Emerging roles of store-operated Ca2+ entry through STIM and ORAI proteins in immunity, hemostasis and cancer

Channels

Volumn 7, Issue 5, 2013, Pages 379-391

  Bergmeier, Wolfgang ^a   Weidinger, Carl ^b   Zee, Isabelle ^b   Feske, Stefan ^b  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Allergy; Autoimmunity; Ca2+; Calcium; Cancer; CRAC; Hemostasis; Immunodeficiency; Lymphocytes; ORAI1; Platelets; STIM1; Tumor

Indexed keywords

CALCIUM ION; CALCIUM RELEASE ACTIVATED CALCIUM CHANNEL; CALCIUM RELEASE ACTIVATED CALCIUM CHANNEL 1; STROMAL INTERACTION MOLECULE 1; STROMAL INTERACTION MOLECULE 2;

ADAPTIVE IMMUNITY; ALLERGY; APOPTOSIS; ARTICLE; CALCIUM TRANSPORT; CANCER CELL; CELL PROLIFERATION; HEMOSTASIS; HUMAN; IMMUNE SYSTEM; IMMUNITY; IMMUNOCOMPETENT CELL; IMMUNOREGULATION; INFECTION; INNATE IMMUNITY; METASTASIS; NEOPLASM; NEOVASCULARIZATION (PATHOLOGY); NONHUMAN; PROTEIN FUNCTION; REGULATORY MECHANISM; STORE OPERATED CALCIUM ENTRY; THROMBOCYTE ACTIVATION; THROMBOCYTE FUNCTION;

ALLERGY; AUTOIMMUNITY; CA2+; CALCIUM; CANCER; CRAC; HEMOSTASIS; IMMUNODEFICIENCY; LYMPHOCYTES; ORAI1; PLATELETS; STIM1; TUMOR,;

ADAPTIVE IMMUNITY; BLOOD PLATELETS; CALCIUM CHANNELS; CALCIUM SIGNALING; HEMOSTASIS; HUMANS; IMMUNITY, INNATE; INFECTION; MEMBRANE PROTEINS; NEOPLASM PROTEINS; NEOPLASMS;

EID: 84883387669     PISSN: 19336950     EISSN: 19336969     Source Type: Journal    
DOI: 10.4161/chan.24302     Document Type: Article

References (142)

1. Prakriya M, Feske S, Gwack Y, Srikanth S, Rao A, Hogan PG. Orai1 is an essential pore subunit of the CRAC channel. Nature 2006; 443:230-3; PMID:16921383; http://dx.doi.org/10.1038/nature05122. (Pubitemid 44387613)
2. Vig M, Beck A, Billingsley JM, Lis A, Parvez S, Peinelt C, et al. CRACM1 multimers form the ion-selective pore of the CRAC channel. Curr Biol 2006; 16:2073-9; PMID:16978865; http://dx.doi.org/10.1016/j. cub.2006.08.085. (Pubitemid 44573821)
3. Yeromin AV, Zhang SL, Jiang W, Yu Y, Safrina O, Cahalan MD. Molecular identification of the CRAC channel by altered ion selectivity in a mutant of Orai. Nature 2006; 443:226-9; PMID:16921385; http://dx.doi.org/10.1038/ nature05108. (Pubitemid 44387612)
4. Feske S, Gwack Y, Prakriya M, Srikanth S, Puppel SH, Tanasa B, et al. A mutation in Orai1 causes immune deficiency by abrogating CRAC channel function. Nature 2006; 441:179-85; PMID:16582901; http://dx.doi.org/10.1038/nature04702.
5. Vig M, Peinelt C, Beck A, Koomoa DL, Rabah D, Koblan-Huberson M, et al. CRACM1 is a plasma membrane protein essential for store-operated Ca2+ entry. Science 2006; 312:1220-3; PMID:16645049; http://dx.doi.org/10.1126/science. 1127883. (Pubitemid 43801149)
6. Zhang SL, Yeromin AV, Zhang XH, Yu Y, Safrina O, Penna A, et al. Genome-wide RNAi screen of Ca(2+) influx identifies genes that regulate Ca(2+) release-activated Ca(2+) channel activity. Proc Natl Acad Sci U S A 2006; 103:9357-62; PMID:16751269; http://dx.doi.org/10.1073/pnas.0603161103. (Pubitemid 43902581)
7. Liou J, Kim ML, Heo WD, Jones JT, Myers JW, Ferrell JE Jr., et al. STIM is a Ca2+ sensor essential for Ca2+-store-depletion-triggered Ca2+ influx. Curr Biol 2005; 15:1235-41; PMID:16005298; http://dx.doi.org/10.1016/j.cub.2005.05. 055. (Pubitemid 40950523)
8. 2+ channel function. J Cell Biol 2005; 169:435-45; PMID:15866891; http://dx.doi.org/10.1083/jcb.200502019. (Pubitemid 40686694)
9. Luik RM, Wu MM, Buchanan J, Lewis RS. The elementary unit of store-operated Ca2+ entry: local activation of CRAC channels by STIM1 at ER-plasma membrane junctions. J Cell Biol 2006; 174:815-25; PMID:16966423; http://dx.doi.org/10.1083/jcb.200604015. (Pubitemid 44373731)
10. Muik M, Frischauf I, Derler I, Fahrner M, Bergsmann J, Eder P, 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; PMID:18187424; http://dx.doi.org/10.1074/jbc. M708898200.
11. Park CY, Hoover PJ, Mullins FM, Bachhawat P, Covington ED, Raunser S, et al. STIM1 clusters and activates CRAC channels via direct binding of a cytosolic domain to Orai1. Cell 2009; 136:876-90; PMID:19249086; http://dx.doi.org/10. 1016/j. cell.2009.02.014.
