Store-operated calcium channels: New Perspectives on mechanism and function

Cold Spring Harbor Perspectives in Biology

Volumn 3, Issue 12, 2011, Pages

  Lewis, Richard S ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CALCIUM CHANNEL;

BIOLOGICAL MODEL; CALCIUM SIGNALING; CELL MEMBRANE; CHEMISTRY; ENAMEL; ENDOPLASMIC RETICULUM; GENETICS; HUMAN; LYMPHOCYTE; METABOLISM; PHYSIOLOGY; REVIEW; SKELETAL MUSCLE; SWEAT GLAND; THROMBOCYTE;

BLOOD PLATELETS; CALCIUM; CALCIUM CHANNELS; CALCIUM SIGNALING; CELL MEMBRANE; DENTAL ENAMEL; ENDOPLASMIC RETICULUM; HUMANS; LYMPHOCYTES; MODELS, BIOLOGICAL; MUSCLE, SKELETAL; SWEAT GLANDS;

EID: 84859618951     PISSN: None     EISSN: 19430264     Source Type: Journal    
DOI: 10.1101/cshperspect.a003970     Document Type: Review

References (156)

1. Baba Y, Kurosaki T. 2009. Physiological function and molecular basis of STIM1-mediated calcium entry in immune cells. Immunol Rev 231: 174-188.
2. 2+ entry through its constitutive and inducible movement in the endoplasmic reticulum. Proc Natl Acad Sci 103: 16704-16709.
3. Baba Y, Nishida K, Fujii Y, Hirano T, Hikida M, Kurosaki T. 2008. Essential function for the calcium sensor STIM1 in mast cell activation and anaphylactic responses. Nat Immunol 9: 81-88.
4. Barr VA, Bernot KM, Srikanth S, Gwack Y, Balagopalan L, Regan CK, Helman DJ, Sommers CL, Oh-Hora M, Rao A, et al. 2008. Dynamic movement of the calcium sensor STIM1 and the calcium channel Orai1 in activated T-cells: Puncta and distal caps. Mol Biol Cell 19: 2802-2817.
5. Bautista DM, Lewis RS. 2004. Modulation of plasma membrane calcium-ATPase activity by local calcium microdomains near CRAC channels in human T cells. J Physiol 556: 805-817.
6. 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.
7. Beyersdorf N, Braun A, Vögtle 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.
8. Bogeski I, Kummerow C, Al-Ansary D, Schwarz EC, Koehler R, Kozai D, Takahashi N, Peinelt C, Griesemer D, Bozem M, et al. 2010. Differential redox regulation of ORAI ion channels: A mechanism to tune cellular calcium signaling. Sci Signal 3: ra24.
9. 2+ levels. Cell 131: 1327-1339.
10. Braun A, Varga-Szabo D, Kleinschnitz C, Pleines I, Bender M, Austinat M, Bösl M, Stoll G, Nieswandt B. 2009. Orai1 (CRACM1) is the platelet SOC channel and essential for pathological thrombus formation. Blood 113: 2056-2063.
11. Cahalan MD, Zhang SL, Yeromin AV, Ohlsen K, Roos J, Stauderman KA. 2007. Molecular basis of the CRAC channel. Cell Calcium 42: 133-144.
12. 2+ stores and on electrostatic interactions. Mol Biol Cell 20: 389-399.
13. 2+ Influx By Interacting With The C-Terminal Acidic Coiled-Coil Of Orai1. Biochemistry 49: 1067-1071.
14. 2+ (CRAC) channels stimulates production of an intracellular messenger and an intercellular pro-inflammatory signal. J Biol Chem 283: 4622-4631.
15. 2+ signals required for specific cell functions. PLoS Biol 9: e1001025.
16. Covington ED, Wu MM, Lewis RS. 2010. Essential role for the CRAC activation domain in store-dependent oligomerization of STIM1. Mol Biol Cell 21: 1897-1907.
