Molecular Regulation of the Pore Component of CRAC Channels, Orai1

Current Topics in Membranes

Volumn 71, Issue , 2013, Pages 181-207

  Srikanth, Sonal ^a   Gwack, Yousang ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Channel gating; Channel inactivation; CRAC channels; Orai1; Posttranslational modification; Protein interaction; STIM1

Indexed keywords

EID: 84880704667     PISSN: 10635823     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-407870-3.00008-1     Document Type: Chapter

References (110)

1. Baba Y., Hayashi K., Fujii Y., Mizushima A., Watarai H., Wakamori M., et al. Coupling of STIM1 to store-operated Ca2+ 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, 103:16704-16709.
2. Baughman J.M., Perocchi F., Girgis H.S., Plovanich M., Belcher-Timme C.A., Sancak Y., et al. Integrative genomics identifies MCU as an essential component of the mitochondrial calcium uniporter. Nature 2011, 476:341-345.
3. Bautista D.M., Hoth M., Lewis R.S. Enhancement of calcium signalling dynamics and stability by delayed modulation of the plasma-membrane calcium-ATPase in human T cells. The Journal of Physiology 2002, 541:877-894.
4. Bautista D.M., Lewis R.S. Modulation of plasma membrane calcium-ATPase activity by local calcium microdomains near CRAC channels in human T cells. The Journal of Physiology 2004, 556:805-817.
5. Berridge M.J. Calcium microdomains: Organization and function. Cell Calcium 2006, 40:405-412.
6. Berridge M.J., Bootman M.D., Roderick H.L. Calcium signalling: Dynamics, homeostasis and remodelling. Nature Reviews. Molecular Cell Biology 2003, 4:517-529.
7. Budd R.C. Activation-induced cell death. Current Opinion in Immunology 2001, 13:356-362.
8. Cahalan M.D., Chandy K.G. The functional network of ion channels in T lymphocytes. Immunological Reviews 2009, 231:59-87.
9. Carrasco S., Meyer T. STIM proteins and the endoplasmic reticulum-plasma membrane junctions. Annual Review of Biochemistry 2011, 80:973-1000.
10. Chen Y.F., Chiu W.T., Chen Y.T., Lin P.Y., Huang H.J., Chou C.Y., et al. Calcium store sensor stromal-interaction molecule 1-dependent signaling plays an important role in cervical cancer growth, migration, and angiogenesis. Proceedings of the National Academy of Sciences of the United States of America 2011, 108:15225-15230.
11. Collins S.R., Meyer T. Evolutionary origins of STIM1 and STIM2 within ancient Ca2+ signaling systems. Trends in Cell Biology 2011, 21:202-211.
12. 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, 21:1897-1907.
13. 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, 108:17832-17837.
14. Derler I., Fahrner M., Muik M., Lackner B., Schindl R., Groschner K., et al. A Ca2(+)release-activated Ca2(+) (CRAC) modulatory domain (CMD) within STIM1 mediates fast Ca2(+)-dependent inactivation of ORAI1 channels. The Journal of Biological Chemistry 2009, 284:24933-24938.
15. De Stefani D., Raffaello A., Teardo E., Szabo I., Rizzuto R. A forty-kilodalton protein of the inner membrane is the mitochondrial calcium uniporter. Nature 2011, 476:336-340.
16. Eylenstein A., Gehring E.M., Heise N., Shumilina E., Schmidt S., Szteyn K., et al. Stimulation of Ca2+-channel Orai1/STIM1 by serum- and glucocorticoid-inducible kinase 1 (SGK1). FASEB Journal: Official Publication of the Federation of American Societies for Experimental Biology 2011, 25:2012-2021.
17. Feng J.M., Givogri I.M., Bongarzone E.R., Campagnoni C., Jacobs E., Handley V.W., et al. Thymocytes express the golli products of the myelin basic protein gene and levels of expression are stage dependent. Journal of Immunology 2000, 165:5443-5450.
18. 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, 143:84-98.
19. Feng J.M., Hu Y.K., Xie L.H., Colwell C.S., Shao X.M., Sun X.P., et al. Golli protein negatively regulates store depletion-induced calcium influx in T cells. Immunity 2006, 24:717-727.
20. Feske S. CRAC channelopathies. Pflügers Archiv 2010, 460:417-435.
21. 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, 441:179-185.
22. 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, 282:16232-16243.