12. Zhou Y, Meraner P, Kwon HT, Machnes D, Oh-hora M, Zimmer J, et al. STIM1 gates the store-operated calcium channel ORAI1 in vitro. Nat Struct Mol Biol 2010; 17:112-6; PMID:20037597; http://dx.doi.org/10.1038/nsmb.1724.
13. 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; PMID:19019825; http://dx.doi.org/10. 1074/jbc.C800178200.
14. Brandman O, Liou J, Park WS, Meyer T. STIM2 is a feedback regulator that stabilizes basal cytosolic and endoplasmic reticulum Ca2+ levels. Cell 2007; 131:1327-39; PMID:18160041; http://dx.doi.org/10.1016/j.cell.2007.11.039. (Pubitemid 350297421)
15. Peinelt C, Vig M, Koomoa DL, Beck A, Nadler MJ, Koblan-Huberson M, et al. Amplification of CRAC current by STIM1 and CRACM1 (Orai1). Nat Cell Biol 2006; 8:771-3; PMID:16733527; http://dx.doi.org/10.1038/ncb1435.
16. Soboloff J, Spassova MA, Tang XD, Hewavitharana T, Xu W, Gill DL. Orai1 and STIM reconstitute store-operated calcium channel function. J Biol Chem 2006; 281:20661-5; PMID:16766533; http://dx.doi.org/10.1074/jbc.C600126200. (Pubitemid 44115407)
17. Shaw PJ, Qu B, Hoth M, Feske S. Molecular regulation of CRAC channels and their role in lymphocyte function. Cell Mol Life Sci 2012; PMID:23052215; http://dx.doi.org/10.1007/s00018-012-1175-2.
18. Derler I, Madl J, Schütz G, Romanin C. Structure, regulation and biophysics of I(CRAC), STIM/Orai1. Adv Exp Med Biol 2012; 740:383-410; PMID:22453951; http://dx.doi.org/10.1007/978-94-007-2888-2-16.
19. Hogan PG, Lewis RS, Rao A. Molecular basis of calcium signaling in lymphocytes: STIM and ORAI. Annu Rev Immunol 2010; 28:491-533; PMID:20307213; http://dx.doi.org/10.1146/annurev. immunol.021908.132550.
20. Soboloff J, Rothberg BS, Madesh M, Gill DL. STIM proteins: dynamic calcium signal transducers. Nat Rev Mol Cell Biol 2012; 13:549-65; PMID:22914293; http://dx.doi.org/10.1038/nrm3414.
21. Cahalan MD. Cell biology. How to STI Mulate calcium channels. Science 2010; 330:43-4; PMID:20929798; http://dx.doi.org/10.1126/science.1196348.
22. Berna-Erro A, Braun A, Kraft R, Kleinschnitz C, Schuhmann MK, Stegner D, et al. STIM2 regulates capacitive Ca2+ entry in neurons and plays a key role in hypoxic neuronal cell death. Sci Signal 2009; 2:ra67; PMID:19843959; http://dx.doi.org/10.1126/scisignal.2000522.
23. Hulot JS, Fauconnier J, Ramanujam D, Chaanine A, Aubart F, Sassi Y, et al. Critical role for stromal interaction molecule 1 in cardiac hypertrophy. Circulation 2011; 124:796-805; PMID:21810664; http://dx.doi.org/10.1161/ CIRCULATIONAHA.111.031229.
24. Zhang W, Halligan KE, Zhang X, Bisaillon JM, Gonzalez-Cobos JC, Motiani RK, et al. Orai1-mediated I (CRAC) is essential for neointima formation after vascular injury. Circ Res 2011; 109:534-42; PMID:21737791; http://dx.doi.org/10. 1161/CIRCRESAHA.111.246777.
25. Guo RW, Wang H, Gao P, Li MQ, Zeng CY, Yu Y, et al. An essential role for stromal interaction molecule 1 in neointima formation following arterial injury. Cardiovasc Res 2009; 81:660-8; PMID:19052075; http://dx.doi.org/10.1093/ cvr/cvn338.
26. Guo RW, Yang LX, Li MQ, Pan XH, Liu B, Deng YL. Stim1-and Orai1-mediated store-operated calcium entry is critical for angiotensin II-induced vascular smooth muscle cell proliferation. Cardiovasc Res 2012; 93:360-70; PMID:22108917; http://dx.doi.org/10.1093/cvr/cvr307.
27. Baba Y, Nishida K, Fujii Y, Hirano T, Hikida M, Kurosaki T. Essential function for the calcium sensor STIM1 in mast cell activation and anaphylactic responses. Nat Immunol 2008; 9:81-8; PMID:18059272; http://dx.doi.org/10.1038/ ni1546. (Pubitemid 350286207)
28. Di Capite J, Nelson C, Bates G, Parekh AB. Targeting Ca2+ release-activated Ca2+ channel channels and leukotriene receptors provides a novel combination strategy for treating nasal polyposis. J Allergy Clin Immunol 2009; 124:1014-21, e1-3; PMID:19895990; http://dx.doi.org/10.1016/j.jaci.2009. 08.030.
29. Ma J, McCarl CA, Khalil S, Lüthy K, Feske S. T-cell-specific deletion of STIM1 and STIM2 protects mice from EAE by impairing the effector functions of Th1 and Th17 cells. Eur J Immunol 2010; 40:3028-42; PMID:21061435; http://dx.doi.org/10.1002/eji.201040614.
30. Matsumoto M, Fujii Y, Baba A, Hikida M, Kurosaki T, Baba Y. The calcium sensors STIM1 and STIM2 control B cell regulatory function through interleukin-10 production. Immunity 2011; 34:703-14; PMID:21530328; http://dx.doi.org/10.1016/j.immuni.2011.03.016.