17. Darbellay B, Arnaudeau S, König S, Jousset H, Bader C, Demaurex N, Bernheim L. 2008. STIM1 and Orai1-dependent store-operated calciumentry regulates human myoblast differentiation. J Biol Chem 284: 5370-5380.
18. 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.
19. DeHaven WI, Jones BF, Petranka JG, Smyth JT, Tomita T, Bird GS, Putney JW. 2009. TRPC channels function independently of STIM1 and Orai1. J Physiol 587: 2275-2298.
20. Derler I, Fahrner M, Carugo O, Muik M, Bergsmann J, Schindl R, Frischauf I, Eshaghi S, Romanin C. 2009a. Increased hydrophobicity at the N terminus/membrane interface impairs gating of the severe combined immunodeficiency-related ORAI1 mutant. J Biol Chem 284: 15903-15915.
21. 2+-dependent inactivation of ORAI1 channels. J Biol Chem 284: 24933-24938.
22. 2+ oscillations through the spatial signature drives gene expression. Curr Biol 19: 853-858.
23. 2+ entry in skeletal muscle. J Physiol 587: 3139-3147.
24. i oscillations in T lymphocytes. J Gen Physiol 103: 365-388.
25. 2+ response amplitude and duration. Nature 386: 855-858.
26. Dolmetsch RE, Xu K, Lewis RS. 1998. Calcium oscillations increase the efficiency and specificity of gene expression. Nature 392: 933-936.
27. 2+ entry in skeletal muscle. Cell Calcium 47: 458-467.
28. Ercan E, Momburg F, Engel U, Temmerman K, Nickel W, Seedorf M. 2009. A conserved, lipid-mediated sorting mechanism of yeast Ist2 and mammalian STIM proteins to the peripheral ER. Traffic 10: 1802-1818.
29. Fahrner M, Muik M, Derler I, Schindl R, Fritsch R, Frischauf I, Romanin C. 2009. Mechanistic view on domains mediating STIM1-Orai coupling. Immunol Rev 231: 99-112.
30. Feng J-M, Hu YK, Xie L-H, Colwell CS, Shao XM, Sun X-P, Chen B, Tang H, Campagnoni AT. 2006. Golli protein negatively regulates store depletion-induced calcium influx in T cells. Immunity 24: 717-727.
31. 2+ entry in the immune system and beyond. Immunol Rev 231: 189-209.
32. Feske S. 2010. CRAC channelopathies. Pflugers Arch 460: 417-435.
33. 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.
34. + channel gating in T cells from immunodeficient patients. J Exp Med 202: 651-662.
35. Feske S, Gwack Y, Prakriya M, Srikanth S, Puppel S, Tanasa B, Hogan P, Lewis R, Daly M, Rao A. 2006. A mutation in Orai1 causes immune deficiency by abrogating CRAC channel function. Nature 441: 179-185.
36. 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.
37. Grigoriev I, Gouveia SM, van der Vaart B, Demmers J, Smyth JT, Honnappa S, Splinter D, Steinmetz MO, Putney JW, Hoogenraad CC, Akhmanova A. 2008. STIM1 is a MT-plus-end-tracking protein involved in remodeling of the ER. Curr Biol 18: 177-182.
38. 2+-selective ion channels. J Biol Chem 284: 34423-34432.
39. 2+ indicators with greatly improved fluorescence properties. J Biol Chem 260: 3440-3450.
40. Gwack Y, Srikanth S, Oh-Hora M, Hogan PG, Lamperti ED, Yamashita M, Gelinas C, Neems DS, Sasaki Y, Feske S, Rao A, et al. 2008. Hair loss and defective T-and B-cell function in mice lacking ORAI1. Mol Cell Biol 28: 5209-5222.
41. Hawkins BJ, Irrinki KM, Mallilankaraman K, Wang Y, Bhanumathy CD, Subbiah R, Ritchie MF, Soboloff J, Baba Y, Kurosaki T, Madesh M, et al. 2010. S-glutathionylation activates STIM1 and alters mitochondrial homeostasis. J Cell Biol 190: 391-405.
42. 2+]. J Cell Biol 140: 325-334.
43. Hogan PG, Lewis RS, Rao A. 2010. Molecular basis of calcium signaling in lymphocytes: STIM and ORAI. Annu Rev Immunol 28: 491-533.
44. Honnappa S, Gouveia SM, Weisbrich A, Damberger FF, Bhavesh NS, Jawhari H, Grigoriev I, van Rijssel, Buey RM, Lawera A, Steinmetz MO, et al. 2009. An EB1-binding motif acts as a microtubule tip localization signal. Cell 138: 366-376.
45. Hoover PJ, Lewis RS. 2011. Stoichiometric requirements for trapping and gating of CRAC channels by stromal interaction molecule 1 (STIM1). Proc Natl Acad Sci doi: 10.1073/pnas.1101664108.
46. Hoth M. 1995. Calcium and barium permeation through calcium release-activated calcium (CRAC) channels. Pflugers Archiv Eur J Physiol 430: 315-322.
47. Hoth M, Penner R. 1992. Depletion of intracellular calcium stores activates a calcium current in mast cells. Nature 355: 353-356.
48. Hoth M, Penner R. 1993. Calcium release-activated calcium current in rat mast cells. J Physiol 465: 359-386.
49. crac and TRPC1 channels. Nat Cell Biol 8: 1003-1010.
50. Ji W, Xu P, Li Z, Lu J, Liu L, Zhan Y, Chen Y, Hille B, Xu T, Chen L. 2008. Functional stoichiometry of the unitary calcium-release-activated calcium channel. Proc Natl Acad Sci 105: 13668-13673.
51. Kar P, Nelson C, Parekh AB. 2011. Selective activation of the transcription factor NFAT1 by calcium microdomains near CRAC channels. J Biol Chem 286: 14795-14803.
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. Korzeniowski M, Popovic M, Szentpetery Z, Varnai P, Stojilkovic S, Balla T. 2009. Dependence of stim1/orai1 mediated calcium entry on plasma membrane phosphoinositides. J Biol Chem 284: 21027-21035.
54. Korzeniowski MK, Manjarrés IM, Varnai P, Balla T. 2010. Activation of STIM1-Orai1 involves an intramolecular switching mechanism. Sci Signal 3: ra82.
55. 2+ release in mammalian skeletal muscle. J Physiol 583: 81-97.
56. 2+ entry in skeletal muscle. Pflugers Arch 460: 813-823.
57. 2+-dependent inactivation and gating of the Orai channels. Proc Natl Acad Sci 106: 14687-14692.
58. 2+ current in human leukemic T cells. Cell Regul 1: 99-112.
59. 2+ channel activation. J Biol Chem 282: 29448-29456.
60. Li Z, Liu L, Deng Y, Ji W, Du W, Xu P, Chen L, Xu T. 2011. Graded activation of CRAC channel by binding of different numbers of STIM1 to Orai1 subunits. Cell Res 21: 305-315.
61. 2+ influx. Curr Biol 15: 1235-1241.
62. 2+ store depletion. Proc Natl Acad Sci 104: 9301-9306.
63. Lioudyno M, Kozak J, Penna A, Safrina O, Zhang S, Sen D, Roos J, Stauderman K, Cahalan M. 2008. Orai1 and STIM1 move to the immunological synapse and are up-regulated during T cell activation. Proc Natl Acad Sci 105: 2011-2016.
64. 2+ channels with distinct functional properties. Curr Biol 17: 794-800.
65. 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.
66. SOC) in liver cells: A role for calmodulin. J Physiol 558: 85-97.
67. 2+ entry: Local activation of CRAC channels by STIM1 at ER-plasma membrane junctions. J Cell Biol 174: 815-825.
68. Luik R, Wang B, Prakriya M, Wu M, Lewis R. 2008. Oligomerization of STIM1 couples ER calcium depletion to CRAC channel activation. Nature 454: 538-542.
69. 3 Receptors. Curr Biol 19: 1648-1653.
70. Madl J, Weghuber J, Fritsch R, Derler I, Fahrner M, Frischauf I, Lackner B, Romanin C, Schütz GJ. 2010. Resting-state Orai1 diffuses as homotetramer in the plasma membrane of live mammalian cells. J Biol Chem 285: 41135-41142.
71. 2+ overload. J Cell Sci 121: 3133-3139.
72. Manji S, Parker N, Williams R, van Stekelenburg L, Pearson R, Dziadek M, Smith P. 2000. STIM1: A novel phosphoprotein located at the cell surface. Biochim Biophys Acta 1481: 147-155.
73. 2+ permeability of unstimulated rat lymphocytes. J Biol Chem 266: 10872-10879.
74. 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.
75. 2+ entry cause immunodeficiency, myopathy, and ectodermal dysplasia. J Allergy Clin Immunol 124: 1311-1318. e7.
76. McNally BA, Yamashita M, Engh A, Prakriya M. 2009. Structural determinants of ion permeation in CRAC channels. Proc Natl Acad Sci 106: 22516-22521.
77. Mercer J, Dehaven W, Smyth J, Wedel B, Boyles R, Bird G, Putney J. 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.
78. 2+selective (ARC) channels without store depletion or translocation to the plasma membrane. J Physiol (Lond) 579: 703-715.
79. Mignen O, Thompson JL, Shuttleworth TJ. 2008. Orai1 subunit stoichiometry of the mammalian CRAC channel pore. J Physiol (Lond) 586: 419-425.
80. 2+-selective ARC channel is a pentameric assembly of Orai1 and Orai3 subunits. J Physiol 587: 4181-4197.
81. Muik M, Frischauf I, Derler I, Fahrner M, Bergsmann J, Eder P, Schindl R, Hesch C, Polzinger B, Fritsch R, Romanin C, et al. 2008. Dynamic coupling of the putative coiled-coil domain of ORAI1 with STIM1 mediates ORAI1 channel activation. J Biol Chem 283: 8014-8022.
82. 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.
83. 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.
84. 2+-dependent inactivation of CRAC channels. Proc Natl Acad Sci 106: 15495-15500.
85. 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.
86. 2+ microdomains to spatially and temporally distinct cellular responses by the tyrosine kinase Syk. J Biol Chem 284: 24767-24772.
87. Oh-Hora M. 2009. Calcium signaling in the development and function of T-lineage cells. Immunol Rev 231: 210-224.
88. Oh-Hora M, Yamashita M, Hogan P, 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.
89. Orci L, Ravazzola M, LeCoadic M, Shen W-W, Demaurex N, Cosson P. 2009. STIM1-induced precortical and cortical subdomains of the endoplasmic reticulum. Proc Natl Acad Sci 106: 19358-19362.
90. Pan Z, Yang D, Nagaraj RY, Nosek TA, Nishi M, Takeshima H, Cheng H, Ma J. 2002. Dysfunction of store-operated calcium channel in muscle cells lacking mg29. Nat Cell Biol 4: 379-383.
91. Parekh AB, Penner R. 1997. Store depletion and calcium influx. Physiol Rev 77: 901-930.
92. Parekh AB, Putney JW. 2005. Store-operated calcium channels. Physiol Rev 85: 757-810.
93. 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.
94. 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.
95. 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.
96. Peinelt C, Vig M, Koomoa D, Beck A, Nadler M, Koblan-Huberson M, Lis A, Fleig A, Penner R, Kinet J. 2006. Amplification of CRAC current by STIM1 and CRACM1 (Orai1). Nat Cell Biol 8: 771-773.
97. 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.
98. Penner R, Matthews G, Neher E. 1988. Regulation of calcium influx by second messengers in rat mast cells. Nature 334: 499-504.
99. Picard C, McCarl C-A, 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.
100. 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.
