Orais and STIMs: Physiological mechanisms and disease

Journal of Cellular and Molecular Medicine

Volumn 16, Issue 3, 2012, Pages 407-424

  Berna Erro, A ^a   Woodard, G E ^b   Rosado, J A ^a  

^a UNIVERSITY OF EXTREMADURA   (Spain)

^b NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

CRAC; Immunodeficiency; Orai; STIM; Store operated Ca 2+ entry

Indexed keywords

CALCIUM; CALCIUM CHANNEL; CELL ADHESION MOLECULE; MEMBRANE PROTEIN; ORAI1 PROTEIN, HUMAN; STIM1 PROTEIN, HUMAN; STIM2 PROTEIN, HUMAN; TUMOR PROTEIN;

ANIMAL; AUTOIMMUNE DISEASE; CALCIUM SIGNALING; CELL MEMBRANE; DROSOPHILA MELANOGASTER; ENDOPLASMIC RETICULUM; GENETICS; HUMAN; IMMUNOLOGY; METABOLISM; MOUSE; MUTATION; PATHOPHYSIOLOGY; REVIEW;

ANIMALS; AUTOIMMUNE DISEASES; CALCIUM; CALCIUM CHANNELS; CALCIUM SIGNALING; CELL ADHESION MOLECULES; CELL MEMBRANE; DROSOPHILA MELANOGASTER; ENDOPLASMIC RETICULUM; HUMANS; MEMBRANE PROTEINS; MICE; MUTATION; NEOPLASM PROTEINS;

DROSOPHILA MELANOGASTER; MUS;

EID: 84857558050     PISSN: 15821838     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1582-4934.2011.01395.x     Document Type: Review

References (152)

