, Song MB, Shi YK, Huang L (2009) An essential role for stromal interaction molecule 1 in neointima formation following arterial injury. Cardiovasc Res 81:660-668
42. Gwack Y, Sharma S, Nardone J, Tanasa B, Iuga A, Srikanth S, Okamura H, Bolton D, Feske S, Hogan PG, Rao A (2006) A genome-wide Drosophila RNAi screen identifies DYRK-family kinases as regulators of NFAT. Nature 441:646-650
43. 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 Bcell function in mice lacking ORAI1. Mol Cell Biol 28:5209-5222
44. Hagedorn I, Vogtle T, Nieswandt B (2010) Arterial thrombus formation. Novel mechanisms and targets Novel mechanisms and targets. Hamostaseologie 30:127-135
45. Hajjar I, Kotchen JM, Kotchen TA (2006) Hypertension: trends in prevalence, incidence, and control. Annu Rev Public Health 27:465-490
46. Harbour JW, Dean DC (2000) Rb function in cell-cycle regulation and apoptosis. Nat Cell Biol 2: E65-E67
47. 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
48. Hoth M, Penner R (1992) Depletion of intracellular calcium stores activates a calcium current in mast cells. Nature 355:353-356
49. House SJ, Potier M, Bisaillon J, Singer HA, Trebak M (2008) The non-excitable smooth muscle: calcium signaling and phenotypic switching during vascular disease. Pflugers Arch 456:769-785
50. Kannel WB (1974) Role of blood pressure in cardiovascular morbidity and mortality. Prog Cardiovasc Dis 17:5-24
51. Kawai-Kowase K, Owens GK (2007) Multiple repressor pathways contribute to phenotypic switching of vascular smooth muscle cells. Am J Physiol Cell Physiol 292:C59-C69
52. 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
53. Kirchhefer U, Schmitz W, Scholz H, Neumann J (1999) Activity of cAMP-dependent protein kinase and Ca2+/calmodulin-dependent protein kinase in failing and nonfailing human hearts. Cardiovasc Res 42:254-261
54. Kitazono T, Ago T, Kamouchi M, Santa N, Ooboshi H, Fujishima M, Ibayashi S (2002) Increased activity of calcium channels and Rho-associated kinase in the basilar artery during chronic hypertension in vivo. J Hypertens 20:879-884
55. 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
56. 2+ store depletion. Proc Natl Acad Sci USA 104:9301-9306
57. 2+ influx. Curr Biol 15:1235-1241
58. Liu Z, Zhang C, Dronadula N, Li Q, Rao GN (2005) Blockade of nuclear factor of activated T cells activation signaling suppresses balloon injury-induced neointima formation in a rat carotid artery model. J Biol Chem 280:14700-14708
59. Loukotova J, Kunes J, Zicha J (2002) Gender-dependent difference in cell calcium handling in VSMC isolated from SHR: the effect of angiotensin II. J Hypertens 20:2213-2219
60. 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
61. 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
62. Manji SS, Parker NJ, Williams RT, van Stekelenburg L, Pearson RB, Dziadek M, Smith PJ (2000) STIM1: a novel phosphoprotein located at the cell surface. Biochim Biophys Acta 1481:147-155
63. Mazzucato M, Pradella P, Cozzi MR, De Marco L, Ruggeri ZM (2002) Sequential cytoplasmic calcium signals in a 2-stage platelet activation process induced by the glycoprotein Ibalpha mechanoreceptor. Blood 100:2793-2800
64. McCarl CA, Picard C, Khalil S, Kawasaki T, Röther 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
65. 2+ entry cause immunodeficiency, myopathy, and ectodermal dysplasia. J Allergy Clin Immunol 124(1311-1318):e1317
66. 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
67. Michell RH (1975) Inositol phospholipids and cell surface receptor function. Biochim Biophys Acta 415:81-147
68. Mignen O, Thompson JL, Shuttleworth TJ (2008) Orai1 subunit stoichiometry of the mammalian CRAC channel pore. J Physiol 586:419-425
69. Molkentin JD, Lu JR, Antos CL, Markham B, Richardson J, Robbins J, Grant SR, Olson EN (1998) A calcineurin-dependent transcriptional pathway for cardiac hypertrophy. Cell 93:215-228
