Calmodulin and STIM proteins: Two major calcium sensors in the cytoplasm and endoplasmic reticulum in memory of Professor Koichi Yagi, