Store-Operated Orai Channels: Structure and Function

Current Topics in Membranes

Volumn 71, Issue , 2013, Pages 1-32

  Prakriya, Murali ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

CRAC channel; Gating; Orai1; Permeation; Review; STIM1; Store operated channel

Indexed keywords

EID: 84880762970     PISSN: 10635823     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-407870-3.00001-9     Document Type: Chapter

References (117)

1. 3+ concentrations block the calcium release-activated channel, and impair CD69 and CD25 expression in CD3- or thapsigargin-activated Jurkat cells. The Biochemical Journal 1996, 313(Pt. 3):909-913.
2. 2+ entry through its constitutive and inducible movement in the endoplasmic reticulum. Proceedings of the National Academy of Sciences of the United States of America 2006, 103(45):16704-16709.
3. CRAC in rat basophilic leukemia cells. Pflügers Archiv: European Journal of Physiology 2002, 443(5-6):892-902.
4. Bird G.S., Hwang S.Y., Smyth J.T., Fukushima M., Boyles R.R., Putney J.W. STIM1 is a calcium sensor specialized for digital signaling. Current Biology 2009, 19(20):1724-1729.
5. 2+ levels. Cell 2007, 131(7):1327-1339.
6. 2+ influx by interacting with the C-terminal acidic coiled coil of Orai1. Biochemistry 2010, 49(6):1067-1071.
7. 2+ stores and on electrostatic interactions. Molecular Biology of the Cell 2009, 20(1):389-399.
8. 2+ current, IL-2 production and activation in T lymphocytes. British Journal of Pharmacology 1994, 113(3):861-868.
9. Chvanov M., Walsh C.M., Haynes L.P., Voronina S.G., Lur G., Gerasimenko O.V., et al. ATP depletion induces translocation of STIM1 to puncta and formation of STIM1-Orai1 clusters: Translocation and re-translocation of STIM1 does not require ATP. Pflügers Archiv: European Journal of Physiology 2008, 457(2):505-517.
10. Contreras J.E., Srikumar D., Holmgren M. Gating at the selectivity filter in cyclic nucleotide-gated channels. Proceedings of the National Academy of Sciences of the United States of America 2008, 105(9):3310-3314.
11. Covington E.D., Wu M.M., Lewis R.S. Essential role for the CRAC activation domain in store-dependent oligomerization of STIM1. Molecular Biology of the Cell 2010, 21(11):1897-1907.
12. DeHaven W.I., Smyth J.T., Boyles R.R., Bird G.S., Putney J.W. Complex actions of 2-aminoethyldiphenyl borate on store-operated calcium entry. The Journal of Biological Chemistry 2008, 283(28):19265-19273.
13. Dehaven W.I., Smyth J.T., Boyles R.R., Putney J.W. Calcium inhibition and calcium potentiation of Orai1, Orai2, and Orai3 calcium release-activated calcium channels. The Journal of Biological Chemistry 2007, 282(24):17548-17556.
14. 2+ concentration with targeted "cameleon" fluorescent proteins. Cell Calcium 2003, 34(2):109-119.
15. Demuro A., Penna A., Safrina O., Yeromin A.V., Amcheslavsky A., Cahalan M.D., et al. Subunit stoichiometry of human Orai1 and Orai3 channels in closed and open states. Proceedings of the National Academy of Sciences of the United States of America 2011, 108(43):17832-17837. (Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't).
16. 2+-dependent inactivation of Orai1 channels. The Journal of Biological Chemistry 2009, 284(37):24933-24938.
17. Di Capite J.L., Bates G.J., Parekh A.B. Mast cell CRAC channel as a novel therapeutic target in allergy. Current Opinion in Allergy and Clinical Immunology 2011, 11(1):33-38. (In Vitro Review).
18. Fanger C.M., Hoth M., Crabtree G.R., Lewis R.S. Characterization of T cell mutants with defects in capacitative calcium entry: Genetic evidence for the physiological roles of CRAC channels. The Journal of Cell Biology 1995, 131(3):655-667.
19. Feng M., Grice D.M., Faddy H.M., Nguyen N., Leitch S., Wang Y., et al. Store-independent activation of Orai1 by SPCA2 in mammary tumors. Cell 2010, 143(1):84-98.
20. 2+ entry in the immune system and beyond. Immunological Reviews 2009, 231(1):189-209.