31. McCarl CA, Khalil S, Ma J, Oh-hora M, Yamashita M, Roether J, et al. Store-operated Ca2+ entry through ORAI1 is critical for T cell-mediated autoimmunity and allograft rejection. J Immunol 2010; 185:5845-58; PMID:20956344; http://dx.doi.org/10.4049/jimmunol.1001796.
32. Oh-Hora M, Yamashita M, Hogan PG, Sharma S, Lamperti E, Chung W, 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; PMID:18327260; http://dx.doi.org/10.1038/ni1574. (Pubitemid 351405113)
33. Schuhmann MK, Stegner D, Berna-Erro A, Bittner S, Braun A, Kleinschnitz C, 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; PMID:20028655; http://dx.doi.org/10. 4049/jimmunol.0902161.
34. Vig M, DeHaven WI, Bird GS, Billingsley JM, Wang H, Rao PE, 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; PMID:18059270; http://dx.doi.org/10.1038/ni1550. (Pubitemid 350286208)
35. Ahmad F, Boulaftali Y, Greene TK, Ouellette TD, Poncz M, Feske S, et al. Relative contributions of stromal interaction molecule 1 and CalDAG-GEFI to calcium-dependent platelet activation and thrombosis. J Thromb Haemost 2011; 9:2077-86; PMID:21848641; http://dx.doi.org/10.1111/j.1538-7836.2011.04474.x.
36. Bergmeier W, Oh-Hora M, McCarl CA, Roden RC, Bray PF, Feske S. R93W mutation in Orai1 causes impaired calcium influx in platelets. Blood 2009; 113:675-8; PMID:18952890; http://dx.doi.org/10.1182/blood-2008-08-174516.
37. Braun A, Varga-Szabo D, Kleinschnitz C, Pleines I, Bender M, Austinat M, et al. Orai1 (CRACM1) is the platelet SOC channel and essential for pathological thrombus formation. Blood 2009; 113:2056-63; PMID:18832659; http://dx.doi.org/10.1182/blood-2008-07-171611.
38. Grosse J, Braun A, Varga-Szabo D, Beyersdorf N, Schneider B, Zeitlmann L, et al. An EF hand mutation in Stim1 causes premature platelet activation and bleeding in mice. J Clin Invest 2007; 117:3540-50; PMID:17965774; http://dx.doi.org/10.1172/JCI32312. (Pubitemid 350097009)
39. Varga-Szabo D, Braun A, Kleinschnitz C, Bender M, Pleines I, Pham M, et al. The calcium sensor STIM1 is an essential mediator of arterial thrombosis and ischemic brain infarction. J Exp Med 2008; 205:1583-91; PMID:18559454; http://dx.doi.org/10.1084/jem.20080302. (Pubitemid 351962022)
40. Chen YF, Chiu WT, Chen YT, Lin PY, Huang HJ, Chou CY, et al. Calcium store sensor stromal-interaction molecule 1-dependent signaling plays an important role in cervical cancer growth, migration, and angiogenesis. Proc Natl Acad Sci U S A 2011; 108:15225-30; PMID:21876174; http://dx.doi.org/10.1073/ pnas.1103315108.
41. Yang S, Zhang JJ, Huang XY. Orai1 and STIM1 are critical for breast tumor cell migration and metastasis. Cancer Cell 2009; 15:124-34; PMID:19185847; http://dx.doi.org/10.1016/j.ccr.2008.12.019.
42. Feske S. ORAI1 and STIM1 deficiency in human and mice: roles of store-operated Ca2+ entry in the immune system and beyond. Immunol Rev 2009; 231:189-209; PMID:19754898; http://dx.doi.org/10.1111/j.1600-065X.2009.00818.x.
43. Feske S. Immunodeficiency due to defects in store-operated calcium entry. Ann N Y Acad Sci 2011; 1238:74-90; PMID:22129055; http://dx.doi.org/10.1111/j. 1749-6632.2011.06240.x.
44. Byun M, Abhyankar A, Lelarge V, Plancoulaine S, Palanduz A, Telhan L, 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; PMID:20876309; http://dx.doi.org/10.1084/jem.20101597.
45. Sahin G, Palanduz A, Aydogan G, Cassar O, Ertem AU, Telhan L, et al. Classic Kaposi sarcoma in 3 unrelated Turkish children born to consanguineous kindreds. Pediatrics 2010; 125:e704-8; PMID:20156905; http://dx.doi.org/10.1542/ peds.2009-2224.
46. Fuchs S, Rensing-Ehl A, Speckmann C, Bengsch B, Schmitt-Graeff A, Bondzio I, et al. Antiviral and regulatory T cell immunity in a patient with stromal interaction molecule 1 deficiency. J Immunol 2012; 188:1523-33; PMID:22190180; http://dx.doi.org/10.4049/jimmunol.1102507.
47. 2+ entry cause immunodeficiency, myopathy, and ectodermal dysplasia. J Allergy Clin Immunol 2009; 124:1311-8, e7; PMID:20004786; http://dx.doi.org/10.1016/j.jaci.2009.10. 007.
48. Partiseti M, Le Deist F, Hivroz C, Fischer A, Korn H, Choquet D. 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; PMID:7798233.
49. Le Deist F, Hivroz C, Partiseti M, Thomas C, Buc HA, Oleastro M, et al. A primary T-cell immunodeficiency associated with defective transmembrane calcium influx. Blood 1995; 85:1053-62; PMID:7531512.
