Capacitative calcium entry: From concept to molecules

Immunological Reviews

Volumn 231, Issue 1, 2009, Pages 10-22

  Putney, James W ^a  

^a NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

Author keywords

Calcium channels; Calcium oscillations; Capacitative calcium entry; Orai; Store operated calcium entry; Stromal interacting molecule

Indexed keywords

CALCIUM; CALCIUM RELEASE ACTIVATED CALCIUM CHANNEL 1; INOSITOL 1,4,5 TRISPHOSPHATE; PROTEIN SUBUNIT;

CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CELL FUNCTION; CELL MEMBRANE; ENDOPLASMIC RETICULUM; HUMAN; IMMUNE SYSTEM; MOLECULAR MECHANICS; OSCILLATION; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; CALCIUM; CELL MEMBRANE; ENDOPLASMIC RETICULUM; HUMANS; IMMUNE SYSTEM; MEMBRANE PROTEINS; SIGNAL TRANSDUCTION;

EID: 70349098735     PISSN: 01052896     EISSN: 1600065X     Source Type: Journal    
DOI: 10.1111/j.1600-065X.2009.00810.x     Document Type: Review

References (171)

1. Penner R, Neher E. Secretory responses of rat peritoneal mast cells to high intracellular calcium. FEBS Lett 1988 226 : 307 313.
2. 2+ influx across the plasma membrane of human neutrophils. Mol Pharmacol 1986 30 : 437 443.
3. 2+/calcineurin signalling in cells of the immune system. Biochem Biophys Res Commun 2003 311 : 1117 1132.
4. Bohr DF. Vascular smooth muscle updated. Circ Res 1973 32 : 665 672.
5. Somlyo AP, Somlyo AV. Electromechanical and pharmacomechanical coupling in vascular smooth muscle. J Pharmacol Exp Ther 1968 159 : 129 145.
6. Putney JW, Poggioli J, Weiss SJ. Receptor regulation of calcium release and calcium permeability in parotid gland cells. Philos Trans R Soc Lond B Biol Sci 1981 296 : 37 45.
7. Berridge MJ. Calcium oscillations. J Biol Chem 1990 265 : 9583 9586.
8. Woods NM, Cuthbertson KS, Cobbold PH. Repetitive transient rises in cytoplasmic free calcium in hormone-stimulated hepatocytes. Nature 1986 319 : 600 602.
9. Thomas AP, Bird GStJ, Hajnóczky G, Robb-Gaspers LD, Putney JW. Spatial and temporal aspects of cellular calcium signalling. FASEB J 1996 10 : 1505 1517.
10. Gilkey JC, Jaffe LF, Ridgway EB, Reynolds GT. A free calcium wave traverses the activating egg of medaka, Oryzias Latipes. J Cell Biol 1978 76 : 448 466.
11. 2+ oscillations: frequency encoding and identification of underlying feedbacks. Biophys J 2006 90 : 3120 3133.
12. Michell RH. Inositol phospholipids and cell surface receptor function. Biochim Biophys Acta 1975 415 : 81 147.
13. Berridge MJ. Rapid accumulation of inositol trisphosphate reveals that agonists hydrolyse polyphosphoinositides instead of phosphatidylinositol. Biochem J 1983 212 : 849 858.
14. 2+ from a nonmitochondrial store in pancreatic cells by inositol-1,4,5- trisphosphate. Nature 1983 306 : 67 68.
15. 2+ from isolated adipocyte endoplasmic reticulum but not from plasma membranes. Biochem J 1986 236 : 37 44.
16. 2+ fluxes in rat liver plasma-membrane vesicles. Biochem J 1988 256 : 117 124.
17. Kuno M, Gardner P. Ion channels activated by inositol 1,4,5-trisphosphate in plasma membrane of human T-lymphocytes. Nature 1987 326 : 301 304.
18. Vazquez G, Wedel BJ, Bird GStJ, Joseph SK, Putney JW. An inositol 1,4,5-trisphosphate receptor-dependent cation entry pathway in DT40 B lymphocytes. EMBO J 2002 21 : 4531 4538.
19. Dellis O, Rossi AM, Dedos SG, Taylor CW. Counting functional Inositol 1,4,5-trisphosphate receptors into the plasma membrane. J Biol Chem 2008 283 : 751 755.
20. Putney JW. Muscarinic, alpha-adrenergic and peptide receptors regulate the same calcium influx sites in the parotid gland. J Physiol (Lond) 1977 268 : 139 149.