21. Feske S. CRAC channelopathies. Pflügers Archiv: European Journal of Physiology 2010, 460:417-435.
22. Feske S., Giltnane J., Dolmetsch R., Staudt L.M., Rao A. Gene regulation mediated by calcium signals in T lymphocytes. Nature Immunology 2001, 2(4):316-324.
23. Feske S., Gwack Y., Prakriya M., Srikanth S., Puppel S.H., Tanasa B., et al. A mutation in Orai1 causes immune deficiency by abrogating CRAC channel function. Nature 2006, 441(7090):179-185.
24. Feske S., Muller J.M., Graf D., Kroczek R.A., Drager 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. European Journal of Immunology 1996, 26(9):2119-2126.
25. + channel gating in T cells from immunodeficient patients. The Journal of Experimental Medicine 2005, 202(5):651-662.
26. Fierro L., Parekh A.B. Fast calcium-dependent inactivation of calcium release-activated calcium current (CRAC) in RBL-1 cells. The Journal of Membrane Biology 1999, 168(1):9-17.
27. Frischauf I., Muik M., Derler I., Bergsmann J., Fahrner M., Schindl R., et al. Molecular determinants of the coupling between STIM1 and Orai channels: Differential activation of Orai1-3 channels by a STIM1 coiled-coil mutant. The Journal of Biological Chemistry 2009, 284(32):21696-21706.
28. Frischauf I., Schindl R., Bergsmann J., Derler I., Fahrner M., Muik M., et al. Cooperativeness of Orai cytosolic domains tunes subtype-specific gating. The Journal of Biological Chemistry 2011, 286(10):8577-8584.
29. Grigoriev I., Gouveia S.M., van der Vaart B., Demmers J., Smyth J.T., Honnappa S., et al. STIM1 is a MT-plus-end-tracking protein involved in remodeling of the ER. Current Biology 2008, 18(3):177-182.
30. 2+ (CRAC) channels. The Journal of Biological Chemistry 2007, 282(27):19375-19384.
31. Gwack Y., Srikanth S., Feske S., Cruz-Guilloty F., Oh-hora M., Neems D.S., et al. Biochemical and functional characterization of Orai proteins. The Journal of Biological Chemistry 2007, 282(22):16232-16243.
32. Gwozdz T., Dutko-Gwozdz J., Zarayskiy V., Peter K., Bolotina V.M. How strict is the correlation between STIM1 and Orai1 expression, puncta formation, and ICRAC activation?. American Journal of Physiology. Cell Physiology 2008, 295(5):C1133-C1140.
33. Hogan P.G., Chen L., Nardone J., Rao A. Transcriptional regulation by calcium, calcineurin, and NFAT. Genes & Development 2003, 17(18):2205-2232.
34. Hogan P.G., Lewis R.S., Rao A. Molecular basis of calcium signaling in lymphocytes: STIM and Orai. Annual Review of Immunology 2010, 28:491-533.
35. Honnappa S., Gouveia S.M., Weisbrich A., Damberger F.F., Bhavesh N.S., Jawhari H., et al. An EB1-binding motif acts as a microtubule tip localization signal. Cell 2009, 138(2):366-376.
36. 2+ (CRAC) channels by stromal interaction molecule 1 (STIM1). Proceedings of the National Academy of Sciences of the United States of America 2011, 108(32):13299-13304.
37. Hoth M., Penner R. Depletion of intracellular calcium stores activates a calcium current in mast cells. Nature 1992, 355(6358):353-356.
38. Hoth M., Penner R. Calcium release-activated calcium current in rat mast cells. The Journal of Physiology 1993, 465:359-386.
39. Hou X., Pedi L., Diver M.M., Long S.B. Crystal structure of the calcium release-activated calcium channel Orai. Science 2012, 338:1308-1313.
40. Huang G.N., Zeng W., Kim J.Y., Yuan J.P., Han L., Muallem S., et al. STIM1 carboxyl-terminus activates native SOC, I(crac) and TRPC1 channels. Nature Cell Biology 2006, 8(9):1003-1010.
41. Ji W., Xu P., Li Z., Lu J., Liu L., Zhan Y., et al. Functional stoichiometry of the unitary calcium-release-activated calcium channel. Proceedings of the National Academy of Sciences of the United States of America 2008, 105(36):13668-13673.
42. Karlin A., Akabas M.H. Substituted-cysteine accessibility method. Methods in Enzymology 1998, 293:123-145.
43. Kawasaki T., Lange I., Feske S. A minimal regulatory domain in the C terminus of STIM1 binds to and activates Orai1 CRAC channels. Biochemical and Biophysical Research Communications 2009, 385:49-54.