50. Feske S, Prakriya M, Rao A, Lewis RS. A severe defect in CRAC Ca2+ channel activation and altered K+ channel gating in T cells from immunodeficient patients. J Exp Med 2005; 202:651-62; PMID:16147976; http://dx.doi.org/10.1084/ jem.20050687. (Pubitemid 41248416)
51. Maul-Pavicic A, Chiang SC, Rensing-Ehl A, Jessen B, Fauriat C, Wood SM, et al. ORAI1-mediated calcium influx is required for human cytotoxic lymphocyte degranulation and target cell lysis. Proc Natl Acad Sci U S A 2011; 108:3324-9; PMID:21300876; http://dx.doi.org/10.1073/pnas.1013285108.
52. Hou X, Pedi L, Diver MM, Long SB. Crystal structure of the calcium release-activated calcium channel Orai. Science 2012; 338:1308-13; PMID:23180775; http://dx.doi.org/10.1126/science.1228757.
53. Picard C, McCarl CA, Papolos A, Khalil S, Lüthy K, Hivroz C, et al. STIM1 mutation associated with a syndrome of immunodeficiency and autoimmunity. N Engl J Med 2009; 360:1971-80; PMID:19420366; http://dx.doi.org/10.1056/ NEJMoa0900082.
54. Feske S, Müller JM, Graf D, Kroczek RA, Dräger R, Niemeyer C, 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; PMID:8814256; http://dx.doi.org/10.1002/eji.1830260924. (Pubitemid 26297511)
55. Feske S, Giltnane J, Dolmetsch R, Staudt LM, Rao A. Gene regulation mediated by calcium signals in T lymphocytes. Nat Immunol 2001; 2:316-24; PMID:11276202; http://dx.doi.org/10.1038/86318. (Pubitemid 33706342)
56. Kim KD, Srikanth S, Yee MK, Mock DC, Lawson GW, Gwack Y. ORAI1 deficiency impairs activated T cell death and enhances T cell survival. J Immunol 2011; 187:3620-30; PMID:21873530; http://dx.doi.org/10.4049/jimmunol.1100847.
57. Beyersdorf N, Braun A, Vögtle T, Varga-Szabo D, Galdos RR, Kissler S, et al. STIM1-independent T cell development and effector function in vivo. J Immunol 2009; 182:3390-7; PMID:19265116; http://dx.doi.org/10.4049/jimmunol. 0802888.
58. Gwack Y, Srikanth S, Oh-Hora M, Hogan PG, Lamperti ED, Yamashita M, et al. Hair loss and defective T-and B-cell function in mice lacking ORAI1. Mol Cell Biol 2008; 28:5209-22; PMID:18591248; http://dx.doi.org/10.1128/MCB.00360- 08.
59. Engelke M, Engels N, Dittmann K, Stork B, Wienands J. Ca(2+) signaling in antigen receptor-activated B lymphocytes. Immunol Rev 2007; 218:235-46; PMID:17624956; http://dx.doi.org/10.1111/j.1600-065X.2007.00539.x. (Pubitemid 47052309)
60. Lazarevic V, Zullo AJ, Schweitzer MN, Staton TL, Gallo EM, Crabtree GR, et al. The gene encoding early growth response 2, a target of the transcription factor NFAT, is required for the development and maturation of natural killer T cells. Nat Immunol 2009; 10:306-13; PMID:19169262; http://dx.doi.org/10.1038/ni. 1696.
61. Rengarajan J, Mittelstadt PR, Mages HW, Gerth AJ, Kroczek RA, Ashwell JD, et al. Sequential involvement of NFAT and Egr transcription factors in FasL regulation. Immunity 2000; 12:293-300; PMID:10755616; http://dx.doi.org/10.1016/ S1074-7613(00)80182-X.
62. Schaff UY, Dixit N, Procyk E, Yamayoshi I, Tse T, Simon SI. Orai1 regulates intracellular calcium, arrest, and shape polarization during neutrophil recruitment in shear flow. Blood 2010; 115:657-66; PMID:19965684; http://dx.doi.org/10.1182/blood-2009-05-224659.
63. Dixit N, Kim MH, Rossaint J, Yamayoshi I, Zarbock A, Simon SI. Leukocyte function antigen-1, kindlin-3, and calcium flux orchestrate neutrophil recruitment during inflammation. J Immunol 2012; 189:5954-64; PMID:23144497; http://dx.doi.org/10.4049/jimmunol.1201638.
64. Kobayashi K, Takahashi K, Nagasawa S. The role of tyrosine phosphorylation and Ca2+ accumulation in Fc gamma-receptor-mediated phagocytosis of human neutrophils. J Biochem 1995; 117:1156-61; PMID:7490254.
65. Steinckwich N, Schenten V, Melchior C, Bréchard S, Tschirhart EJ. An essential role of STIM1, Orai1, and S100A8-A9 proteins for Ca2+ signaling and FcγR-mediated phagosomal oxidative activity. J Immunol 2011; 186:2182-91; PMID:21239714; http://dx.doi.org/10.4049/jimmunol.1001338.
