STIM and Orai proteins and the non-capacitative ARC channels

Frontiers in Bioscience

Volumn 17, Issue 3, 2012, Pages 847-860

  Shuttleworth, Trevor J ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

Arachidonic acid; Beta cells; Calcium channels; Calcium entry; Calcium oscillations; Calcium signaling; CRAC channels; Orai proteins; Review; STIM proteins

Indexed keywords

EID: 84860347137     PISSN: 27686701     EISSN: 27686698     Source Type: Journal    
DOI: 10.2741/3960     Document Type: Article

References (86)

1. J. W. Putney, Jr.: A model for receptor-regulated calcium entry. Cell Calcium 7, 1-12, (1986). (Pubitemid 16130733)
2. A. B. Parekh and J. W. Putney, Jr.: Store-operated calcium channels. Physiol Rev. 85, 757-810, (2005). (Pubitemid 40404641)
3. R. S. Lewis and M. D. Cahalan: Mitogen-induced oscillations of cytosolic Ca2+ and transmembrane Ca2+ current in human leukemic T cells. Cell Regul. 1, 99-112, (1989).
4. M. Hoth and R. Penner: Depletion of intracellular calcium stores activates a calcium current in mast cells. Nature 355, 353-356, (1992).
5. W. C. Chang, J. Di Capite, C. Nelson, and A. B. Parekh: All-or-none activation of CRAC channels by agonist elicits graded responses in populations of mast cells. J.Immunol. 179, 5255-5263, (2007).
6. C. Peinelt, A. Beck, M. K. Monteilh-Zoller, R. Penner, and A. Fleig: IP(3) receptor subtype-dependent activation of store-operated calcium entry through I(CRAC). Cell Calcium (2009).
7. M. K. Park, O. H. Petersen, and A. V. Tepikin: The endoplasmic reticulum as one continuous Ca(2+) pool: visualization of rapid Ca(2+) movements and equilibration. EMBO J. 19, 5729-5739, (2000).
8. R. Jacob, J. E. Merritt, T. J. Hallam, and T. J. Rink: Repetitive spikes in cytoplasmic calcium evoked by histamine in human endothelial cells. Nature 335, 40-45, (1988).
9. T. Kawanishi, L. M. Blank, A. T. Harootunian, M. T. Smith, and R. Y. Tsien: Ca2+ oscillations induced by hormonal stimulation of individual fura-2-loaded hepatocytes. J.Biol.Chem. 264, 12859-12866, (1989). (Pubitemid 19194855)
10. T. A. Rooney, E. J. Sass, and A. P. Thomas: Characterization of cytosolic calcium oscillations induced by phenylephrine and vasopressin in single fura- 2-loaded hepatocytes. J.Biol.Chem. 264, 17131-17141, (1989). (Pubitemid 19255543)
11. S. Girard and D. Clapham: Acceleration of intracellular calcium waves in Xenopus oocytes by calcium influx. Science 260, 229-232, (1993). (Pubitemid 23140891)
12. M. J. Berridge: Relationship between latency and period for 5-hydroxytryptamine- induced membrane responses in the Calliphora salivary gland. Biochem.J. 302, 545-550, (1994). (Pubitemid 24280111)
13. R. M. Luik, B. Wang, M. Prakriya, M. M. Wu, and R. S. Lewis: Oligomerization of STIM1 couples ER calcium depletion to CRAC channel activation. Nature 454, 538-542, (2008).
14. T. J. Shuttleworth and J. L. Thompson: Evidence for a non-capacitative Ca2+ entry during [Ca2+] oscillations. Biochem.J. 316 ( Pt 3), 819-824, (1996).
15. T. J. Shuttleworth: What drives calcium entry during [Ca2+]i oscillations?-challenging the capacitative model. Cell Calcium 25, 237-246, (1999).