21. Parod RJ, Putney JW. The role of calcium in the receptor mediated control of potassium permeability in the rat lacrimal gland. J Physiol (Lond) 1978 281 : 371 381.
22. Casteels R, Droogmans G. Exchange characteristics of the noradrenaline-sensitive calcium store in vascular smooth muscle cells of rabbit ear artery. J Physiol (Lond) 1981 317 : 263 279. (Pubitemid 12205874)
23. Putney JW. A model for receptor-regulated calcium entry. Cell Calcium 1986 7 : 1 12.
24. Takemura H, Putney JW. Capacitative calcium entry in parotid acinar cells. Biochem J 1989 258 : 409 412.
25. Thastrup O, Linnebjerg H, Bjerrum PJ, Knudsen JB, Christensen SB. The inflammatory and tumor-promoting sesquiterpene lactone, thapsigargin, activates platelets by selective mobilization of calcium as shown by protein phosphorylations. Biochim Biophys Acta 1987 927 : 65 73.
26. 2+ without generation of inositol phosphates in NG115-401L neuronal cells. Biochem J 1988 253 : 81 86.
27. Takemura H, Hughes AR, Thastrup O, Putney JW. Activation of calcium entry by the tumor promoter, thapsigargin, in parotid acinar cells. Evidence that an intracellular calcium pool, and not an inositol phosphate, regulates calcium fluxes at the plasma membrane. J Biol Chem 1989 264 : 12266 12271.
28. 2+ stores. FEBS Lett 1990 274 : 214 216.
29. 2+ -pump inhibitor of rat aortic smooth muscle. Acta Pharmacol Sinica 1991 12 : 1 6.
30. 2+current. Cell Regul 1989 1 : 99 112.
31. Hoth M, Penner R. Depletion of intracellular calcium stores activates a calcium current in mast cells. Nature 1992 355 : 353 355.
32. Hoth M, Penner R. Calcium release-activated calcium current in rat mast cells. J Physiol (Lond) 1993 465 : 359 386. (Pubitemid 23201401)
33. Parekh AB, Penner R. Store depletion and calcium influx. Physiol Rev 1997 77 : 901 930.
34. Parekh AB, Putney JW. Store-operated calcium channels. Physiol Rev 2005 85 : 757 810.
35. Prakriya M, Lewis RS. Regulation of CRAC channel activity by recruitment of silent channels to a high open-probability gating mode. J Gen Physiol 2006 128 : 373 386.
36. crac) in a mast cell line (RBL-1). J Biol Chem 1998 273 : 19554 19559.
37. CRAC. EMBO J 2000 19 : 6401 6407.
38. 2+ entry. Science 2006 312 : 1220 1223.
39. DeHaven WI, Smyth JT, Boyles RR, Putney JW. Calcium inhibition and calcium potentiation of Orai1, Orai2, and Orai3 calcium release-activated calcium channels. J Biol Chem 2007 282 : 17548 17556.
40. Zweifach A, Lewis RS. Calcium-dependent potentiation of store-operated calcium channels in T lymphocytes. J Gen Physiol 1996 107 : 597 610.
41. 2+influx. J Biol Chem 1994 269 : 12645 12653.
42. 2+stores. FASEB J 1992 6 : 786 792.
43. 2+ entry in human and bovine endothelial cells. J Physiol (Lond) 1995 482 : 259 274.
44. 2+ entry by inositol phosphates - a possible mechanism. FEBS Lett 1990 263 : 5 9.
45. 2+ influx. Nature 1993 364 : 809 814.
46. Kim HY, Thomas D, Hanley MR. Chromatographic resolution of an intracellular calcium influx factor from thapsigargin-activated Jurkat cells. J Biol Chem 1995 270 : 9706 9708.
47. Csutora P, et al. Calcium influx factor is synthesized by yeast and mammalian cells depleted of organellar calcium stores. Proc Natl Acad Sci USA 1999 96 : 121 126.
48. 2+-entry pathway. Trends Biochem Sci 2005 30 : 378 387.
49. 2+ current in Xenopus oocytes requires SNAP-25 but not a diffusible messenger. Cell 1999 98 : 475 485.
50. Berridge MJ. Capacitative calcium entry. Biochem J 1995 312 : 1 11.
51. Schneider MF. Control of calcium release in functioning muscle fibers. Ann Rev Physiol 1994 56 : 463 484.
52. 3 receptors and store-operated Htrp3 channels. Nature 1998 396 : 478 482.
53. 2+ entry. Proc Natl Acad Sci USA 1999 96 : 14955 14960.