66. Steinckwich N, Frippiat JP, Stasia MJ, Erard M, Boxio R, Tankosic C, et al. Potent inhibition of store-operated Ca2+ influx and superoxide production in HL60 cells and polymorphonuclear neutrophils by the pyrazole derivative BTP2. J Leukoc Biol 2007; 81:1054-64; PMID:17261548; http://dx.doi.org/10.1189/jlb. 0406248. (Pubitemid 46495654)
67. Greenberg S, el Khoury J, di Virgilio F, Kaplan EM, Silverstein SC. Ca(2+)-independent F-actin assembly and disassembly during Fc receptor-mediated phagocytosis in mouse macrophages. J Cell Biol 1991; 113:757-67; PMID:2026648; http://dx.doi.org/10.1083/jcb.113.4.757. (Pubitemid 21909712)
68. Hishikawa T, Cheung JY, Yelamarty RV, Knutson DW. Calcium transients during Fc receptor-mediated and nonspecific phagocytosis by murine peritoneal macrophages. J Cell Biol 1991; 115:59-66; PMID:1918139; http://dx.doi.org/10. 1083/jcb.115.1.59. (Pubitemid 21909893)
69. McNeil PL, Swanson JA, Wright SD, Silverstein SC, Taylor DL. Fc-receptor-mediated phagocytosis occurs in macrophages without an increase in average [Ca++] i. J Cell Biol 1986; 102:1586-92; PMID:3700467; http://dx.doi.org/10.1083/jcb.102.5.1586. (Pubitemid 16078743)
70. Braun A, Gessner JE, Varga-Szabo D, Syed SN, Konrad S, Stegner D, et al. STIM1 is essential for Fcgamma receptor activation and autoimmune inflammation. Blood 2009; 113:1097-104; PMID:18941110; http://dx.doi.org/10.1182/blood-2008- 05-158477.
71. Bréchard S, Plançon S, Melchior C, Tschirhart EJ. STIM1 but not STIM2 is an essential regulator of Ca2+ influx-mediated NADPH oxidase activity in neutrophil-like HL-60 cells. Biochem Pharmacol 2009; 78:504-13; PMID:19433064; http://dx.doi.org/10.1016/j.bcp.2009.05.006.
72. Schenten V, Melchior C, Steinckwich N, Tschirhart EJ, Bréchard S. Sphingosine kinases regulate NOX2 activity via p38 MAPK-dependent translocation of S100A8/A9. J Leukoc Biol 2011; 89:587-96; PMID:21233411; http://dx.doi.org/ 10.1189/jlb.0510304.
73. Chen BC, Chou CF, Lin WW. Pyrimidinoceptor-mediated potentiation of inducible nitric-oxide synthase induction in J774 macrophages. Role of intracellular calcium. J Biol Chem 1998; 273:29754-63; PMID:9792689; http://dx.doi.org/10.1074/jbc.273.45.29754.
74. Tapper H. The secretion of preformed granules by macrophages and neutrophils. J Leukoc Biol 1996; 59:613-22; PMID:8656045. (Pubitemid 26198072)
75. Watanabe N, Suzuki J, Kobayashi Y. Role of calcium in tumor necrosis factor-alpha production by activated macrophages. J Biochem 1996; 120:1190-5; PMID:9010769; http://dx.doi.org/10.1093/oxfordjournals.jbchem.a021540.
76. Dawicki W, Marshall JS. New and emerging roles for mast cells in host defence. Curr Opin Immunol 2007; 19:31-8; PMID:17126541; http://dx.doi.org/10. 1016/j.coi.2006.11.006. (Pubitemid 46073696)
77. Hide M, Beaven MA. Calcium influx in a rat mast cell (RBL-2H3) line. Use of multivalent metal ions to define its characteristics and role in exocytosis. J Biol Chem 1991; 266:15221-9; PMID:1869551. (Pubitemid 21907638)
78. Penner R, Neher E. The role of calcium in stimulus-secretion coupling in excitable and non-excitable cells. J Exp Biol 1988; 139:329-45; PMID:2850338. (Pubitemid 18268028)
79. Takei M, Urashima H, Endo K, Muramatu M. Role of calcium in histamine release from rat mast cells activated by various secretagogues; intracellular calcium mobilization correlates with histamine release. Biol Chem Hoppe Seyler 1989; 370:1-10; PMID:2469433; http://dx.doi.org/10.1515/bchm3.1989.370.1.1. (Pubitemid 19043064)
80. Nishida K, Yamasaki S, Ito Y, Kabu K, Hattori K, Tezuka T, et al. FcepsilonRI-mediated mast cell degranulation requires calcium-independent microtubule-dependent translocation of granules to the plasma membrane. J Cell Biol 2005; 170:115-26; PMID:15998803; http://dx.doi.org/10.1083/jcb.200501111. (Pubitemid 40994101)
81. Di Capite JL, Bates GJ, Parekh AB. Mast cell CRAC channel as a novel therapeutic target in allergy. Curr Opin Allergy Clin Immunol 2011; 11:33-8; PMID:21150433; http://dx.doi.org/10.1097/ACI.0b013e32834232b0.
82. Lin L, Zheng C, Zhang L, Da C, Zhao K. Up-regulation of Orai1 in murine allergic rhinitis. Histochem Cell Biol 2010; 134:93-102; PMID:20552218; http://dx.doi.org/10.1007/s00418-010-0717-7.
83. Wang Y, Lin L, Zheng C. Downregulation of Orai1 expression in the airway alleviates murine allergic rhinitis. Exp Mol Med 2012; 44:177-90; PMID:22170034; http://dx.doi.org/10.3858/emm.2012.44.3.013.
84. Feinstein MB, Becker EL, Fraser C. Thrombin, collagen and A23187 stimulated endogenous platelet arachidonate metabolism: differential inhibition by PGE1, local anesthetics and a serine-protease inhibitor. Prostaglandins 1977; 14:1075-93; PMID:341226; http://dx.doi.org/10.1016/0090-6980(77)90286-6. (Pubitemid 8260077)
85. nd, Scarborough DE, Brinkhous KM. Morphological study of early phases of platelet adhesion to foreign surfaces: effect of calcium. Ann N Y Acad Sci 1983; 416:351-62; PMID:6587812; http://dx.doi.org/10. 1111/j.1749-6632.1983.tb35198.x. (Pubitemid 14140662)
86. Wörner P, Brossmer R. Platelet aggregation and the release induced by inophores for divalent cations. Thromb Res 1975; 6:295-305; PMID:1094583; http://dx.doi.org/10.1016/0049-3848(75)90079-1.