16. L. Munaron, S. Antoniotti, C. Distasi, and D. Lovisolo: Arachidonic acid mediates calcium influx induced by basic fibroblast growth factor in Balb-c 3T3 fibroblasts. Cell Calcium 22, 179-188, (1997). (Pubitemid 27434799)
17. L. M. Broad, T. R. Cannon, and C. W. Taylor: A non-capacitative pathway activated by arachidonic acid is the major Ca2+ entry mechanism in rat A7r5 smooth muscle cells stimulated with low concentrations of vasopressin. J.Physiol 517 ( Pt 1), 121-134, (1999). (Pubitemid 29243476)
18. T. J. Shuttleworth: Arachidonic acid activates the noncapacitative entry of Ca2+ during [Ca2+]i oscillations. J.Biol.Chem. 271, 21720-21725, (1996). (Pubitemid 26303786)
19. T. J. Shuttleworth and J. L. Thompson: Muscarinic receptor activation of arachidonate-mediated Ca2+ entry in HEK293 cells is independent of phospholipase C. J.Biol.Chem. 273, 32636-32643, (1998). (Pubitemid 28557645)
20. O. Mignen and T. J. Shuttleworth: I(ARC), a novel arachidonate-regulated, noncapacitative Ca(2+) entry channel. J.Biol.Chem. 275, 9114-9119, (2000). (Pubitemid 30185125)
21. O. Mignen, J. L. Thompson, and T. J. Shuttleworth: Ca2+ selectivity and fatty acid specificity of the noncapacitative, arachidonate-regulated Ca2+ (ARC) channels. J.Biol.Chem. 278, 10174-10181, (2003). (Pubitemid 36800276)
22. O. Mignen, J. L. Thompson, and T. J. Shuttleworth: Reciprocal regulation of capacitative and arachidonateregulated noncapacitative Ca2+ entry pathways. J.Biol.Chem. 276, 35676-35683, (2001).
23. R. J. Soberman, T. W. Harper, D. Betteridge, R. A. Lewis, and K. F. Austen: Characterization and separation of the arachidonic acid 5-lipoxygenase and linoleic acid omega-6 lipoxygenase (arachidonic acid 15-lipoxygenase) of human polymorphonuclear leukocytes. J.Biol.Chem. 260, 4508-4515, (1985). (Pubitemid 15092935)
24. Y. Xu, S. Phipps, M. J. Turner, and D. L. Simmons: The N-terminus of COX-1 and its effect on cyclooxygenase-1 catalytic activity. J.Genet.Genomics 37, 117-123, (2010).
25. W. Liu, D. Cao, S. F. Oh, C. N. Serhan, and R. J. Kulmacz: Divergent cyclooxygenase responses to fatty acid structure and peroxide level in fish and mammalian prostaglandin H synthases. FASEB J. 20, 1097-1108, (2006). (Pubitemid 44943906)
26. G. V. Richieri, R. T. Ogata, and A. M. Kleinfeld: A fluorescently labeled intestinal fatty acid binding protein. Interactions with fatty acids and its use in monitoring free fatty acids. J.Biol.Chem. 267, 23495-23501, (1992). (Pubitemid 23088146)
27. D. B. Sawyer and O. S. Andersen: Platelet-activating factor is a general membrane perturbant. Biochim.Biophys.Acta 987, 129-132, (1989). (Pubitemid 20009007)
28. A. S. Yoo, I. Cheng, S. Chung, T. Z. Grenfell, H. Lee, E. Pack-Chung, M. Handler, J. Shen, W. M. Xia, G. Tesco, A. J. Saunders, K. Ding, M. P. Frosch, R. E. Tanzi, and T. W. Kim: Presenilin-mediated modulation of capacitative calcium entry. Neuron 27, 561-572, (2000).
29. Y. S. Li, P. Wu, X. Y. Zhou, J. G. Chen, L. Cai, F. Wang, L. M. Xu, X. L. Zhang, Y. Chen, S. J. Liu, Y. P. Huang, and D. Y. Ye: Formyl-peptide receptor like 1: a potent mediator of the Ca2+ release-activated Ca2+ current ICRAC. Arch.Biochem.Biophys. 478, 110-118, (2008).
30. V. Yeung-Yam-Wah, A. K. Lee, F. W. Tse, and A. Tse: Arachidonic acid stimulates extracellular Ca(2+) entry in rat pancreatic beta cells via activation of the noncapacitative arachidonate-regulated Ca(2+) (ARC) channels. Cell Calcium 47, 77-83, (2010).