44. Korzeniowski M.K., Manjarres I.M., Varnai P., Balla T. Activation of STIM1-Orai1 involves an intramolecular switching mechanism. Science Signaling 2010, 3(148):ra82.
45. 2+. Voltage and concentration dependence of calcium entry into the pore. The Journal of General Physiology 1986, 88(3):321-347.
46. Le Deist F., Hivroz C., Partiseti M., Thomas C., Buc H.A., Oleastro M., et al. A primary T-cell immunodeficiency associated with defective transmembrane calcium influx. Blood 1995, 85(4):1053-1062.
47. 2+-dependent inactivation and gating of the Orai channels. Proceedings of the National Academy of Sciences of the United States of America 2009, 106(34):14687-14692.
48. CRAC) in Jurkat T cells. Biophysical Journal 1996, 71(2):787-794.
49. Lewis R.S. Calcium signaling mechanisms in T lymphocytes. Annual Review of Immunology 2001, 19:497-521.
50. Lewis R.S. Store-operated calcium channels: New perspectives on mechanism and function. Cold Spring Harbor Perspectives in Biology 2011, 3. a003970.
51. 2+ current in human leukemic T cells. Cell Regulation 1989, 1(1):99-112.
52. Li Z., Liu L., Deng Y., Ji W., Du W., Xu P., et al. Graded activation of CRAC channel by binding of different numbers of STIM1 to Orai1 subunits. Cell Research 2010, 21(2):305-315.
53. 2+ channel activation. The Journal of Biological Chemistry 2007, 282(40):29448-29456.
54. 2+ store depletion. Proceedings of the National Academy of Sciences of the United States of America 2007, 104(22):9301-9306.
55. 2+ influx. Current Biology 2005, 15(13):1235-1241.
56. 2+ channels with distinct functional properties. Current Biology 2007, 17(9):794-800.
57. Lis A., Zierler S., Peinelt C., Fleig A., Penner R. A single lysine in the N-terminal region of store-operated channels is critical for STIM1-mediated gating. The Journal of General Physiology 2010, 136(6):673-686.
58. Luik R.M., Wang B., Prakriya M., Wu M.M., Lewis R.S. Oligomerization of STIM1 couples ER calcium depletion to CRAC channel activation. Nature 2008, 454:538-542.
59. 2+ entry: Local activation of CRAC channels by STIM1 at ER-plasma membrane junctions. The Journal of Cell Biology 2006, 174(6):815-825.
60. Ma J., McCarl C.A., Khalil S., Luthy 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. European Journal of Immunology 2010, 40(11):3028-3042. (Research Support, N.I.H., Extramural).
61. Madl J., Weghuber J., Fritsch R., Derler I., Fahrner M., Frischauf I., et al. Resting-state Orai1 diffuses as homotetramer in the plasma membrane of live mammalian cells. The Journal of Biological Chemistry 2010, 285:41135-41142.
62. Maruyama Y., Ogura T., Mio K., Kato K., Kaneko T., Kiyonaka S., et al. Tetrameric Orai1 is a teardrop-shaped molecule with a long, tapered cytoplasmic domain. The Journal of Biological Chemistry 2009, 284(20):13676-13685.
63. 2+ entry through Orai1 is critical for T cell-mediated autoimmunity and allograft rejection. The Journal of Immunology 2010, 185(10):5845-5858.
64. McNally B.A., Somasundaram A., Jairaman A., Yamashita M., Prakriya M. The C- and N-terminal STIM1 binding sites on Orai1 are required for both trapping and gating CRAC channels. The Journal of Physiology 2013, 591:2833-2850.
65. McNally B.A., Somasundaram A., Yamashita M., Prakriya M. Gated regulation of CRAC channel ion selectivity by STIM1. Nature 2012, 482:241-245.
66. McNally B.A., Yamashita M., Engh A., Prakriya M. Structural determinants of ion permeation in CRAC channels. Proceedings of the National Academy of Sciences of the United States of America 2009, 106:22516-22521.
67. Mercer J.C., Dehaven W.I., Smyth J.T., Wedel B., Boyles R.R., Bird G.S., et al. Large store-operated calcium selective currents due to co-expression of Orai1 or Orai2 with the intracellular calcium sensor, Stim1. The Journal of Biological Chemistry 2006, 281(34):24979-24990.
68. Mignen O., Thompson J.L., Shuttleworth T.J. Orai1 subunit stoichiometry of the mammalian CRAC channel pore. The Journal of Physiology 2008, 586(2):419-425.