87. Bevers EM, Comfurius P, Zwaal RF. Changes in membrane phospholipid distribution during platelet activation. Biochim Biophys Acta 1983; 736:57-66; PMID:6418205; http://dx.doi.org/10.1016/0005-2736(83)90169-4. (Pubitemid 14201823)
88. 2+ stores. Biochem J 1991; 280:783-9; PMID:1764041.
89. Sage SO, Pintado E, Mahaut-Smith MP, Merritt JE. Rapid kinetics of agonist-evoked changes in cytosolic free Ca2+ concentration in fura-2-loaded human neutrophils. Biochem J 1990; 265:915-8; PMID:2306226. (Pubitemid 20053903)
90. Sage SO, Reast R, Rink TJ. ADP evokes biphasic Ca2+ influx in fura-2-loaded human platelets. Evidence for Ca2+ entry regulated by the intracellular Ca2+ store. Biochem J 1990; 265:675-80; PMID:2306207. (Pubitemid 20053869)
91. Stefanini L, Bergmeier W. CalDAG-GEFI and platelet activation. Platelets 2010; 21:239-43; PMID:20218908; http://dx.doi.org/10.3109/09537101003639931.
92. Crittenden JR, Bergmeier W, Zhang Y, Piffath CL, Liang Y, Wagner DD, et al. CalDAG-GEFI integrates signaling for platelet aggregation and thrombus formation. Nat Med 2004; 10:982-6; PMID:15334074; http://dx.doi.org/10.1038/ nm1098. (Pubitemid 39273740)
93. Stefanini L, Roden RC, Bergmeier W. CalDAG-GEFI is at the nexus of calcium-dependent platelet activation. Blood 2009; 114:2506-14; PMID:19628710; http://dx.doi.org/10.1182/blood-2009-04-218768.
94. Stefanini L, Boulaftali Y, Ouellette TD, Holinstat M, Désiré L, Leblond B, et al. Rap1-Rac1 circuits potentiate platelet activation. Arterioscler Thromb Vasc Biol 2012; 32:434-41; PMID:22075250; http://dx.doi.org/10.1161/ATVBAHA.111.239194.
95. Henderson NS, So SS, Martin C, Kulkarni R, Thanassi DG. Topology of the outer membrane usher PapC determined by site-directed fluorescence labeling. J Biol Chem 2004; 279:53747-54; PMID:15485883; http://dx.doi.org/10.1074/jbc. M409192200. (Pubitemid 40051883)
96. Kulkarni S, Jackson SP. Platelet factor XIII and calpain negatively regulate integrin alphaIIbbeta3 adhesive function and thrombus growth. J Biol Chem 2004; 279:30697-706; PMID:15131115; http://dx.doi.org/10.1074/jbc. M403559200. (Pubitemid 38938002)
97. Tolhurst G, Carter RN, Amisten S, Holdich JP, Erlinge D, Mahaut-Smith MP. Expression profiling and electrophysiological studies suggest a major role for Orai1 in the store-operated Ca2+ influx pathway of platelets and megakaryocytes. Platelets 2008; 19:308-13; PMID:18569867; http://dx.doi.org/10.1080/ 09537100801935710. (Pubitemid 351874159)
98. Gilio K, van Kruchten R, Braun A, Berna-Erro A, Feijge MA, Stegner D, 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; PMID:20519511; http://dx.doi.org/10.1074/jbc.M110.108696.
99. Darbousset R, Thomas GM, Mezouar S, Frère C, Bonier R, Mackman N, et al. Tissue factor-positive neutrophils bind to injured endothelial wall and initiate thrombus formation. Blood 2012; 120:2133-43; PMID:22837532; http://dx.doi.org/10.1182/blood-2012-06-437772.
100. Jin R, Yang G, Li G. Inflammatory mechanisms in ischemic stroke: role of inflammatory cells. J Leukoc Biol 2010; 87:779-89; PMID:20130219; http://dx.doi.org/10.1189/jlb.1109766.
101. Rosado JA, Sage SO. Coupling between inositol 1,4,5-trisphosphate receptors and human transient receptor potential channel 1 when intracellular Ca2+ stores are depleted. Biochem J 2000; 350:631-5; PMID:10970773; http://dx.doi.org/10.1042/0264-6021:3500631.
102. Jardin I, Lopez JJ, Salido GM, Rosado JA. Orai1 mediates the interaction between STIM1 and hTRPC1 and regulates the mode of activation of hTRPC1-forming Ca2+ channels. J Biol Chem 2008; 283:25296-304; PMID:18644792; http://dx.doi.org/10.1074/jbc. M802904200.
103. Varga-Szabo D, Authi KS, Braun A, Bender M, Ambily A, Hassock SR, et al. Store-operated Ca(2+) entry in platelets occurs independently of transient receptor potential (TRP) C1. Pflugers Arch 2008; 457:377-87; PMID:18546016; http://dx.doi.org/10.1007/s00424-008-0531-4.
104. Hassock SR, Zhu MX, Trost C, Flockerzi V, Authi KS. Expression and role of TRPC proteins in human platelets: evidence that TRPC6 forms the store-independent calcium entry channel. Blood 2002; 100:2801-11; PMID:12351388; http://dx.doi.org/10.1182/blood-2002-03-0723.
105. Hechler B, Lenain N, Marchese P, Vial C, Heim V, Freund M, et al. A role of the fast ATP-gated P2X1 cation channel in thrombosis of small arteries in vivo. J Exp Med 2003; 198:661-7; PMID:12913094; http://dx.doi.org/10.1084/jem. 20030144. (Pubitemid 37040400)
106. Hu H, Hoylaerts MF. The P2X1 ion channel in platelet function. Platelets 2010; 21:153-66; PMID:20201633; http://dx.doi.org/10.3109/09537101003599549.