31. J. Liou, M. L. Kim, W. D. Heo, J. T. Jones, J. W. Myers, J. E. Ferrell, Jr., and T. Meyer: STIM is a Ca2+ sensor essential for Ca2+-store-depletion- triggered Ca2+ influx. Curr.Biol. 15, 1235-1241, (2005). (Pubitemid 40950523)
32. J. Roos, P. J. DiGregorio, A. V. Yeromin, K. Ohlsen, M. Lioudyno, S. Zhang, O. Safrina, J. A. Kozak, S. L. Wagner, M. D. Cahalan, G. Velicelebi, and K. A. Stauderman: STIM1, an essential and conserved component of store-operated Ca2+ channel function. J.Cell Biol. 169, 435-445, (2005). (Pubitemid 40686694)
33. S. Feske, Y. Gwack, M. Prakriya, S. Srikanth, S. H. Puppel, B. Tanasa, P. G. Hogan, R. S. Lewis, M. Daly, and A. Rao: A mutation in Orai1 causes immune deficiency by abrogating CRAC channel function. Nature 441, 179-185, (2006).
34. S. L. Zhang, Y. Yu, J. Roos, J. A. Kozak, T. J. Deerinck, M. H. Ellisman, K. A. Stauderman, and M. D. Cahalan: STIM1 is a Ca2+ sensor that activates CRAC channels and migrates from the Ca2+ store to the plasma membrane. Nature 437, 902-905, (2005). (Pubitemid 41486767)
35. M. M. Wu, J. Buchanan, R. M. Luik, and R. S. Lewis: Ca2+ store depletion causes STIM1 to accumulate in ER regions closely associated with the plasma membrane. J.Cell Biol. 174, 803-813, (2006). (Pubitemid 44373730)
36. M. Prakriya, S. Feske, Y. Gwack, S. Srikanth, A. Rao, and P. G. Hogan: Orai1 is an essential pore subunit of the CRAC channel. Nature 443, 230-233, (2006). (Pubitemid 44387613)
37. A. V. Yeromin, S. L. Zhang, W. Jiang, Y. Yu, O. Safrina, and M. D. Cahalan: Molecular identification of the CRAC channel by altered ion selectivity in a mutant of Orai. Nature 443, 226-229, (2006). (Pubitemid 44387612)
38. C. Peinelt, M. Vig, D. L. Koomoa, A. Beck, M. J. Nadler, M. Koblan-Huberson, A. Lis, A. Fleig, R. Penner, and J. P. Kinet: Amplification of CRAC current by STIM1 and CRACM1 (Orai1). Nat.Cell Biol. 8, 771- 773, (2006).
39. O. Mignen, J. L. Thompson, and T. J. Shuttleworth: STIM1 regulates Ca2+ entry via arachidonate-regulated Ca2+-selective (ARC) channels without store depletion or translocation to the plasma membrane. J.Physiol 579, 703-715, (2007). (Pubitemid 46404353)
40. K. Oritani and P. W. Kincade: Identification of stromal cell products that interact with pre-B cells. J.Cell Biol. 134, 771-782, (1996). (Pubitemid 26269146)
41. S. S. Manji, N. J. Parker, R. T. Williams, L. Van Stekelenburg, R. B. Pearson, M. Dziadek, and P. J. Smith: STIM1: a novel phosphoprotein located at the cell surface. Biochim.Biophys.Acta 1481, 147-155, (2000). (Pubitemid 30658091)
42. R. T. Williams, P. V. Senior, L. Van Stekelenburg, J. E. Layton, P. J. Smith, and M. A. Dziadek: Stromal interaction molecule 1 (STIM1), a transmembrane protein with growth suppressor activity, contains an extracellular SAM domain modified by N-linked glycosylation. Biochim.Biophys.Acta 1596, 131-137, (2002). (Pubitemid 34450846)
43. M. A. Spassova, J. Soboloff, L. P. He, W. Xu, M. A. Dziadek, and D. L. Gill: STIM1 has a plasma membrane role in the activation of store-operated Ca(2+) channels. Proc.Natl.Acad.Sci.U.S.A 103, 4040-4045, (2006).