54. Vazquez G, Bird GS, Mori Y, Putney JW. Native TRPC7 channel activation by an inositol trisphosphate receptor-dependent mechanism. J Biol Chem 2006 281 : 25250 25258.
55. Zarayskiy V, Monje F, Peter K, Csutora P, Khodorov BI, Bolotina VM. Store-operated Orai1 and IP3 receptor-operated TRPC1 channel. Channels (Austin) 2007 1 : 246 252.
56. 2+ channel in drosophila photoreceptors. Neuron 1992 8 : 643 651.
57. 2+ entry. Cell 1996 85 : 661 671.
58. Yue L, Peng J-B, Hediger MA, Clapham DE. CaT1 manifests the pore properties of the calcium release activated calcium channel. Nature 2001 410 : 705 709.
59. Voets T, et al. CaT1 and the calcium release-activated calcium channel manifest distinct pore properties. J Biol Chem 2001 276 : 47767 47770.
60. Zitt C, et al. Expression of TRPC3 in Chinese hamster ovary cells results in calcium-activated cation currents not related to store depletion. J Cell Biol 1997 138 : 1333 1341.
61. Schaefer M, Plant TD, Obukhov AG, Hofmann T, Gudermann T, Schultz G. Receptor-mediated regulation of the nonselective cation channels TRPC4 and TRPC5. J Biol Chem 2000 275 : 17517 17526.
62. Dietrich A, et al. Pressure-induced and store-operated cation influx in vascular smooth muscle cells is independent of TRPC1. Pflugers Arch 2007 455 : 465 477.
63. Varga-Szabo D, et al. Store-operated Ca(2+) entry in platelets occurs independently of transient receptor potential (TRP) C1. Pflugers Arch 2008 457 : 377 387.
64. McKay RR, et al. Cloning and expression of the human transient receptor potential 4 (TRP4) gene: localization and functional expression of human TRP4 and TRP3. Biochem J 2000 351 : 735 746.
65. Trebak M, Bird GStJ, McKay RR, Birnbaumer L, Putney JW. Signaling mechanism for receptor-activated TRPC3 channels. J Biol Chem 2003 278 : 16244 16252.
66. DeHaven WI, et al. TRPC channels function independently of STIM1 and Orai1. J Physiol (Lond) 2009 587 : 2275 2298.
67. Vazquez G, Lièvremont J-P, Bird GStJ, Putney JW. Human Trp3 forms both inositol trisphosphate receptor-dependent and receptor-independent store-operated cation channels in DT40 avian B-lymphocytes. Proc Natl Acad Sci USA 2001 98 : 11777 11782.
68. Lievremont JP, Bird GS, Putney JW. Canonical transient receptor potential TRPC7 can function as both a receptor- and store-operated channel in HEK-293 cells. Am J Physiol Cell Physiol 2004 287 : C1709 C1716.
69. 2+ current impairs agonist-dependent vasorelaxation in TRP4-/- mice. Nat Cell Biol 2001 3 : 121 127.
70. Groschner K, et al. Trp proteins form store-operated cation channels in human vascular endothelial cells. FEBS Lett 1998 437 : 101 106.
71. Beech DJ. TRPC1: store-operated channel and more. Pflugers Arch 2005 451 : 53 60.
72. 2+ entry. Role in signaling increased endothelial permeability. J Biol Chem 2003 278 : 33492 33500.
73. 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 1299.
74. Zeng W, et al. STIM1 gates TRPC channels, but not Orai1, by electrostatic interaction. Mol Cell 2008 32 : 439 448.
75. Yuan JP, Zeng W, Huang GN, Worley PF, Muallem S. STIM1 heteromultimerizes TRPC channels to determine their function as store-operated channels. Nat Cell Biol 2007 9 : 636 645.
76. Huang GN, et al. STIM1 carboxyl-terminus activates native SOC, Icrac and TRPC1 channels. Nat Cell Biol 2006 8 : 1003 1010.
77. Liao Y, et al. Functional interactions among Orai1, TRPCs, and STIM1 suggest a STIM-regulated heteromeric Orai/TRPC model for SOCE/Icrac channels. Proc Natl Acad Sci USA 2008 105 : 2895 2900.
78. Cheng KT, Liu X, Ong HL, Ambudkar IS. Functional requirement for Orai1 in store-operated TRPC1-STIM1 channels. J Biol Chem 2008 283 : 12935 12940.
79. Jardin I, Salido GM, Rosado JA. Role of lipid rafts in the interaction between hTRPC1, Orai1 and STIM1. Channels (Austin) 2008 2 : 401 403.