23. Hogan P.G., Chen L., Nardone J., Rao A. Transcriptional regulation by calcium, calcineurin, and NFAT. Genes & Development 2003, 17:2205-2232.
24. 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.
25. Hoth M., Fanger C.M., Lewis R.S. Mitochondrial regulation of store-operated calcium signaling in T lymphocytes. The Journal of Cell Biology 1997, 137:633-648.
26. Hoth M., Penner R. Depletion of intracellular calcium stores activates a calcium current in mast cells. Nature 1992, 355:353-356.
27. Hoth M., Penner R. Calcium release-activated calcium current in rat mast cells. The Journal of Physiology 1993, 465:359-386.
28. 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.
29. Jans R., Mottram L., Johnson D.L., Brown A.M., Sikkink S., Ross K., et al. Lysophosphatidic acid promotes cell migration through STIM1- and Orai1-mediated Ca(2+)(i) mobilization and NFAT2 activation. The Journal of Investigative Dermatology 2012, 133:793-802.
30. 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, 105:13668-13673.
31. 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.
32. Kawasaki T., Ueyama T., Lange I., Feske S., Saito N. Protein kinase C-induced phosphorylation of Orai1 regulates the intracellular Ca2+ level via the store-operated Ca2+ channel. The Journal of Biological Chemistry 2010, 285:25720-25730.
33. Keil J.M., Shen Z., Briggs S.P., Patrick G.N. Regulation of STIM1 and SOCE by the ubiquitin-proteasome system (UPS). PLoS One 2010, 5:e13465.
34. Kim K.D., Srikanth S., Yee M.K., Mock D.C., Lawson G.W., Gwack Y. ORAI1 deficiency impairs activated T cell death and enhances T cell survival. Journal of Immunology 2011, 187:3620-3630.
35. Korzeniowski M.K., Manjarres I.M., Varnai P., Balla T. Activation of STIM1-Orai1 involves an intramolecular switching mechanism. Science Signaling 2010, 3:ra82.
36. Korzeniowski M.K., Popovic M.A., Szentpetery Z., Varnai P., Stojilkovic S.S., Balla T. Dependence of STIM1/Orai1-mediated calcium entry on plasma membrane phosphoinositides. The Journal of Biological Chemistry 2009, 284:21027-21035.
37. Krammer P.H., Arnold R., Lavrik I.N. Life and death in peripheral T cells. Nature Reviews. Immunology 2007, 7:532-542.
38. Krapivinsky G., Krapivinsky L., Stotz S.C., Manasian Y., Clapham D.E. POST, partner of stromal interaction molecule 1 (STIM1), targets STIM1 to multiple transporters. Proceedings of the National Academy of Sciences of the United States of America 2011, 108:19234-19239.
39. +-dependent inactivation and gating of the Orai channels. Proceedings of the National Academy of Sciences of the United States of America 2009, 106:14687-14692.
40. Lefkimmiatis K., Srikanthan M., Maiellaro I., Moyer M.P., Curci S., Hofer A.M. Store-operated cyclic AMP signalling mediated by STIM1. Nature Cell Biology 2009, 11:433-442.
41. Lewis R.S. Calcium signaling mechanisms in T lymphocytes. Annual Review of Immunology 2001, 19:497-521.
42. Lewis R.S. Store-operated calcium channels: New perspectives on mechanism and function. Cold Spring Harbor Perspectives in Biology 2011, 3. 10.1101/cshperspect.a003970.
43. Liou J., Fivaz M., Inoue T., Meyer T. Live-cell imaging reveals sequential oligomerization and local plasma membrane targeting of stromal interaction molecule 1 after Ca2+ store depletion. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:9301-9306.
44. Liou J., Kim M.L., Heo W.D., Jones J.T., Myers J.W., Ferrell J.E., et al. STIM is a Ca2+ sensor essential for Ca2+-store-depletion-triggered Ca2+ influx. Current Biology 2005, 15:1235-1241.
45. Lis A., Peinelt C., Beck A., Parvez S., Monteilh-Zoller M., Fleig A., et al. CRACM1, CRACM2, and CRACM3 are store-operated Ca2+ channels with distinct functional properties. Current Biology 2007, 17:794-800.
46. Liu Y., Zheng X., Mueller G.A., Sobhany M., Derose E.F., Zhang Y., et al. Crystal structure of calmodulin binding domain of orai1 in complex with ca2+ calmodulin displays a unique binding mode. The Journal of Biological Chemistry 2012, 287:43030-43041.