44. O. Mignen, J. L. Thompson, and T. J. Shuttleworth: Both Orai1 and Orai3 are essential components of the arachidonate-regulated Ca2+-selective (ARC) channels. J.Physiol 586, 185-195, (2008).
45. Y. Gwack, S. Srikanth, S. Feske, F. Cruz-Guilloty, M. Oh-Hora, D. S. Neems, P. G. Hogan, and A. Rao: Biochemical and functional characterization of orai proteins. J.Biol.Chem. 282, 16232-16243, (2007). (Pubitemid 47100386)
46. M. Vig, A. Beck, J. M. Billingsley, A. Lis, S. Parvez, C. Peinelt, D. L. Koomoa, J. Soboloff, D. L. Gill, A. Fleig, J. P. Kinet, and R. Penner: CRACM1 multimers form the ion-selective pore of the CRAC channel. Curr.Biol. 16, 2073-2079, (2006). (Pubitemid 44573821)
47. O. Mignen, J. L. Thompson, and T. J. Shuttleworth: Orai1 subunit stoichiometry of the mammalian CRAC channel pore. J.Physiol 586, 419-425, (2008).
48. W. Ji, P. Xu, Z. Li, J. Lu, L. Liu, Y. Zhan, Y. Chen, B. Hille, T. Xu, and L. Chen: Functional stoichiometry of the unitary calcium-release-activated calcium channel. Proc.Natl.Acad.Sci.U.S.A 105, 13668-13673, (2008).
49. A. Penna, A. Demuro, A. V. Yeromin, S. L. Zhang, O. Safrina, I. Parker, and M. D. Cahalan: The CRAC channel consists of a tetramer formed by Stim-induced dimerization of Orai dimers. Nature 456, 116-120, (2008).
50. Y. Maruyama, T. Ogura, K. Mio, K. Kato, T. Kaneko, S. Kiyonaka, Y. Mori, and C. Sato: Tetrameric Orai1 Is a Teardrop-shaped Molecule with a Long, Tapered Cytoplasmic Domain. J.Biol.Chem. 284, 13676-13685, (2009).
51. C. Y. Park, P. J. Hoover, F. M. Mullins, P. Bachhawat, E. D. Covington, S. Raunser, T. Walz, K. C. Garcia, R. E. Dolmetsch, and R. S. Lewis: STIM1 clusters and activates CRAC channels via direct binding of a cytosolic domain to Orai1. Cell 136, 876-890, (2009).
52. O. Mignen, J. L. Thompson, and T. J. Shuttleworth: The molecular architecture of the arachidonate-regulated Ca2+-selective ARC channel is a pentameric assembly of Orai1 and Orai3 subunits. J.Physiol 587, 4181-4197, (2009).
53. J. L. Thompson, O. Mignen, and T. J. Shuttleworth: The N-terminal domain of Orai3 determines selectivity for activation of the store-independent ARC channel by arachidonic acid. Channels (in press), (2010).
54. R. K. Motiani, I. F. Abdullaev, and M. Trebak: 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, (2010).
55. M. Faouzi, F. Hague, M. Potier, A. Ahidouch, H. Sevestre, and H. Ouadid-Ahidouch: 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 226, 542-551, (2011).
56. C. Peinelt, A. Lis, A. Beck, A. Fleig, and R. Penner: 2- Aminoethoxydiphenyl borate directly facilitates and indirectly inhibits STIM1-dependent gating of CRAC channels. J.Physiol 586, 3061-3073, (2008). (Pubitemid 351984690)
57. R. Schindl, J. Bergsmann, I. Frischauf, I. Derler, M. Fahrner, M. Muik, R. Fritsch, K. Groschner, and C. Romanin: 2-aminoethoxydiphenyl borate alters selectivity of Orai3 channels by increasing their pore size. J.Biol.Chem. 283, 20261-20267, (2008).