107. Ramanathan G, Gupta S, Thielmann I, Pleines I, Varga-Szabo D, May F, et al. Defective diacylglycerol-induced Ca2+ entry but normal agonist-induced activation responses in TRPC6-deficient mouse platelets. J Thromb Haemost 2012; 10:419-29; PMID:22176814; http://dx.doi.org/10.1111/j.1538-7836.2011.04596.x.
108. Suzuki J, Umeda M, Sims PJ, Nagata S. Calcium-dependent phospholipid scrambling by TMEM16F. Nature 2010; 468:834-8; PMID:21107324; http://dx.doi.org/10.1038/nature09583.
109. Yang H, Kim A, David T, Palmer D, Jin T, Tien J, et al. TMEM16F forms a Ca2+-activated cation channel required for lipid scrambling in platelets during blood coagulation. Cell 2012; 151:111-22; PMID:23021219; http://dx.doi.org/10. 1016/j.cell.2012.07.036.
110. van Kruchten R, Braun A, Feijge MA, Kuijpers MJ, Rivera-Galdos R, Kraft P, et al. Antithrombotic potential of blockers of store-operated calcium channels in platelets. Arterioscler Thromb Vasc Biol 2012; 32:1717-23; PMID:22580895; http://dx.doi.org/10.1161/ATVBAHA.111.243907.
111. Hanahan D, Weinberg RA. The hallmarks of cancer. Cell 2000; 100:57-70; PMID:10647931; http://dx.doi.org/10.1016/S0092-8674(00)81683-9. (Pubitemid 30046295)
112. Monteith GR, McAndrew D, Faddy HM, Roberts-Thomson SJ. Calcium and cancer: targeting Ca2+ transport. Nat Rev Cancer 2007; 7:519-30; PMID:17585332; http://dx.doi.org/10.1038/nrc2171. (Pubitemid 46985398)
113. Sabbioni S, Barbanti-Brodano G, Croce CM, Negrini M. GOK: a gene at 11p15 involved in rhabdomyosarcoma and rhabdoid tumor development. Cancer Res 1997; 57:4493-7; PMID:9377559. (Pubitemid 27441051)
114. Sabbioni S, Veronese A, Trubia M, Taramelli R, Barbanti-Brodano G, Croce CM, et al. Exon structure and promoter identification of STIM1 (alias GOK), a human gene causing growth arrest of the human tumor cell lines G401 and RD. Cytogenet Cell Genet 1999; 86:214-8; PMID:10575208; http://dx.doi.org/10.1159/ 000015341.
115. Flourakis M, Lehen'kyi V, Beck B, Raphaël M, Vandenberghe M, Abeele FV, et al. Orai1 contributes to the establishment of an apoptosis-resistant phenotype in prostate cancer cells. Cell Death Dis 2010; 1:e75; PMID:21364678; http://dx.doi.org/10.1038/cddis.2010.52.
116. Fedida-Metula S, Feldman B, Koshelev V, Levin-Gromiko U, Voronov E, Fishman D. Lipid rafts couple store-operated Ca2+ entry to constitutive activation of PKB/Akt in a Ca2+/calmodulin-, Src-and PP2A-mediated pathway and promote melanoma tumor growth. Carcinogenesis 2012; 33:740-50; PMID:22287561; http://dx.doi.org/10.1093/carcin/bgs021.
117. Liu H, Hughes JD, Rollins S, Chen B, Perkins E. Calcium entry via ORAI1 regulates glioblastoma cell proliferation and apoptosis. Exp Mol Pathol 2011; 91:753-60; PMID:21945734; http://dx.doi.org/10.1016/j.yexmp.2011.09.005.
118. Ruano Y, Mollejo M, Ribalta T, Fiaño C, Camacho FI, Gómez E, et al. Identification of novel candidate target genes in amplicons of Glioblastoma multiforme tumors detected by expression and CGH microarray profiling. Mol Cancer 2006; 5:39; PMID:17002787; http://dx.doi.org/10.1186/1476- 4598-5-39.
119. McAndrew D, Grice DM, Peters AA, Davis FM, Stewart T, Rice M, et al. ORAI1-mediated calcium influx in lactation and in breast cancer. Mol Cancer Ther 2011; 10:448-60; PMID:21224390; http://dx.doi.org/10.1158/1535-7163.MCT-10- 0923.
120. Faouzi M, Hague F, Potier M, Ahidouch A, Sevestre H, Ouadid-Ahidouch H. 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; PMID:20683915; http://dx.doi.org/10.1002/jcp.22363.
121. 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; PMID:20395295; http://dx.doi.org/10.1074/ jbc. M110.102582.
122. Motiani RK, et al. Orai3 is an estrogen receptor alpha-regulated Ca2+ channel that promotes tumorigenesis. FASEB J 2012; 2012:19.
123. Feng M, Grice DM, Faddy HM, Nguyen N, Leitch S, Wang Y, et al. Store-independent activation of Orai1 by SPCA2 in mammary tumors. Cell 2010; 143:84-98; PMID:20887894; http://dx.doi.org/10.1016/j. cell.2010.08.040.
124. Hu J, Qin K, Zhang Y, Gong J, Li N, Lv D, et al. Downregulation of transcription factor Oct4 induces an epithelial-to-mesenchymal transition via enhancement of Ca2+ influx in breast cancer cells. Biochem Biophys Res Commun 2011; 411:786-91; PMID:21798248; http://dx.doi.org/10.1016/j.bbrc.2011.07.025.