80. Ong HL, et al. Dynamic assembly of TRPC1/STIM1/Orai1 ternary complex is involved in store operated calcium influx: evidence for similarities in SOC and CRAC channel components. J Biol Chem 2007 282 : 9105 9116.
81. 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 4497.
82. Oritani K, Kincade PW. Identification of stromal cell products that interact with pre-B cells. J Cell Biol 1996 134 : 771 782.
83. Dziadek MA, Johnstone LS. Biochemical properties and cellular localisation of STIM proteins. Cell Calcium 2007 42 : 123 132.
84. 2+ channel function. J Cell Biol 2005 169 : 435 445.
85. 2+ influx. Curr Biol 2005 15 : 1235 1241.
86. 2+ entry. Curr Biol 2006 16 : 1465 1470.
87. Lewis RS. The molecular choreography of a store-operated calcium channel. Nature 2007 446 : 284 287.
88. Cahalan MD, Zhang SL, Yeromin AV, Ohlsen K, Roos J, Stauderman KA. Molecular basis of the CRAC channel. Cell Calcium 2007 42 : 133 144.
89. 2+ entry. J Cell Sci 2007 120 : 1959 1965.
90. Feske S, et al. A mutation in Orai1 causes immune deficiency by abrogating CRAC channel function. Nature 2006 441 : 179 185.
91. Gwack Y, et al. Biochemical and functional characterization of Orai proteins. J Biol Chem 2007 282 : 16232 16243.
92. 2+ channel activity. Proc Natl Acad Sci USA 2006 103 : 9357 9362.
93. Peinelt C, et al. Amplification of CRAC current by STIM1 and CRACM1 (Orai1). Nat Cell Biol 2006 8 : 771 773.
94. 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 20665.
95. Mercer JC, et al. Large store-operated calcium-selected currents due to co-expression of orai1 or orai2 with the intracellular calcium sensor, stim1. J Biol Chem 2006 281 : 24979 24990.
96. 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 : 230 233.
97. 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 : 226 229.
98. Vig M, et al. CRACM1 multimers form the ion-selective pore of the CRAC channel. Curr Biol 2006 16 : 2073 2079.
99. Mignen O, Thompson JL, Shuttleworth TJ. Orai1 subunit stoichiometry of the mammalian CRAC channel pore. J Physiol 2008 586 : 419 425.
100. Penna A, et al. The CRAC channel consists of a tetramer formed by Stim-induced dimerization of Orai dimers. Nature 2008 456 : 116 120.
101. 2+ store to the plasma membrane. Nature 2005 437 : 902 905.
102. Wu MM, Buchanan J, Luik RM, Lewis RS. Ca2+ store depletion causes STIM1 to accumulate in ER regions closely associated with the plasma membrane. J Cell Biol 2006 174 : 803 813.
103. Xu P, Lu J, Li Z, Yu X, Chen L, Xu T. Aggregation of STIM1 underneath the plasma membrane induces clustering of Orai1. Biochem Biophys Res Commun 2006 350 : 969 976.
104. 2+ -dye label reveals STIM1 surface exposure. Proc Natl Acad Sci USA 2007 104 : 3693 3697.
105. Baba Y, et al. Coupling of STIM1 to store-operated Ca2+ entry through its constitutive and inducible movement in the endoplasmic reticulum. Proc Nat Acad Sci USA 2006 103 : 16704 16709.
106. Oh-Hora M, et al. Dual functions for the endoplasmic reticulum calcium sensors STIM1 and STIM2 in T cell activation and tolerance. Nature Immunol 2008 9 : 432 443.
107. 2+-selective (ARC) channels without store depletion or translocation to the plasma membrane. J Physiol (Lond) 2007 579 : 703 715.
108. 2+ channel activator STIM1. J Cell Sci 2007 120 : 3762 3771.
109. Grigoriev I, et al. STIM1 is a MT-plus-end-tracking protein involved in remodeling of the ER. Curr Biol 2008 18 : 177 182.
110. 2+ store depletion. Proc Natl Acad Sci USA 2007 104 : 9301 9306.
111. 2+ -store-dependent and -independent reversal of Stim1 localization and function. J Cell Sci 2008 121 : 762 772.