58. S. L. Zhang, J. A. Kozak, W. Jiang, A. V. Yeromin, J. Chen, Y. Yu, A. Penna, W. Shen, V. Chi, and M. D. Cahalan: Store-dependent and -independent Modes Regulating Ca2+ Release-activated Ca2+ Channel Activity of Human Orai1 and Orai3. J.Biol.Chem. 283, 17662- 17671, (2008).
59. W. I. Dehaven, J. T. Smyth, R. R. Boyles, G. S. Bird, and J. W. Putney, Jr.: Complex actions of 2- aminoethyldiphenyl borate on store-operated calcium entry. J.Biol.Chem. 283, 19265-19273, (2008).
60. J. W. Putney and G. S. Bird: Cytoplasmic calcium oscillations and store-operated calcium influx. J.Physiol 586, 3055-3059, (2008). (Pubitemid 351984689)
61. B. Wedel, R. R. Boyles, J. W. Putney, and G. S. Bird: Role of the Store-operated Calcium Entry Proteins, Stim1 and Orai1, in Muscarinic- Cholinergic Receptor Stimulated Calcium Oscillations in Human Embryonic Kidney Cells. J.Physiol (2007).
62. R. S. Lewis: Calcium signaling mechanisms in T lymphocytes. Annu.Rev.Immunol. 19, 497-521, (2001). (Pubitemid 32368044)
63. G. S. Bird, S. Y. Hwang, J. T. Smyth, M. Fukushima, R. R. Boyles, and J. W. Putney, Jr.: STIM1 is a calcium sensor specialized for digital signaling. Curr.Biol. 19, 1724-1729, (2009).
64. O. Mignen, J. L. Thompson, D. I. Yule, and T. J. Shuttleworth: Agonist activation of arachidonate-regulated Ca2+-selective (ARC) channels in murine parotid and pancreatic acinar cells. J.Physiol 564, 791-801, (2005). (Pubitemid 40704145)
65. X. Liu, W. Wang, B. B. Singh, T. Lockwich, J. Jadlowiec, B. O'Connell, R. Wellner, M. X. Zhu, and I. S. Ambudkar: Trp1, a candidate protein for the store-operated Ca(2+) influx mechanism in salivary gland cells. J.Biol.Chem. 275, 3403-3411, (2000). (Pubitemid 30083047)
66. X. Liu, K. T. Cheng, B. C. Bandyopadhyay, B. Pani, A. Dietrich, B. C. Paria, W. D. Swaim, D. Beech, E. Yildrim, B. B. Singh, L. Birnbaumer, and I. S. Ambudkar: Attenuation of store-operated Ca2+ current impairs salivary gland fluid secretion in TRPC1(/) mice. Proc.Natl.Acad.Sci.U.S.A (2007).
67. R. A. Liddle, I. D. Goldfine, M. S. Rosen, R. A. Taplitz, and J. A. Williams: Cholecystokinin bioactivity in human plasma. Molecular forms, responses to feeding, and relationship to gallbladder contraction. J.Clin.Invest 75, 1144-1152, (1985). (Pubitemid 15087139)
68. E. Krause, F. Pfeiffer, A. Schmid, and I. Schulz: Depletion of intracellular calcium stores activates a calcium conducting nonselective cation current in mouse pancreatic acinar cells. J.Biol.Chem. 271, 32523-32528, (1996). (Pubitemid 27008668)
69. M. Raraty, J. Ward, G. Erdemli, C. Vaillant, J. P. Neoptolemos, R. Sutton, and O. H. Petersen: Calciumdependent enzyme activation and vacuole formation in the apical granular region of pancreatic acinar cells. Proc.Natl.Acad.Sci.U.S.A 97, 13126-13131, (2000).
70. M. J. Berridge: Inositol trisphosphate and calcium signalling. Nature 361, 315-325, (1993). (Pubitemid 23041621)
71. P. De Koninck and H. Schulman: Sensitivity of CaM kinase II to the frequency of Ca2+ oscillations. Science 279, 227-230, (1998). (Pubitemid 28103880)
72. R. E. Dolmetsch, K. L. Xu, and R. S. Lewis: Calcium oscillations increase the efficiency and specificity of gene expression. Nature 392, 933-936, (1998). (Pubitemid 28232066)
73. G. Hajnoczky, L. D. Robb-Gaspers, M. B. Seitz, and A. P. Thomas: Decoding of cytosolic calcium oscillations in the mitochondria. Cell 82, 415-424, (1995).