69. Muik M., Fahrner M., Derler I., Schindl R., Bergsmann J., Frischauf I., et al. A cytosolic homomerization and a modulatory domain within STIM1 C terminus determine coupling to Orai1 channels. The Journal of Biological Chemistry 2009, 284(13):8421-8426.
70. Muik M., Fahrner M., Schindl R., Stathopulos P., Frischauf I., Derler I., et al. STIM1 couples to Orai1 via an intramolecular transition into an extended conformation. The EMBO Journal 2011, 30:1678-1689.
71. 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. The Journal of Biological Chemistry 2008, 283:8014-8022.
72. 2+-dependent inactivation of CRAC channels. Proceedings of the National Academy of Sciences of the United States of America 2009, 106(36):15495-15500.
73. Navarro-Borelly L., Somasundaram A., Yamashita M., Ren D., Miller R.J., Prakriya M. STIM1-Orai1 interactions and Orai1 conformational changes revealed by live-cell FRET microscopy. The Journal of Physiology 2008, 586(22):5383-5401.
74. Park C.Y., Hoover P.J., Mullins F.M., Bachhawat P., Covington E.D., Raunser S., et al. STIM1 clusters and activates CRAC channels via direct binding of a cytosolic domain to Orai1. Cell 2009, 136(5):876-890.
75. 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. The Journal of Biological Chemistry 1994, 269(51):32327-32335.
76. Parvez S., Beck A., Peinelt C., Soboloff J., Lis A., Monteilh-Zoller M., et al. STIM2 protein mediates distinct store-dependent and store-independent modes of CRAC channel activation. The FASEB Journal 2008, 22(3):752-761.
77. Peinelt C., Lis A., Beck A., Fleig A., Penner R. 2-Aminoethoxydiphenyl borate directly facilitates and indirectly inhibits STIM1-dependent gating of CRAC channels. The Journal of Physiology 2008, 586(13):3061-3073.
78. Peinelt C., Vig M., Koomoa D.L., Beck A., Nadler M.J., Koblan-Huberson M., et al. Amplification of CRAC current by STIM1 and CRACM1 (Orai1). Nature Cell Biology 2006, 8(7):771-773.
79. Penna A., Demuro A., Yeromin A.V., Zhang S.L., Safrina O., Parker I., et al. The CRAC channel consists of a tetramer formed by Stim-induced dimerization of Orai dimers. Nature 2008, 456(7218):116-120.
80. Prakriya M. The molecular physiology of CRAC channels. Immunological Reviews 2009, 231(1):88-98.
81. Prakriya M., Feske S., Gwack Y., Srikanth S., Rao A., Hogan P.G. Orai1 is an essential pore subunit of the CRAC channel. Nature 2006, 443(7108):230-233.
82. 2+-inhibited cation (MIC) channels. The Journal of General Physiology 2002, 119(5):487-507.
83. Prakriya M., Lewis R.S. CRAC channels: Activation, permeation, and the search for a molecular identity. Cell Calcium 2003, 33(5-6):311-321.
84. Prakriya M., Lewis R.S. Store-operated calcium channels: Properties, functions and the search for a molecular mechanism. Advances in Molecular and Cell Biology 2004, 32:121-140.
85. Prakriya M., Lewis R.S. Regulation of CRAC channel activity by recruitment of silent channels to a high open-probability gating mode. The Journal of General Physiology 2006, 128(3):373-386.
86. Prevarskaya N., Skryma R., Shuba Y. Calcium in tumour metastasis: New roles for known actors. Nature Reviews. Cancer 2011, 11:609-618. (Research Support, Non-U.S. Gov't Review).
87. 2+ channel function. The Journal of Cell Biology 2005, 169(3):435-445.
88. Sather W.A., McCleskey E.W. Permeation and selectivity in calcium channels. Annual Review of Physiology 2003, 65:133-159.
89. Schindl R., Bergsmann J., Frischauf I., Derler I., Fahrner M., Muik M., et al. 2-Aminoethoxydiphenyl borate alters selectivity of Orai3 channels by increasing their pore size. The Journal of Biological Chemistry 2008, 283(29):20261-20267.
90. Schuhmann M.K., 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. The Journal of Immunology 2010, 184(3):1536-1542.
91. Scrimgeour N., Litjens T., Ma L., Barritt G.J., Rychkov G.Y. Properties of Orai1 mediated store-operated current depend on the expression levels of STIM1 and Orai1 proteins. The Journal of Physiology 2009, 587:2903-2918.