47. Loewen C.J., Young B.P., Tavassoli S., Levine T.P. Inheritance of cortical ER in yeast is required for normal septin organization. The Journal of Cell Biology 2007, 179:467-483.
48. Lopez E., Jardin I., Berna-Erro A., Bermejo N., Salido G.M., Sage S.O., et al. STIM1 tyrosine-phosphorylation is required for STIM1-Orai1 association in human platelets. Cellular Signalling 2012, 24:1315-1322.
49. Macian F., Garcia-Cozar F., Im S.H., Horton H.F., Byrne M.C., Rao A. Transcriptional mechanisms underlying lymphocyte tolerance. Cell 2002, 109:719-731.
50. 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.
51. Manford A.G., Stefan C.J., Yuan H.L., Macgurn J.A., Emr S.D. ER-to-plasma membrane tethering proteins regulate cell signaling and ER morphology. Developmental Cell 2012, 23:1129-1140.
52. 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, 281:24979-24990.
53. Mignen O., Thompson J.L., Shuttleworth T.J. STIM1 regulates Ca2+ entry via arachidonate-regulated Ca2+-selective (ARC) channels without store depletion or translocation to the plasma membrane. The Journal of Physiology 2007, 579:703-715.
54. Mignen O., Thompson J.L., Shuttleworth T.J. Orai1 subunit stoichiometry of the mammalian CRAC channel pore. The Journal of Physiology 2008, 586:419-425.
55. Mignen O., Thompson J.L., Shuttleworth T.J. The molecular architecture of the arachidonate-regulated Ca2+-selective ARC channel is a pentameric assembly of Orai1 and Orai3 subunits. The Journal of Physiology 2009, 587:4181-4197.
56. 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, 284:8421-8426.
57. Mullins F.M., Park C.Y., Dolmetsch R.E., Lewis R.S. STIM1 and calmodulin interact with Orai1 to induce Ca2+-dependent inactivation of CRAC channels. Proceedings of the National Academy of Sciences of the United States of America 2009, 106:15495-15500.
58. Oh-hora M., Rao A. Calcium signaling in lymphocytes. Current Opinion in Immunology 2008, 20:250-258.
59. Palty R., Raveh A., Kaminsky I., Meller R., Reuveny E. SARAF inactivates the store operated calcium entry machinery to prevent excess calcium refilling. Cell 2012, 149:425-438.
60. Parekh A.B. Slow feedback inhibition of calcium release-activated calcium current by calcium entry. The Journal of Biological Chemistry 1998, 273:14925-14932.
61. 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, 136:876-890.
62. 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, 22:752-761.
63. 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, 8:771-773.
64. 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, 456:116-120.
65. Pozo-Guisado E., Campbell D.G., Deak M., Alvarez-Barrientos A., Morrice N.A., Alvarez I.S., et al. Phosphorylation of STIM1 at ERK1/2 target sites modulates store-operated calcium entry. Journal of Cell Science 2010, 123:3084-3093.
66. Prakriya M., Lewis R.S. CRAC channels: Activation, permeation, and the search for a molecular identity. Cell Calcium 2003, 33:311-321.
67. Prins D., Groenendyk J., Touret N., Michalak M. Modulation of STIM1 and capacitative Ca(2+) entry by the endoplasmic reticulum luminal oxidoreductase ERp57. EMBO Reports 2011, 12:1182-1188.
68. Putney J.W. A model for receptor-regulated calcium entry. Cell Calcium 1986, 7:1-12.
69. Putney J.W. Capacitative calcium entry: From concept to molecules. Immunological Reviews 2009, 231:10-22.
70. Quintana A., Pasche M., Junker C., Al-Ansary D., Rieger H., Kummerow C., et al. Calcium microdomains at the immunological synapse: How ORAI channels, mitochondria and calcium pumps generate local calcium signals for efficient T-cell activation. The EMBO Journal 2011, 30:3895-3912.
71. Quintana A., Schwindling C., Wenning A.S., Becherer U., Rettig J., Schwarz E.C., et al. T cell activation requires mitochondrial translocation to the immunological synapse. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:14418-14423.
72. Ritchie M.F., Samakai E., Soboloff J. STIM1 is required for attenuation of PMCA-mediated Ca(2+) clearance during T-cell activation. The EMBO Journal 2012, 31:1123-1133.