112. Barr VA, et al. Dynamic movement of the calcium sensor STIM1 and the calcium channel Orai1 in activated T-cells: punctae and distal caps. Mol Biol Cell 2008 19 : 2802 2817.
113. Navarro-Borelly L, Somasundaram A, Yamashita M, Ren D, Miller RJ, Prakriya M. STIM1-Orai1 interactions and Orai1 conformational changes revealed by live-cell FRET microscopy. J Physiol (Lond) 2008 586 : 5383 5401.
114. 2+ stores and on electrostatic interactions. Mol Biol Cell 2009 20 : 389 399.
115. Muik M, et al. Dynamic coupling of the putative coiled-coil domain of ORAI1 with STIM1 mediates ORAI1 channel activation. J Biol Chem 2008 283 : 8014 8022.
116. 2+ channel activity of human orai1 and orai3. J Biol Chem 2008 283 : 17662 17671.
117. Muik M, et al. A cytosolic homomerization and a modulatory domain within STIM1 C-terminus determine coupling to ORAI1 channels. J Biol Chem 2009 284 : 8421 8426.
118. Yuan JP, Zeng W, Dorwart MR, Choi YJ, Worley PF, Muallem S. SOAR and the polybasic STIM1 domains gate and regulate Orai channels. Nat Cell Biol 2009 11 : 337 343.
119. Park CY, et al. STIM1 clusters and activates CRAC channels via direct binding of a cytosolic domain to Orai1. Cell 2009 136 : 876 890.
120. Csutora P, et al. Novel role for STIM1 as a trigger for calcium influx factor production. J Biol Chem 2008 283 : 14524 14531.
121. Putney JW. Pharmacology of capacitative calcium entry. Mol Intervent 2001 1 : 84 94.
122. 2+ channels and T-lymphocyte activation by the pyrazole derivative BTP2. J Biol Chem 2004 279 : 12427 12437.
123. 2+ influx and cytokine production by facilitating transient receptor potential melastatin 4 channel activity. Mol Pharmacol 2006 69 : 1413 1420.
124. Merritt JE, et al. SK&F 96365, a novel inhibitor of receptor-mediated calcium entry. Biochem J 1990 271 : 515 522.
125. 2+ -entry pathways regulated by vasopressin. Biochem J 2003 370 : 439 448.
126. 2+ current Icrac in RBL-1 cells. J Physiol (Lond) 2001 532 : 55 71.
127. Saitoh M, Ishikawa T, Matsushima S, Naka M, Hidaka H. Selective inhibition of catalytic activity of smooth muscle myosin light chain kinase. J Biol Chem 1987 262 : 7796 7801.
128. Tran QK, et al. Myosin light chain kinase regulates capacitative Ca(2+) entry in human monocytes/macrophages. Arterioscler Thromb Vasc Biol 2001 21 : 509 515.
129. 2+ release. J Biochem 1997 122 : 498 505.
130. 2+ channels. Science 2000 287 : 1647 1651.
131. Braun F-J, Broad LM, Armstrong DL, Putney JW. Stable activation of single CRAC-channels in divalent cation-free solutions. J Biol Chem 2001 276 : 1063 1070.
132. 2+ channels by 2-aminoethyldiphenyl borate (2-APB) occurs independently of IP3 receptors. J Physiol (Lond) 2001 536 : 3 19.
133. 2+ entry channels. J Biol Chem 2001 276 : 18888 18896.
134. Iwasaki H, Mori Y, Hara Y, Uchida K, Zhou H, Mikoshiba K. 2-Aminoethoxydiphenyl borate (2-APB) inhibits capacitative calcium entry independently of the function of inositol 1,4,5-trisphosphate receptors. Recept Channels 2001 7 : 429 439.
135. DeHaven WI, Smyth JT, Boyles RR, Bird GS, Putney JW Jr. Complex actions of 2-aminoethyldiphenyl borate on store-operated calcium entry. J Biol Chem 2008 283 : 19265 19273.
136. Peinelt C, Lis A, Beck A, Fleig A, Penner R. 2-APB directly facilitates and indirectly inhibits STIM1-dependent gating of CRAC channels. J Physiol 2008 586 : 3061 3073.
137. Schindl R, et al. 2-Aminoethoxydiphenyl borate alters selectivity of Orai3 channels by increasing their pore size. J Biol Chem 2008 283 : 20261 20267.
138. Putney JW. Capacitative calcium entry revisited. Cell Calcium 1990 11 : 611 624.
139. Meldolesi J. Keeping the stores full. Current Biol 1993 3 : 910 912.
140. Le Deist F, et al. A primary T-cell immunodeficiency associated with defective transmembrane calcium influx. Blood 1995 85 : 1053 1062.