1. Berridge MJ, Lipp P, Bootman MD. The versatility and universality of calcium signalling. Nat Rev Mol Cell Biol. 2000; 1: 11-21.
2. Berridge MJ, Irvine RF. Inositol phosphates and cell signalling. Nature. 1989; 341: 197-205.
3. 2+ mobilization by ryanodine receptors is due to all-or-none release from functionally discrete intracellular stores. Biochem J. 1994; 301: 879-83.
4. 2+-signalling patterns by NAADP in pancreatic acinar cells. Nature. 1999; 398: 74-6.
5. Churchill GC, Okada Y, Thomas JM, et al.NAADP mobilizes Ca(2+) from reserve granules, lysosome-related organelles, in sea urchin eggs. Cell. 2002; 111: 703-8.
6. Xu SZ, Muraki K, Zeng F, et al.A sphingosine-1-phosphate-activated calcium channel controlling vascular smooth muscle cell motility. Circ Res. 2006; 98: 1381-9.
7. Sage SO The Wellcome Prize Lecture. Calcium entry mechanisms in human platelets. Exp Physiol. 1997; 82: 807-23.
8. 2+ entry. Curr Biol. 1992; 2: 312-4.
9. Salido GM, Sage SO, Rosado JA. TRPC channels and store-operated Ca(2+) entry. Biochim Biophys Acta. 2009; 1793: 223-30.
10. Parekh AB, Putney JWJr. Store-operated calcium channels. Physiol Rev. 2005; 85: 757-810.
11. Hoth M, Penner R. Depletion of intracellular calcium stores activates a calcium current in mast cells. Nature. 1992; 355: 353-6.
12. 2+ stores. Proc Natl Acad Sci USA. 1993; 90: 6295-9.
13. 2+ entry. Science. 2006; 312: 1220-3.
14. Peinelt C, Vig M, Koomoa DL, et al.Amplification of CRAC current by STIM1 and CRACM1 (Orai1). Nat Cell Biol. 2006; 8: 771-3.
15. Prakriya M, Feske S, Gwack Y, et al.Orai1 is an essential pore subunit of the CRAC channel. Nature. 2006; 443: 230-3.
16. Prakriya M The molecular physiology of CRAC channels. Immunol Rev. 2009; 231: 88-98.
17. Lis A, Zierler S, Peinelt C, et al.A single lysine in the N-terminal region of store-operated channels is critical for STIM1-mediated gating. J Gen Physiol. 2010; 136: 673-86.
18. 2+ entry. Biochem Biophys Res Commun. 2007; 356: 45-52.
19. Muik M, Frischauf I, Derler I, et al.Dynamic coupling of the putative coiled-coil domain of ORAI1 with STIM1 mediates ORAI1 channel activation. J Biol Chem. 2008; 283: 8014-22.
20. 2+ channel activation. J Biol Chem. 2007; 282: 29448-56.
21. 2+-dependent inactivation of CRAC channels. Proc Natl Acad Sci USA. 2009; 106: 15495-500.
22. Feske S, Gwack Y, Prakriya M, et al.A mutation in Orai1 causes immune deficiency by abrogating CRAC channel function. Nature. 2006; 441: 179-85.
23. 2+-dependent fast inactivation of CRAC channels: evidence for coupling of permeation and gating. J Gen Physiol. 2007; 130: 525-40.
24. Mercer JC, Dehaven WI, Smyth JT, et al.Large store-operated calcium selective currents due to co-expression of Orai1 or Orai2 with the intracellular calcium sensor, Stim1. J Biol Chem. 2006; 281: 24979-90.
25. Flourakis M, Van Coppenolle F, Lehen 'kyi V, et al.Passive calcium leak via translocon is a first step for iPLA2-pathway regulated store operated channels activation. FASEB J. 2006; 20: 1215-7.
26. Rosado JA, Sage SO. Platelet signalling: calcium. In: Gresele P, Page CP, Fuster V, Vermylen J, editors. Platelets in thrombotic and non-thrombotic disorders pathophysiology, pharmacology and therapeutics. Cambridge: Cambridge University Press, 2000. p. 260-71.
27. Berridge MJ, Bootman MD, Roderick HL. Calcium signalling: dynamics, homeostasis and remodelling. Nat Rev Mol Cell Biol. 2003; 4: 517-29.
28. 2+ ATPase 2 (SERCA2) activity: cell biological implications. Cell Calcium. 2005; 38: 291-302.
29. Aulestia FJ, Redondo PC, Rodriguez -Garcia A, et al.Two distinct calcium pools in the endoplasmic reticulum of HEK-293T cells. Biochem J. 2011; 435: 227-35.
30. Petersen OH, Gerasimenko OV, Gerasimenko JV, et al.The calcium store in the nuclear envelope. Cell Calcium. 1998; 23: 87-90.
31. 2+ from a thapsigargin-sensitive store in the nuclear envelope by activating ryanodine receptors. J Cell Biol. 2003; 163: 271-82.
32. 2+ signaling. Trends Cell Biol. 2010; 20: 277-86.
33. +-ATPases in human platelets. Biochem J. 2005; 390: 243-52.
34. Jacobson J, Duchen MR. Interplay between mitochondria and cellular calcium signalling. Mol Cell Biochem. 2004; 256-257: 209-18.
35. Walsh C, Barrow S, Voronina S, et al.Modulation of calcium signalling by mitochondria. Biochim Biophys Acta. 2009; 1787: 1374-82.
36. 2+ entry: dynamic interplay between endoplasmic reticulum, mitochondria and plasma membrane. J Physiol. 2003; 547: 333-48.
37. 2+ refilling of the endoplasmic reticulum. J Biol Chem. 2005; 280: 12114-22.
38. Missiaen L, Van Acker K, Van Baelen K, et al.Calcium release from the Golgi apparatus and the endoplasmic reticulum in HeLa cells stably expressing targeted aequorin to these compartments. Cell Calcium. 2004; 36: 479-87.
39. 2+ release from endoplasmic reticulum and Golgi. J Biol Chem. 2007; 282: 3325-36.
40. 2+ pumps in the Golgi apparatus. Biochim Biophys Acta. 2004; 1742: 103-12.
41. 2+ accumulation in the Golgi apparatus of HeLa cells assessed via RNA-mediated interference. Biochem Biophys Res Commun. 2003; 306: 430-6.
42. 2+ store. Pflugers Arch. 2003; 446: 148-53.
43. Putney JW, Bird GS. Cytoplasmic calcium oscillations and store-operated calcium influx. J Physiol. 2008; 586: 3055-9.
44. del Monte F, Hajjar RJ, Harding SE. Overwhelming evidence of the beneficial effects of SERCA gene transfer in heart failure. Circ Res. 2001; 88: E66-7.
45. Auffret A, Gautheron V, Mattson MP, et al.Progressive age-related impairment of the late long-term potentiation in Alzheimer's disease presenilin-1 mutant knock-in mice. J Alzheimers Dis. 2010; 19: 1021-33.
46. Vanoevelen J, Dode L, Raeymaekers L, et al.Diseases involving the Golgi calcium pump. Subcell Biochem. 2007; 45: 385-404.
47. Richter M, Schleithoff L, Deufel T, et al.Functional characterization of a distinct ryanodine receptor mutation in human malignant hyperthermia-susceptible muscle. J Biol Chem. 1997; 272: 5256-60.
48. 2+ channels. Pflugers Arch. 2010; 460: 361-74.
49. Kiselyov K, Soyombo A, Muallem S. TRPpathies. J Physiol. 2007; 578: 641-53.
50. Nilius B, Owsianik G, Voets T, et al. Transient receptor potential cation channels in disease. Physiol Rev. 2007; 87: 165-217.
51. Putney JW Jr A model for receptor-regulated calcium entry. Cell Calcium. 1986; 7: 1-12.
52. 2+ channel function. J Cell Biol. 2005; 169: 435-45.
53. 2+ store to the plasma membrane. Nature. 2005; 437: 902-5.
54. Abdullaev IF, Bisaillon JM, Potier M, et al.Stim1 and Orai1 mediate CRAC currents and store-operated calcium entry important for endothelial cell proliferation. Circ Res. 2008; 103: 1289-99.
55. 2+ stores. J Biol Chem. 2006; 281: 28254-64.
56. Stiber J, Hawkins A, Zhang ZS, et al.STIM1 signalling controls store-operated calcium entry required for development and contractile function in skeletal muscle. Nat Cell Biol. 2008; 10: 688-97.
57. Frischauf I, Muik M, Derler I, et al.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. 2009; 284: 21696-706.
58. 2+ entry. J Biol Chem. 2006; 281: 35855-62.
59. Zheng L, Stathopulos PB, Schindl R, et al.Auto-inhibitory role of the EF-SAM domain of STIM proteins in store-operated calcium entry. Proc Natl Acad Sci USA. 2011; 108: 1337-42.
60. Schindl R, Muik M, Fahrner M, et al.Recent progress on STIM1 domains controlling Orai activation. Cell Calcium. 2009; 46: 227-32.
61. Yuan JP, Zeng W, Dorwart MR, et al.SOAR and the polybasic STIM1 domains gate and regulate Orai channels. Nat Cell Biol. 2009; 11: 337-43.
62. Muik M, Fahrner M, Derler I, et al.A cytosolic homomerization and a modulatory domain within STIM1 C terminus determine coupling to ORAI1 channels. J Biol Chem. 2009; 284: 8421-6.
63. Park CY, Hoover PJ, Mullins FM, et al.STIM1 clusters and activates CRAC channels via direct binding of a cytosolic domain to Orai1. Cell. 2009; 136: 876-90.
64. Kawasaki T, Lange I, Feske S. A minimal regulatory domain in the C terminus of STIM1 binds to and activates ORAI1 CRAC channels. Biochem Biophys Res Commun. 2009; 385: 49-54.
65. Wang Y, Deng X, Gill DL. Calcium signaling by STIM and Orai: intimate coupling details revealed. Sci Signal. 2010; 3: pe42.
66. 2+ sensory region of STIM1 and STIM2. Biochem Biophys Res Commun. 2008; 369: 240-6.
67. 2+ entry. Curr Biol. 2006; 16: 1465-70.
68. 2+ levels. Cell. 2007; 131: 1327-39.
69. Parvez S, Beck A, Peinelt C, et al.STIM2 protein mediates distinct store-dependent and store-independent modes of CRAC channel activation. FASEB J. 2008; 22: 752-61.
70. 2+ entry in neurons and plays a key role in hypoxic neuronal cell death. Sci Signal. 2009; 2: ra67.
71. 2+ ATPases (SERCA) pumps silently refill the endoplasmic reticulum. J Biol Chem. 2007; 282: 11456-64.
72. 2+ stores and associates with Orai1 upon depletion of the acidic stores in human platelets. J Biol Chem. 2011; 286: 12257-70.
73. 2+ entry cause immunodeficiency, myopathy, and ectodermal dysplasia. J Allergy Clin Immunol. 2009; 124: 1311-8 e7.
74. Gwack Y, Srikanth S, Feske S, et al.Biochemical and functional characterization of Orai proteins. J Biol Chem. 2007; 282: 16232-43.
75. Su AI, Wiltshire T, Batalov S, et al.A gene atlas of the mouse and human protein-encoding transcriptomes. Proc Natl Acad Sci USA. 2004; 101: 6062-7.
76. Wissenbach U, Philipp SE, Gross SA, et al.Primary structure, chromosomal localization and expression in immune cells of the murine ORAI and STIM genes. Cell Calcium. 2007; 42: 439-46.
77. Williams RT, Manji SS, Parker NJ, et al.Identification and characterization of the STIM (stromal interaction molecule) gene family: coding for a novel class of transmembrane proteins. Biochem J. 2001; 357: 673-85.
78. Picard C, McCarl CA, Papolos A, et al.STIM1 mutation associated with a syndrome of immunodeficiency and autoimmunity. N Engl J Med. 2009; 360: 1971-80.
79. Skibinska-Kijek A, Wisniewska MB, Gruszczynska-Biegala J, et al.Immunolocalization of STIM1 in the mouse brain. Acta Neurobiol Exp (Wars). 2009; 69: 413-28.
80. Overall ML, Parker NJ, Scarcella DL, et al.Murine Stim1 maps to distal chromosome 7 and is not imprinted. Mamm Genome. 1998; 9: 657-9.
81. Zhou Y, Mancarella S, Wang Y, et al.The short N-terminal domains of STIM1 and STIM2 control the activation kinetics of Orai1 channels. J Biol Chem. 2009; 284: 19164-8.
82. El Boustany C, Katsogiannou M, Delcourt P, et al.Differential roles of STIM1, STIM2 and Orai1 in the control of cell proliferation and SOCE amplitude in HEK293 cells. Cell Calcium. 2010; 47: 350-9.
83. Feske S, Giltnane J, Dolmetsch R, et al.Gene regulation mediated by calcium signals in T lymphocytes. Nat Immunol. 2001; 2: 316-24.