73. Roos J., DiGregorio P.J., Yeromin A.V., Ohlsen K., Lioudyno M., Zhang S., et al. STIM1, an essential and conserved component of store-operated Ca2+ channel function. The Journal of Cell Biology 2005, 169:435-445.
74. Samelson L.E. Immunoreceptor signaling. Cold Spring Harbor Perspectives in Biology 2011, 3. 10.1101/cshperspect.a011510.
75. Santoso N.G., Cebotaru L., Guggino W.B. Polycystin-1, 2, and STIM1 interact with IP(3)R to modulate ER Ca release through the PI3K/Akt pathway. Cellular Physiology and Biochemistry: International Journal of Experimental Cellular Physiology, Biochemistry, and Pharmacology 2011, 27:715-726.
76. Serfling E., Avots A., Klein-Hessling S., Rudolf R., Vaeth M., Berberich-Siebelt F. NFATc1/alphaA: The other Face of NFAT Factors in Lymphocytes. Cell communication and signaling: CCS 2012, 10:16.
77. Smyth J.T., Petranka J.G., Boyles R.R., DeHaven W.I., Fukushima M., Johnson K.L., et al. Phosphorylation of STIM1 underlies suppression of store-operated calcium entry during mitosis. Nature Cell Biology 2009, 11:1465-1472.
78. Soboloff J., Rothberg B.S., Madesh M., Gill D.L. STIM proteins: Dynamic calcium signal transducers. Nature Reviews. Molecular Cell Biology 2012, 13:549-565.
79. Srikanth S., Gwack Y. Orai1, STIM1, and their associating partners. The Journal of Physiology 2012, 590:4169-4177.
80. Srikanth S., Gwack Y. Orai1-NFAT signalling pathway triggered by T cell receptor stimulation. Molecules and Cells 2013, 35:182-194.
81. Srikanth S., Jew M., Kim K.D., Yee M.K., Abramson J., Gwack Y. Junctate is a Ca2+-sensing structural component of Orai1 and stromal interaction molecule 1 (STIM1). Proceedings of the National Academy of Sciences of the United States of America 2012, 109:8682-8687.
82. Srikanth S., Jung H.J., Kim K.D., Souda P., Whitelegge J., Gwack Y. A novel EF-hand protein, CRACR2A, is a cytosolic Ca2+ sensor that stabilizes CRAC channels in T cells. Nature Cell Biology 2010, 12:436-446.
83. Srikanth S., Jung H.J., Ribalet B., Gwack Y. The intracellular loop of Orai1 plays a central role in fast inactivation of Ca2+ release-activated Ca2+ channels. The Journal of Biological Chemistry 2010, 285:5066-5075.
84. Srikanth S., Ribalet B., Gwack Y. Regulation of CRAC channels by protein interactions and posttranslational modification. Channels 2013, 7(5). 10.4161/chan.23801.
85. Srikanth S., Yee M.K., Gwack Y., Ribalet B. The third transmembrane segment of orai1 protein modulates Ca2+ release-activated Ca2+ (CRAC) channel gating and permeation properties. The Journal of Biological Chemistry 2011, 286:35318-35328.
86. Stathopulos P.B., Li G.Y., Plevin M.J., Ames J.B., Ikura M. Stored Ca2+ depletion-induced oligomerization of stromal interaction molecule 1 (STIM1) via the EF-SAM region: An initiation mechanism for capacitive Ca2+ entry. The Journal of Biological Chemistry 2006, 281:35855-35862.
87. Stefan C.J., Manford A.G., Emr S.D. ER-PM connections: Sites of information transfer and inter-organelle communication. Current Opinion in Cell Biology 2013, 25. 10.1016/j.ceb.2013.02.020.
88. Strasser A. The role of BH3-only proteins in the immune system. Nature Reviews. Immunology 2005, 5:189-200.
89. Takeshima H., Komazaki S., Nishi M., Iino M., Kangawa K. Junctophilins: A novel family of junctional membrane complex proteins. Molecular Cell 2000, 6:11-22.
90. Treves S., Feriotto G., Moccagatta L., Gambari R., Zorzato F. Molecular cloning, expression, functional characterization, chromosomal localization, and gene structure of junctate, a novel integral calcium binding protein of sarco(endo)plasmic reticulum membrane. The Journal of Biological Chemistry 2000, 275:39555-39568.