70. 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
71. 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
72. 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
73. Nagai M, Hoshide S, Kario K (2010) Hypertension and dementia. Am J Hypertens 23:116-124
74. Navarro-Borelly L, Somasundaram A, Yamashita M, Ren D, Miller RJ, Prakriya M (2008) STIM1-Orai1 interactions and Orai1 conformational changes revealed by live-cell FRET microscopy. J Physiol 586:5383-5401
75. Ohba T, Watanabe H, Murakami M, Sato T, Ono K, Ito H (2009) Essential role of STIM1 in the development of cardiomyocyte hypertrophy. Biochem Biophys Res Commun 389:172-176
76. Oka T, Hori M, Ozaki H (2005) Microtubule disruption suppresses allergic response through the inhibition of calcium influx in the mast cell degranulation pathway. J Immunol 174:4584-4589
77. Oritani K, Kincade PW (1996) Identification of stromal cell products that interact with pre-B cells. J Cell Biol 134:771-782
78. Owens GK, Kumar MS, Wamhoff BR (2004) Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol Rev 84:767-801
79. Parekh AB (2006) Cell biology: cracking the calcium entry code. Nature 441:163-165
80. Parekh AB (2010) Store-operated CRAC channels: function in health and disease. Nat Rev Drug Discov 9:399-410
81. Parekh AB, Putney JW Jr (2005) Store-operated calcium channels. Physiol Rev 85:757-810
82. 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
83. Parker NJ, Begley CG, Smith PJ, Fox RM (1996) Molecular cloning of a novel human gene (D11S4896E) at chromosomal region 11p15.5. Genomics 37:253-256
84. Passier R, Zeng H, Frey N, Naya FJ, Nicol RL, McKinsey TA, Overbeek P, Richardson JA, Grant SR, Olson EN (2000) CaM kinase signaling induces cardiac hypertrophy and activates the MEF2 transcription factor in vivo. J Clin Invest 105:1395-1406
85. 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
86. Penna A, Demuro A, Yeromin AV, Zhang SL, Safrina O, Parker I, Cahalan MD (2008) The CRAC channel consists of a tetramer formed by Stim-induced dimerization of Orai dimers. Nature 456:116-120
87. Picard C, McCarl CA, Papolos A, Khalil S, Lüthy 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
88. 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
89. Potier M, Trebak M (2008) New developments in the signaling mechanisms of the store-operated calcium entry pathway. Pflugers Arch 457:405-415
90. Putney Jr JW (2011) The physiological function of store-operated calcium entry. Neurochem Res [in press]
91. Putney JW Jr (1986) A model for receptor-regulated calcium entry. Cell Calcium 7:1-12
92. Putney JW Jr (1990) Capacitative calcium entry revisited. Cell Calcium 11:611-624
93. Raines EW (2004) PDGF and cardiovascular disease. Cytokine Growth Factor Rev 15:237-254
94. Ramirez MT, Zhao XL, Schulman H, Brown JH (1997) The nuclear deltaB isoform of Ca2+/ calmodulin-dependent protein kinase II regulates atrial natriuretic factor gene expression in ventricular myocytes. J Biol Chem 272:31203-31208
95. Rink TJ, Sage SO (1990) Calcium signaling in human platelets. Annu Rev Physiol 52:431-449
96. 2+ channel function. J Cell Biol 169:435-445
97. Sabbioni S, Barbanti-Brodano G, Croce CM, Negrini M (1997) GOK: a gene at 11p15 involved in rhabdomyosarcoma and rhabdoid tumor development. Cancer Res 57:4493-4497
98. Safar ME, Smulyan H (2004) Hypertension in women. Am J Hypertens 17:82-87
99. Schaff UY, Dixit N, Procyk E, Yamayoshi I, Tse T, Simon SI (2010) Orai1 regulates intracellular calcium, arrest, and shape polarization during neutrophil recruitment in shear flow. Blood 115:657-666
100. 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