84. + channel gating in T cells from immunodeficient patients. J Exp Med. 2005; 202: 651-62.
85. Byun M, Abhyankar A, Lelarge V, et al.Whole-exome sequencing-based discovery of STIM1 deficiency in a child with fatal classic Kaposi sarcoma. J Exp Med. 2010; 207: 2307-12.
86. Le Deist F, Hivroz C, Partiseti M, et al.A primary T-cell immunodeficiency associated with defective transmembrane calcium influx. Blood. 1995; 85: 1053-62.
87. Partiseti M, Le Deist F, Hivroz C, et al.The calcium current activated by T cell receptor and store depletion in human lymphocytes is absent in a primary immunodeficiency. J Biol Chem. 1994; 269: 32327-35.
88. Feske S, Picard C, Fischer A. Immunodeficiency due to mutations in ORAI1 and STIM1. Clin Immunol. 2010; 135: 169-82.
89. 2+ entry in the immune system and beyond. Immunol Rev. 2009; 231: 189-209.
90. 2+ channel function in the heterozygous condition. J Biol Chem. 2009; 284: 6620-6.
91. Feske S CRAC channelopathies. Pflugers Arch. 2010; 460: 417-35.
92. Feske S, Muller JM, Graf D, et al.Severe combined immunodeficiency due to defective binding of the nuclear factor of activated T cells in T lymphocytes of two male siblings. Eur J Immunol. 1996; 26: 2119-26.
93. Feske S, Draeger R, Peter HH, et al.The duration of nuclear residence of NFAT determines the pattern of cytokine expression in human SCID T cells. J Immunol. 2000; 165: 297-305.
94. Maul-Pavicic A, Chiang SC, Rensing-Ehl A, et al.ORAI1-mediated calcium influx is required for human cytotoxic lymphocyte degranulation and target cell lysis. Proc Natl Acad Sci USA. 2011; 108: 3324-9.
95. Darbellay B, Arnaudeau S, Konig S, et al.STIM1- and Orai1-dependent store-operated calcium entry regulates human myoblast differentiation. J Biol Chem. 2009; 284: 5370-80.
96. Darbellay B, Arnaudeau S, Ceroni D, et al.Human muscle economy myoblast differentiation and excitation-contraction coupling use the same molecular partners, STIM1 and STIM2. J Biol Chem. 2010; 285: 22437-47.
97. 2+)](i) changes in normal and hyperhidrotic human sweat gland cells. Eur J Pharmacol. 2000; 403: 45-8.
98. 2+ entry through apical and basolateral membranes of cultured equine sweat gland epithelium. J Physiol. 1996; 497: 19-29.
99. Beyersdorf N, Braun A, Vogtle T, et al.STIM1-independent T cell development and effector function in vivo. J Immunol. 2009; 182: 3390-7.
100. Oh-Hora M, Yamashita M, Hogan PG, et al.Dual functions for the endoplasmic reticulum calcium sensors STIM1 and STIM2 in T cell activation and tolerance. Nat Immunol. 2008; 9: 432-43.
101. Gwack Y, Srikanth S, Oh-Hora M, et al.Hair loss and defective T- and B-cell function in mice lacking ORAI1. Mol Cell Biol. 2008; 28: 5209-22.
102. Xu P, Lu J, Li Z, et al.Aggregation of STIM1 underneath the plasma membrane induces clustering of Orai1. Biochem Biophys Res Commun. 2006; 350: 969-76.
103. Soboloff J, Spassova MA, Tang XD, et al.Orai1 and STIM reconstitute store-operated calcium channel function. J Biol Chem. 2006; 281: 20661-5.
104. Jardin I, Lopez JJ, Zbidi H, et al.Attenuated store-operated divalent cation entry and association between STIM1, Orai1, hTRPC1 and hTRPC6 in platelets from type 2 diabetic patients. Blood Cells Mol Dis. 2011; 46: 252-60.
105. Vig M, DeHaven WI, Bird GS, et al.Defective mast cell effector functions in mice lacking the CRACM1 pore subunit of store-operated calcium release-activated calcium channels. Nat Immunol. 2008; 9: 89-96.
106. Bergmeier W, Oh-Hora M, McCarl CA, et al.R93W mutation in Orai1 causes impaired calcium influx in platelets. Blood. 2009; 113: 675-8.