101. Prakriya M, Lewis R. 2006. Regulation of CRAC channel activity by recruitment of silent channels to a high openprobability gating mode. J Gen Physiol 128: 373-386.
102. Prakriya M, Lewis R, Maue R, Bittar E. 2004. Store-operated calcium channels: Properties, functions and the search for a molecular mechanism. Adv Molec Cell Biol 32: 121-140.
103. Prakriya M, Feske S, Gwack Y, Srikanth S, Rao A, Hogan P. 2006. Orai1 is an essential pore subunit of the CRAC channel. Nature 443: 230-233.
104. Putney JW. 1986. A model for receptor-regulated calcium entry. Cell Calcium 7: 1-12.
105. Putney JW. 2009. Capacitative calcium entry: From concept to molecules. Immunol Rev 231: 10-22.
106. Putney JW, Bird GS. 1993. The inositol phosphate-calcium signaling system in nonexcitable cells. Endocr Rev 14: 610-631.
107. 2+ channel function. J Cell Biol 169: 435-445.
108. Sarkadi B, Tordai A, Homolya L, Scharff O, Gárdos G. 1991. Calcium influx and intracellular calcium release in anti-CD3 antibody-stimulated and thapsigargin-treated human T lymphoblasts. J Membr Biol 123: 9-21.
109. 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.
110. Shuttleworth TJ. 2009. Arachidonic acid, ARC channels, and Orai proteins. Cell Calcium 45: 602-610.
111. 2+ store to the plasma membrane in cells with depolarised mitochondria. J Biol Chem 286: 12189-12201.
112. 2+ channel activator STIM1. J Cell Sci 120: 3762-3771.
113. 2+-storedependent and-independent reversal of Stim1 localization and function. J Cell Sci 121: 762-772.
114. Smyth JT, Petranka JG, Boyles RR, DeHaven WI, Fukushima M, Johnson KL, Williams JG, Putney JW. 2009. Phosphorylation of STIM1 underlies suppression of storeoperated calcium entry during mitosis. Nat Cell Biol 11: 1465-1472.
115. Soboloff J, Spassova M, Tang X, Hewavitharana T, Xu W, Gill D. 2006. Orai1 and STIM reconstitute store-operated calcium channel function. J Biol Chem 281: 20661-20665.
116. 2+ sensor that stabilizes CRAC channels in T cells. Nat Cell Biol 12: 436-446.
117. 2+ channels. J Biol Chem 285: 5066-5075.
118. 2+ entry. J Biol Chem 281: 35855-35862.
119. Stathopulos PB, Zheng L, Li G-Y, Plevin MJ, Ikura M. 2008. Structural and mechanistic insights into STIM1-mediated initiation of store-operated calcium entry. Cell 135: 110-122.
120. Stemmer, Paul M, Klee, Claude B. 1994. Dual calcium ion regulation of calcineurin by calmodulin and calcineurin B. Biochemistry 33: 6859-6866.
121. Stiber J, Hawkins A, Wang S, Burch J, Graham V, Ward CC, Seth M, Finch E, Malouf N, Williams RS, Rosenberg P, et al. 2008. STIM1 signalling controls store-operated calcium entry required for development and contractile function in skeletal muscle. Nat Cell Biol 10: 688-697.
122. Südhof TC, Rothman JE. 2009. Membrane fusion: Grappling with SNARE and SM proteins. Science 323: 474-477.
123. Thastrup O, Dawson AP, Scharff O, Foder B, Cullen PJ, Drøbak BK, Bjerrum PJ, Christensen SB, Hanley MR. 1989. Thapsigargin, a novel molecular probe for studying intracellular calcium release and storage. Agents Actions 27: 17-23.
124. 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.
125. 3 receptors and/or calcium store depletion. J Cell Biol 166: 537-548.
126. 2+ influx occurs at stable plasma membrane and endoplasmic reticulum junctions. J Cell Sci 123: 4170-4181.