74. E. Oancea and T. Meyer: Protein kinase C as a molecular machine for decoding calcium and diacylglycerol signals. Cell 95, 307-318, (1998). (Pubitemid 28507320)
75. T. Tomida, K. Hirose, A. Takizawa, F. Shibasaki, and M. Iino: NFAT functions as a working memory of Ca2+ signals in decoding Ca2+ oscillation. EMBO J. 22, 3825- 3832, (2003). (Pubitemid 36975710)
76. O. Mignen, J. L. Thompson, and T. J. Shuttleworth: Calcineurin directs the reciprocal regulation of calcium entry pathways in nonexcitable cells. J.Biol.Chem. 278, 40088-40096, (2003). (Pubitemid 37248575)
77. B. A. Wolf, S. M. Pasquale, and J. Turk: Free fatty acid accumulation in secretagogue-stimulated pancreatic islets and effects of arachidonate on depolarization-induced insulin secretion. Biochemistry 30, 6372-6379, (1991).
78. A. M. Band, P. M. Jones, and S. L. Howell: Arachidonic acid-induced insulin secretion from rat islets of Langerhans. J.Mol.Endocrinol. 8, 95-101, (1992).
79. P. M. Jones and S. J. Persaud: Arachidonic acid as a second messenger in glucose-induced insulin secretion from pancreatic beta-cells. J.Endocrinol. 137, 7-14, (1993). (Pubitemid 23100188)
80. S. Ramanadham, R. Gross, and J. Turk: Arachidonic acid induces an increase in the cytosolic calcium concentration in single pancreatic islet beta cells. Biochem.Biophys.Res.Commun. 184, 647-653, (1992).
81. Y. Itoh, Y. Kawamata, M. Harada, M. Kobayashi, R. Fujii, S. Fukusumi, K. Ogi, M. Hosoya, Y. Tanaka, H. Uejima, H. Tanaka, M. Maruyama, R. Satoh, S. Okubo, H. Kizawa, H. Komatsu, F. Matsumura, Y. Noguchi, T. Shinohara, S. Hinuma, Y. Fujisawa, and M. Fujino: Free fatty acids regulate insulin secretion from pancreatic beta cells through GPR40. Nature 422, 173-176, (2003). (Pubitemid 36362750)
82. E. Simonsson, S. Karlsson, and B. Ahren: Ca2+- independent phospholipase A2 contributes to the insulinotropic action of cholecystokinin-8 in rat islets: dissociation from the mechanism of carbachol. Diabetes 47, 1436-1443, (1998). (Pubitemid 28396947)
83. R. J. Konrad, Y. C. Jolly, C. Major, and B. A. Wolf: Carbachol stimulation of phospholipase A2 and insulin secretion in pancreatic islets. Biochem.J. 287 ( Pt 1), 283- 290, (1992).
84. D. A. Jacobson, C. R. Weber, S. Bao, J. Turk, and L. H. Philipson: Modulation of the pancreatic islet beta-celldelayed rectifier potassium channel Kv2.1 by the polyunsaturated fatty acid arachidonate. J.Biol.Chem. 282, 7442-7449, (2007). (Pubitemid 47093692)
85. E. Simonsson, S. Karlsson, and B. Ahren: Involvement of phospholipase A2 and arachidonic acid in cholecystokinin-8-induced insulin secretion in rat islets. Regul.Pept. 65, 101-107, (1996). (Pubitemid 26301014)
86. S. J. Persaud, D. Muller, V. D. Belin, I. Kitsou- Mylona, H. Asare-Anane, A. Papadimitriou, C. J. Burns, G. C. Huang, S. A. Amiel, and P. M. Jones: The role of arachidonic acid and its metabolites in insulin secretion from human islets of langerhans. Diabetes 56, 197-203, (2007).