107. Braun A, Varga-Szabo D, Kleinschnitz C, et al.Orai1 (CRACM1) is the platelet SOC channel and essential for pathological thrombus formation. Blood. 2009; 113: 2056-63.
108. Varga-Szabo D, Braun A, Kleinschnitz C, et al.The calcium sensor STIM1 is an essential mediator of arterial thrombosis and ischemic brain infarction. J Exp Med. 2008; 205: 1583-91.
109. 2+ mobilization and activation of NF-kappaB and NFAT. Nat Immunol. 2001; 2: 403-9.
110. von Boehmer H, Fehling HJ. Structure and function of the pre-T cell receptor. Annu Rev Immunol. 1997; 15: 433-52.
111. Wu Y, Borde M, Heissmeyer V, et al.FOXP3 controls regulatory T cell function through cooperation with NFAT. Cell. 2006; 126: 375-87.
112. Braun A, Gessner JE, Varga-Szabo D, et al.STIM1 is essential for Fcgamma receptor activation and autoimmune inflammation. Blood. 2009; 113: 1097-104.
113. Schuhmann MK, Stegner D, Berna-Erro A, et al.Stromal interaction molecules 1 and 2 are key regulators of autoreactive T cell activation in murine autoimmune central nervous system inflammation. J Immunol. 2010; 184: 1536-42.
114. Franzini-Armstrong C The sarcoplasmic reticulum and the control of muscle contraction. FASEB J. 1999; 13: S266-70.
115. Pisaniello A, Serra C, Rossi D, et al.The block of ryanodine receptors selectiveJ Cell Sci. 2003; 116: 1589-97.
116. Arnaudeau S, Holzer N, Konig S, et al.Calcium sources used by post-natal human myoblasts during initial differentiation. J Cell Physiol. 2006; 208: 435-45.
117. Gilio K, van Kruchten R, Braun A, et al.Roles of platelet STIM1 and Orai1 in glycoprotein VI- and thrombin-dependent procoagulant activity and thrombus formation. J Biol Chem. 2010; 285: 23629-38.
118. Keil JM, Shen Z, Briggs SP, et al. Regulation of STIM1 and SOCE by the ubiquitin-proteasome system (UPS). PLoS One. 2010; 5: e13465.
119. Gasperini R, Choi-Lundberg D, Thompson MJ, et al.Homer regulates calcium signalling in growth cone turning. Neural Dev. 2009; 4: 29.
120. Danoff SK, Ross CA. The inositol trisphosphate receptor gene family: implications for normal and abnormal brain function. Prog Neuropsychopharmacol Biol Psychiatry. 1994; 18: 1-16.
121. Putney JW Jr Capacitative calcium entry in the nervous system. Cell Calcium. 2003; 34: 339-44.
122. Morris RG, Anderson E, Lynch GS, et al. Selective impairment of learning and blockade of long-term potentiation by an N-methyl-D-aspartate receptor antagonist, AP5. Nature. 1986; 319: 774-6.
123. 2+ entry, and spontaneous transmitter release. Neuron. 2001; 29: 197-208.
124. 2+ deregulation in isolated CA1 neurons during oxygen and glucose deprivation. Neurochem Res. 2005; 30: 651-9.
125. Henrich M, Buckler KJ. Effects of anoxia and aglycemia on cytosolic calcium regulation in rat sensory neurons. J Neurophysiol. 2008; 100: 456-73.
126. 2+ release from intracellular stores in cultured cerebral cortical neurons. J Neurochem. 1991; 56: 1075-8.
127. Mattson MP, Zhu H, Yu J, et al. Presenilin-1 mutation increases neuronal vulnerability to focal ischemia in vivo and to hypoxia and glucose deprivation in cell culture: involvement of perturbed calcium homeostasis. J Neurosci. 2000; 20: 1358-64.
128. Arundine M, Tymianski M. Molecular mechanisms of glutamate-dependent neurodegeneration in ischemia and traumatic brain injury. Cell Mol Life Sci. 2004; 61: 657-68.
129. McAndrew D, Grice DM, Peters AA, et al.ORAI1-mediated calcium influx in lactation and in breast cancer. Mol Cancer Ther. 2011; 10: 448-60.
130. 2+ signaling in dendritic cells occurs independently of STIM1. J Leukoc Biol. 2011; 89: 57-62.