127. Varga-Szabo D, Braun A, Kleinschnitz C, Bender M, Pleines I, Pham M, Renné 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.
128. Varga-Szabo D, Braun A, Nieswandt B. 2009. Calcium signaling in platelets. J Thromb Haemost 7: 1057-1066.
129. Várnai P, Tó th B, Tó th DJ, Hunyady L, Balla T. 2007. Visualization and manipulation of plasma membrane-endoplasmic reticulum contact sites indicates the presence of additional molecular components within the STIM1-Orai1 Complex. J Biol Chem 282: 29678-29690.
130. Várnai P, Hunyady L, Balla T. 2009. STIM and Orai: The long-awaited constituents of store-operated calcium entry. Trends Pharmacol Sci 30: 118-128.
131. Vig M, Kinet J-P. 2009. Calcium signaling in immune cells. Nat Immunol 10: 21-27.
132. Vig M, Beck A, Billingsley J, Lis A, Parvez S, Peinelt C, Koomoa D, Soboloff J, Gill D, Fleig A, Penner R, et al. 2006a. CRACM1 multimers form the ion-selective pore of the CRAC channel. Curr Biol 16: 2073-2079.
133. 2+ entry. Science 312: 1220-1223.
134. Vig M, DeHaven W, Bird G, Billingsley J, Wang H, Rao P, Hutchings A, Jouvin M, Putney J, Kinet J. 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.
135. 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: 159-168.
136. 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: 453-460.
137. V1.2 channels. Science 330: 105-109.
138. Williams R, Manji S, Parker N, Hancock M, Van Stekelenburg L, Eid J, Senior P, Kazenwadel J, Shandala T, Saint R. 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.
139. 2+ regulation of adenylyl cyclases in cAMP microdomains. Physiol Rev 87: 965-1010.
140. 2+ store depletion. AmJ Physiol, Cell Physiol 294: C1323-C1331.
141. 2+ store depletion causes STIM1 to accumulate in ER regions closely associated with the plasma membrane. J Cell Biol 174: 803-813.
142. 2+ entry. Cell Calcium 42: 163-172.
143. 2+ influx and modulates gene expression. Nat Chem Biol 7: 351-358.
144. 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.
145. 2+dependent fast inactivation of CRAC channels: Evidence for coupling of permeation and gating. J Gen Physiol 130: 525-540.
146. Yeromin A, Zhang S, Jiang W, Yu Y, Safrina O, Cahalan M. 2006. Molecular identification of the CRAC channel by altered ion selectivity in a mutant of Orai. Nature 443: 226-229.
147. Yu F, Sun L, Machaca K. 2009. Orai1 internalization and STIM1 clustering inhibition modulate SOCE inactivation during meiosis. Proc Natl Acad Sci 106: 17401-17406.
148. 2+ channel Orai1 and its internalization during meiosis. J Cell Biol 191: 523-535.
149. Yuan J, Zeng W, Dorwart M, Choi Y, Worley P, Muallem S. 2009. SOAR and the polybasic STIM1 domains gate and regulate Orai channels. Nat Cell Biol 11: 337-343.
150. 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.
151. 2+ store to the plasma membrane. Nature 437: 902-905.
152. 2+ channel activity. Proc Natl Acad Sci 103: 9357-9362.
153. Zhou Y, Meraner P, Kwon HT, Machnes D, Masatsugu O-H, Zimmer J, Huang Y, Stura A, Rao A, Hogan PG. 2010a. STIM1 gates the store-operated calcium channel ORAI1 in vitro. Nat Struct Mol Biol 17: 112-116.
154. Zhou Y, Ramachandran S, Oh-hora M, Rao A, Hogan PG. 2010b. Pore architecture of the ORAI1 store-operated calcium channel. Proc Natl Acad Sci 107: 4896-4901.
155. 2+ stores. Proc Natl Acad Sci 90: 6295-6299.
156. CRAC) due to local calcium feedback. J Gen Physiol 105: 209-226.