125. Jauliac S, López-Rodriguez C, Shaw LM, Brown LF, Rao A, Toker A. The role of NFAT transcription factors in integrin-mediated carcinoma invasion. Nat Cell Biol 2002; 4:540-4; PMID:12080349; http://dx.doi.org/10.1038/ncb816. (Pubitemid 34752442)
126. Mancini M, Toker A. NFAT proteins: emerging roles in cancer progression. Nat Rev Cancer 2009; 9:810-20; PMID:19851316; http://dx.doi.org/10.1038/nrc2735.
127. Bos PD, Zhang XH, Nadal C, Shu W, Gomis RR, Nguyen DX, et al. Genes that mediate breast cancer metastasis to the brain. Nature 2009; 459:1005-9; PMID:19421193; http://dx.doi.org/10.1038/nature08021.
128. Huang WC, Chai CY, Chen WC, Hou MF, Wang YS, Chiu YC, et al. Histamine regulates cyclooxygenase 2 gene activation through Orai1-mediated NFκB activation in lung cancer cells. Cell Calcium 2011; 50:27-35; PMID:21605904; http://dx.doi.org/10.1016/j. ceca.2011.04.004.
129. Abdullaev IF, Bisaillon JM, Potier M, Gonzalez JC, Motiani RK, Trebak M. Stim1 and Orai1 mediate CRAC currents and store-operated calcium entry important for endothelial cell proliferation. Circ Res 2008; 103:1289-99; PMID:18845811; http://dx.doi.org/10.1161/01.RES.0000338496.95579.56.
130. Dragoni S, Laforenza U, Bonetti E, Lodola F, Bottino C, Berra-Romani R, et al. Vascular endothelial growth factor stimulates endothelial colony forming cells proliferation and tubulogenesis by inducing oscillations in intracellular Ca2+ concentration. Stem Cells 2011; 29:1898-907; PMID:21905169; http://dx.doi.org/10.1002/stem.734.
131. Müller MR, Rao A. NFAT, immunity and cancer: a transcription factor comes of age. Nat Rev Immunol 2010; 10:645-56; PMID:20725108; http://dx.doi.org/10.1038/nri2818.
132. Armesilla AL, Lorenzo E, Gómez del Arco P, Martínez- Martínez S, Alfranca A, Redondo JM. Vascular endothelial growth factor activates nuclear factor of activated T cells in human endothelial cells: a role for tissue factor gene expression. Mol Cell Biol 1999; 19:2032-43; PMID:10022890. (Pubitemid 29098261)
133. van den Berg YW, Osanto S, Reitsma PH, Versteeg HH. The relationship between tissue factor and cancer progression: insights from bench and bedside. Blood 2012; 119:924-32; PMID:22065595; http://dx.doi.org/10.1182/blood-2011-06- 317685.
134. Gupta GP, Nguyen DX, Chiang AC, Bos PD, Kim JY, Nadal C, et al. Mediators of vascular remodelling co-opted for sequential steps in lung metastasis. Nature 2007; 446:765-70; PMID:17429393; http://dx.doi.org/10.1038/nature05760. (Pubitemid 46582040)
135. Hernández GL, Volpert OV, Iñiguez MA, Lorenzo E, Martínez-Martínez S, Grau R, et al. Selective inhibition of vascular endothelial growth factor-mediated angiogenesis by cyclosporin A: roles of the nuclear factor of activated T cells and cyclooxygenase 2. J Exp Med 2001; 193:607-20; PMID:11238591; http://dx.doi.org/10.1084/jem.193.5.607. (Pubitemid 32539557)
136. Baek KH, Zaslavsky A, Lynch RC, Britt C, Okada Y, Siarey RJ, et al. Down's syndrome suppression of tumour growth and the role of the calcineurin inhibitor DSCR1. Nature 2009; 459:1126-30; PMID:19458618; http://dx.doi.org/10. 1038/nature08062.
137. Siamakpour-Reihani S, Caster J, Bandhu Nepal D, Courtwright A, Hilliard E, Usary J, et al. The role of calcineurin/NFAT in SFRP2 induced angiogenesis-a rationale for breast cancer treatment with the calcineurin inhibitor tacrolimus. PLoS One 2011; 6:e20412; PMID:21673995; http://dx.doi.org/10.1371/journal. pone.0020412.
138. Jackson SP, Schoenwaelder SM. Procoagulant platelets: are they necrotic? Blood 2010; 116:2011-8; PMID:20538794; http://dx.doi.org/10.1182/blood-2010-01- 261669.
139. Pores-Fernando AT, Zweifach A. Calcium influx and signaling in cytotoxic T-lymphocyte lytic granule exocytosis. Immunol Rev 2009; 231:160-73; PMID:19754896; http://dx.doi.org/10.1111/j.1600-065X.2009.00809.x.
140. Dantal J, Soulillou JP. Immunosuppressive drugs and the risk of cancer after organ transplantation. N Engl J Med 2005; 352:1371-3; PMID:15800234; http://dx.doi.org/10.1056/NEJMe058018. (Pubitemid 40411505)
141. Hojo M, Morimoto T, Maluccio M, Asano T, Morimoto K, Lagman M, et al. Cyclosporine induces cancer progression by a cell-autonomous mechanism. Nature 1999; 397:530-4; PMID:10028970; http://dx.doi.org/10.1038/17401.
142. Oh-Hora M, Komatsu N, Pishyareh M, Feske S, Hori S, Taniguchi M, Rao A, Takayanagi H. Agonist-selected T cell development requires strong T cell receptor signaling and store-operated calcium entry. Immunity. 2013; 38:881-895; PMID:23499491; http://dx.doi.org/10.1016/j.immuni.2013.02.008