101. Serruys PW, de Jaegere P, Kiemeneij F, Macaya C, Rutsch W, Heyndrickx G, Emanuelsson H, Marco J, Legrand V, Materne P et al (1994) A comparison of balloon-expandable-stent implantation with balloon angioplasty in patients with coronary artery disease. Benestent study group. N Engl J Med 331:489-495
102. Shuttleworth TJ (2009) Arachidonic acid, ARC channels, and Orai proteins. Cell Calcium 45:602-610
103. 2+ channel activator STIM1. J Cell Sci 120:3762-3771
104. 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
105. 2+ sensor that stabilizes CRAC channels in T cells. Nat Cell Biol 12:436-446
106. 2+ entry. J Biol Chem 281:35855-35862
107. 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
108. 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
109. Takuwa N, Zhou W, Kumada M, Takuwa Y (1993) Ca(2+)-dependent stimulation of retinoblastoma gene product phosphorylation and p34cdc2 kinase activation in serum-stimulated human fibroblasts. J Biol Chem 268:138-145
110. Ter Keurs HE, Boyden PA (2007) Calcium and arrhythmogenesis. Physiol Rev 87:457-506
111. Trebak M, St J, Bird G, McKay RR, Birnbaumer L, Putney JW Jr (2003a) Signaling mechanism for receptor-activated canonical transient receptor potential 3 (TRPC3) channels. J Biol Chem 278:16244-16252
112. Trebak M, Vazquez G, Bird GS, Putney JW Jr (2003b) The TRPC3/6/7 subfamily of cation channels. Cell Calcium 33:451-461
113. 2+ handling of smooth muscle cells in aorta of apolipoprotein E-deficient mice before development of atherosclerotic lesions. Cell Calcium 41:295-302
114. Varga-Szabo D, Authi KS, Braun A, Bender M, Ambily A, Hassock SR, Gudermann T, Dietrich A, Nieswandt B (2008a) Store-operated Ca(2+) entry in platelets occurs independently of transient receptor potential (TRP) C1. Pflugers Arch 457:377-387
115. Varga-Szabo D, Braun A, Kleinschnitz C, Bender M, Pleines I, Pham M, Renne T, Stoll G, Nieswandt B (2008b) The calcium sensor STIM1 is an essential mediator of arterial thrombosis and ischemic brain infarction. J Exp Med 205:1583-1591
116. Varga-Szabo D, Braun A, Nieswandt B (2009) Calcium signaling in platelets. J Thromb Haemost 7:1057-1066
117. 2+ entry are required in Drosophila neurons for flight. Proc Natl Acad Sci USA 106:10326-10331
118. 2+ entry. Science 312:1220-1223
119. Voelkers M, Salz M, Herzog N, Frank D, Dolatabadi N, Frey N, Gude N, Friedrich O, Koch WJ, Katus HA, Sussman MA, Most P (2010) Orai1 and Stim1 regulate normal and hypertrophic growth in cardiomyocytes. J Mol Cell Cardiol 48:1329-1334
120. Wehrens XH, Marks AR (2004) Novel therapeutic approaches for heart failure by normalizing calcium cycling. Nat Rev Drug Discov 3:565-573
121. Wellman GC, Cartin L, Eckman DM, Stevenson AS, Saundry CM, Lederer WJ, Nelson MT (2001) Membrane depolarization, elevated Ca(2+) entry, and gene expression in cerebral arteries of hypertensive rats. Am J Physiol Heart Circ Physiol 281:H2559-H2567
122. Welt FG, Edelman ER, Simon DI, Rogers C (2000) Neutrophil, not macrophage, infiltration precedes neointimal thickening in balloon-injured arteries. Arterioscler Thromb Vasc Biol 20:2553-2558
123. 2+ store depletion causes STIM1 to accumulate in ER regions closely associated with the plasma membrane. J Cell Biol 174:803-813
124. 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
125. Yu H, Sliedregt-Bol K, Overkleeft H, van der Marel GA, van Berkel TJ, Biessen EA (2006) Therapeutic potential of a synthetic peptide inhibitor of nuclear factor of activated T cells as antirestenotic agent. Arterioscler Thromb Vasc Biol 26:1531-1537
126. 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
127. 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 USA 103:9357-9362
128. 2+ store to the plasma membrane. Nature 437:902-905
129. Zhou Y, Meraner P, Kwon HT, Machnes D, Oh-hora M, Zimmer J, Huang Y, Stura A, Rao A, Hogan PG (2010) STIM1 gates the store-operated calcium channel ORAI1 in vitro. Nat Struct Mol Biol 17:112-116