92. Soboloff J., Spassova M.A., Tang X.D., Hewavitharana T., Xu W., Gill D.L. Orai1 and STIM reconstitute store-operated calcium channel function. The Journal of Biological Chemistry 2006, 281(30):20661-20665.
93. 2+ channels. The Journal of Biological Chemistry 2010, 285(7):5066-5075.
94. 2+ entry. The Journal of Biological Chemistry 2006, 281(47):35855-35862.
95. 2+ channels is responsible for the inactivation of its monovalent cation current. Biophysical Journal 2004, 86(2):805-814.
96. 2+-activated K+channels. The Journal of General Physiology 2012, 139(3):235-244.
97. Ulbrich M.H., Isacoff E.Y. Subunit counting in membrane-bound proteins. Nature Methods 2007, 4(4):319-321.
98. Varga-Szabo D., Braun A., Nieswandt B. STIM and Orai in platelet function. Cell Calcium 2011, 50(3):270-278.
99. Vig M., Beck A., Billingsley J.M., Lis A., Parvez S., Peinelt C., et al. CRACM1 multimers form the ion-selective pore of the CRAC channel. Current Biology 2006, 16(20):2073-2079.
100. 2+ entry. Science 2006, 312:1220-1223.
101. Wissenbach U., Philipp S.E., Gross S.A., Cavalie A., Flockerzi V. Primary structure, chromosomal localization and expression in immune cells of the murine Orai and STIM genes. Cell Calcium 2007, 42(4-5):439-446.
102. 2+ store depletion causes STIM1 to accumulate in ER regions closely associated with the plasma membrane. The Journal of Cell Biology 2006, 174(6):803-813.
103. 2+-dependent inactivation of CRAC channels: Evidence for coupling of permeation and gating. The Journal of General Physiology 2007, 130(5):525-540.
104. Yamashita M., Somasundaram A., Prakriya M. Competitive modulation of CRAC channel gating by STIM1 and 2-aminoethyldiphenyl borate (2-APB). The Journal of Biological Chemistry 2011, 286:9429-9442.
105. Yang X., Jin H., Cai X., Li S., Shen Y. Structural and mechanistic insights into the activation of Stromal interaction molecule 1 (STIM1). Proceedings of the National Academy of Sciences of the United States of America 2012, 109(15):5657-5662. (Research Support, Non-U.S. Gov't).
106. Yeromin A.V., Zhang S.L., Jiang W., Yu Y., Safrina O., Cahalan M.D. Molecular identification of the CRAC channel by altered ion selectivity in a mutant of Orai. Nature 2006, 443(7108):226-229.
107. Yu F., Sun L., Hubrack S., Selvaraj S., Machaca K. Intramolecular shielding maintains STIM1 in an inactive conformation. Journal of Cell Science 2013, 10.1242/jcs.117200.
108. Yuan J.P., Zeng W., Dorwart M.R., Choi Y.J., Worley P.F., Muallem S. SOAR and the polybasic STIM1 domains gate and regulate Orai channels. Nature Cell Biology 2009, 11(3):337-343.
109. 2+ channel activity of human Orai1 and Orai3. The Journal of Biological Chemistry 2008, 283(25):17662-17671.
110. 2+ channel activity. Proceedings of the National Academy of Sciences of the United States of America 2006, 103(24):9357-9362.
111. 2+ store to the plasma membrane. Nature 2005, 437(7060):902-905.
112. Zheng L., Stathopulos P.B., Schindl R., Li G.Y., Romanin C., Ikura M. Auto-inhibitory role of the EF-SAM domain of STIM proteins in store-operated calcium entry. Proceedings of the National Academy of Sciences of the United States of America 2011, 108(4):1337-1342.
113. Zhou Y., Meraner P., Kwon H.T., Machnes D., Oh-hora M., Zimmer J., et al. STIM1 gates the store-operated calcium channel Orai1 in vitro. Nature Structural & Molecular Biology 2010, 17(1):112-116.
114. Zhou Y., Ramachandran S., Oh-Hora M., Rao A., Hogan P.G. Pore architecture of the Orai1 store-operated calcium channel. Proceedings of the National Academy of Sciences of the United States of America 2010, 107(11):4896-4901.
115. 2+ stores. Proceedings of the National Academy of Sciences of the United States of America 1993, 90(13):6295-6299.
116. CRAC) due to local calcium feedback. The Journal of General Physiology 1995, 105(2):209-226.
117. Zweifach A., Lewis R.S. Calcium-dependent potentiation of store-operated calcium channels in T lymphocytes. The Journal of General Physiology 1996, 107(5):597-610.