141. Picard C, et al. STIM1 Mutation Associated with a Syndrome of Immunodeficiency and Autoimmunity. N Engl J Med 2009 360 : 1971 1980.
142. 2+ channel activation and altered K+ channel gating in T cells from immunodeficient patients. J Exp Med 2005 202 : 651 662.
143. Vig M, 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.
144. Stiber J, et al. STIM1 signalling controls store-operated calcium entry required for development and contractile function in skeletal muscle. Nat Cell Biol 2008 10 : 688 697.
145. Gwack Y, et al. Hair loss and defective T- and B-cell function in mice lacking ORAI1. Mol Cell Biol 2008 28 : 5209 5222.
146. Berridge MJ, Galione A. Cytosolic calcium oscillators. FASEB J 1988 2 : 3074 3082.
147. i oscillations? Challenging the capacitative model Cell Calcium 1999 25 : 237 246.
148. 2+ entry channel. J Biol Chem 2000 275 : 9114 9119.
149. i oscillations in HEK293 cells. J Biol Chem 2001 276 : 5613 5621.
150. Bird GS, Putney JW. Capacitative calcium entry supports calcium oscillations in human embryonic kidney cells. J Physiol 2005 562 : 697 706.
151. Sneyd J, Tsaneva-Atanasova K, Yule DI, Thompson JL, Shuttleworth TJ. Control of calcium oscillations by membrane fluxes. Proc Natl Acad Sci USA 2004 101 : 1392 1396.
152. Wedel B, Boyles RR, Putney JW, Bird GS. 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 579 : 679 689.
153. 2+-selective (ARC) channels. J Physiol (Lond) 2008 586 : 185 195.
154. Brandman O, Liou J, Park WS, Meyer T. STIM2 is a feedback regulator that stabilizes basal cytosolic and endoplasmic reticulum Ca(2+) levels. Cell 2007 131 : 1327 1339.
155. Ribeiro CMP, Putney JW. Differential effects of protein kinase C activation on calcium storage and capacitative calcium entry in NIH 3T3 cells. J Biol Chem 1996 271 : 21522 21528.
156. 2+ inflow in rat hepatocytes. Biochem J 1999 341 : 401 408.
157. 2+ current in rat basophilic leukemia cells. J Physiol (Lond) 2000 522 : 247 257.
158. Turner H, Fleig A, Stokes A, Kinet JP, Penner R. Discrimination of intracellular calcium store subcompartments using TRPV1 (transient receptor potential channel, vanilloid subfamily member 1) release channel activity. Biochem J 2003 371 : 341 350.
159. Meyer T, Hanson PI, Stryer L, Schulman H. Calmodulin trapping by calcium-calmodulin-dependent protein kinase. Science 1992 256 : 1199 1202.
160. Dolmetsch RE, Xu KL, Lewis RS. Calcium oscillations increase the efficiency and specificity of gene expression. Nature 1998 392 : 933 936.
161. 2+ release: an intimate connection. Trends Biochem Sci 2000 25 : 215 221.
162. Lin X, et al. Control of calcium signal propagation to the mitochondria by inositol 1,4,5-trisphosphate-binding proteins. J Biol Chem 2005 280 : 12820 12832.
163. Hoth M, Fanger CM, Lewis RS. Mitochondrial regulation of store-operated calcium signaling in T lymphocytes. J Cell Biol 1997 137 : 633 648.
164. 2+ uptake. EMBO J 2002 21 : 6744 6754.
165. 2+ entry in HeLa cells. Cell Calcium 2004 36 : 499 508.
166. 2+ -sensitive adenylyl cyclases. Biochem J 1994 297 : 437 440.
167. 2+ -stimulable adenylyl cyclases with capacitative calcium entry sites. J Biol Chem 1996 271 : 12438 12444.
168. 2+ (CRAC) channels stimulates production of an intracellular messenger and an intercellular pro-inflammatory signal. J Biol Chem 2008 283 : 4622 4631.
169. 2+ channels. J Biol Chem 2008 283 : 31348 31355.
170. 2+ channels: impact on cell function. J Physiol 2008 586 : 3043 3054.
171. Lefkimmiatis K, Srikanthan M, Maiellaro I, Moyer MP, Curci S, Hofer AM. Store-operated cyclic AMP signaling mediated by STIM1. Nat Cell Biol 2009 11 : 433 442.