91. Treves S., Franzini-Armstrong C., Moccagatta L., Arnoult C., Grasso C., Schrum A., et al. Junctate is a key element in calcium entry induced by activation of InsP3 receptors and/or calcium store depletion. The Journal of Cell Biology 2004, 166:537-548.
92. Treves S., Vukcevic M., Griesser J., Armstrong C.F., Zhu M.X., Zorzato F. Agonist-activated Ca2+ influx occurs at stable plasma membrane and endoplasmic reticulum junctions. Journal of Cell Science 2010, 123:4170-4181.
93. Varnai P., Toth B., Toth D.J., Hunyady L., Balla T. Visualization and manipulation of plasma membrane-endoplasmic reticulum contact sites indicates the presence of additional molecular components within the STIM1-Orai1 Complex. The Journal of Biological Chemistry 2007, 282:29678-29690.
94. Vig M., Peinelt C., Beck A., Koomoa D.L., Rabah D., Koblan-Huberson M., et al. CRACM1 is a plasma membrane protein essential for store-operated Ca2+ entry. Science 2006, 312:1220-1223.
95. Walsh C.M., Chvanov M., Haynes L.P., Petersen O.H., Tepikin A.V., Burgoyne R.D. Role of phosphoinositides in STIM1 dynamics and store-operated calcium entry. The Biochemical Journal 2010, 425:159-168.
96. Walsh C.M., Doherty M.K., Tepikin A.V., Burgoyne R.D. Evidence for an interaction between Golli and STIM1 in store-operated calcium entry. The Biochemical Journal 2010, 430:453-460.
97. Weisleder N., Takeshima H., Ma J. Immuno-proteomic approach to excitation-contraction coupling in skeletal and cardiac muscle: Molecular insights revealed by the mitsugumins. Cell Calcium 2008, 43:1-8.
98. Willoughby D., Everett K.L., Halls M.L., Pacheco J., Skroblin P., Vaca L., et al. Direct binding between Orai1 and AC8 mediates dynamic interplay between Ca2+ and cAMP signaling. Science Signaling 2012, 5:ra29.
99. Woodward O.M., Li Y., Yu S., Greenwell P., Wodarczyk C., Boletta A., et al. Identification of a polycystin-1 cleavage product, P100, that regulates store operated Ca entry through interactions with STIM1. PLoS One 2010, 5:e12305.
100. Wu M.M., Buchanan J., Luik R.M., Lewis R.S. Ca2+ store depletion causes STIM1 to accumulate in ER regions closely associated with the plasma membrane. The Journal of Cell Biology 2006, 174:803-813.
101. Yang S., Zhang J.J., Huang X.Y. Orai1 and STIM1 are critical for breast tumor cell migration and metastasis. Cancer Cell 2009, 15:124-134.
102. Yu F., Sun L., Machaca K. Orai1 internalization and STIM1 clustering inhibition modulate SOCE inactivation during meiosis. Proceedings of the National Academy of Sciences of the United States of America 2009, 106:17401-17406.
103. Yu F., Sun L., Machaca K. Constitutive recycling of the store-operated Ca2+ channel Orai1 and its internalization during meiosis. The Journal of Cell Biology 2010, 191:523-535.
104. 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, 11:337-343.
105. Zeiger W., Ito D., Swetlik C., Oh-hora M., Villereal M.L., Thinakaran G. Stanniocalcin 2 is a negative modulator of store-operated calcium entry. Molecular and Cellular Biology 2011, 31:3710-3722.
106. Zhang S.L., Yeromin A.V., Zhang X.H., 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. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:9357-9362.
107. Zhang S.L., Yu Y., Roos J., Kozak J.A., Deerinck T.J., Ellisman M.H., et al. STIM1 is a Ca2+ sensor that activates CRAC channels and migrates from the Ca2+ store to the plasma membrane. Nature 2005, 437:902-905.
108. 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, 17:112-116.
109. Zweifach A., Lewis R.S. Rapid inactivation of depletion-activated calcium current (ICRAC) due to local calcium feedback. The Journal of General Physiology 1995, 105:209-226.
110. Zweifach A., Lewis R.S. Slow calcium-dependent inactivation of depletion-activated calcium current. Store-dependent and -independent mechanisms. The Journal of Biological Chemistry 1995, 270:14445-14451.