131. Kim D, Jun KS, Lee SB, et al.Phospholipase C isozymes selectively couple to specific neurotransmitter receptors. Nature. 1997; 389: 290-3.
132. Matsumoto M, Nagata E. Type 1 inositol 1, 4, 5-trisphosphate receptor knock-out mice: their phenotypes and their meaning in neuroscience and clinical practice. J Mol Med. 1999; 77: 406-11.
133. Wojda U, Salinska E, Kuznicki J. Calcium ions in neuronal degeneration. IUBMB Life. 2008; 60: 575-90.
134. Mattson MP Calcium and neurodegeneration. Aging Cell. 2007; 6: 337-50.
135. Sabbioni S, Veronese A, Trubia M, et al.Exon structure and promoter identification of STIM1 (alias GOK), a human gene causing growth arrest of the human tumour cell lines G401 and RD. Cytogenet Cell Genet. 1999; 86: 214-8.
136. Sabbioni S, Barbanti-Brodano G, Croce CM, et al. GOK: a gene at 11p15 involved in rhabdomyosarcoma and rhabdoid tumour development. Cancer Res. 1997; 57: 4493-7.
137. Ritchie MF, Yue C, Zhou Y, et al.Wilms tumour suppressor 1 (WT1) and early growth response 1 (EGR1) are regulators of STIM1 expression. J Biol Chem. 2010; 285: 10591-6.
138. Motiani RK, Abdullaev IF, Trebak M. 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. 2010; 285: 19173-83.
139. Faouzi M, Hague F, Potier M, et al.Down-regulation of Orai3 arrests cell-cycle progression and induces apoptosis in breast cancer cells but not in normal breast epithelial cells. J Cell Physiol. 2011; 226: 542-51.
140. Flourakis M, Lehen'kyi V, Beck B, et al.Orai1 contributes to the establishment of an apoptosis-resistant phenotype in prostate cancer cells. Cell Death Dis. 2010; 1: e75.
141. 2+ entry in human platelets. Cell Signal. 2008; 20: 737-47.
142. 2+ mobilization by mediating the interaction between type I inositol 1, 4, 5-trisphosphate receptor, RACK1, and Orai1. J Biol Chem. 2010; 285: 8045-53.
143. Huang YH, Hoebe K, Sauer K. New therapeutic targets in immune disorders: ItpkB, Orai1 and UNC93B. Expert Opin Ther Targets. 2008; 12: 391-413.
144. Ong HL, Cheng KT, Liu X, et al.Dynamic assembly of TRPC1-STIM1-Orai1 ternary complex is involved in store-operated calcium influx. Evidence for similarities in store-operated and calcium release-activated calcium channel components. J Biol Chem. 2007; 282: 9105-16.
145. Salido GM, Jardin I, Rosado JA. The TRPC ion channels: association with Orai1 and STIM1 proteins and participation in capacitative and non-capacitative calcium entry. Adv Exp Med Biol. 2011; 704: 413-33.
146. Hicks GA TRP channels as therapeutic targets: hot property, or time to cool down? Neurogastroenterol Motil. 2006; 18: 590-4.
147. Abramowitz J, Birnbaumer L. Physiology and pathophysiology of canonical transient receptor potential channels. FASEB J. 2009; 23: 297-328.
148. Fahrner M, Muik M, Derler I, et al.Mechanistic view on domains mediating STIM1-Orai coupling. Immunol Rev. 2009; 231: 99-112.
149. Stathopulos PB, Zheng L, Ikura M. Stromal interaction molecule (STIM) 1 and STIM2 calcium sensing regions exhibit distinct unfolding and oligomerization kinetics. J Biol Chem. 2009; 284: 728-32.
150. Stathopulos PB, Zheng L, Li GY, et al.Structural and mechanistic insights into STIM1-mediated initiation of store-operated calcium entry. Cell. 2008; 135: 110-22.
151. 2+ entry through ORAI1 is critical for T cell-mediated autoimmunity and allograft rejection. J Immunol. 2010; 185: 5845-58.
152. Baba Y, Nishida K, Fujii Y, et al.Essential function for the calcium sensor STIM1 in mast cell activation and anaphylactic responses. Nat Immunol. 2008; 9: 81-8.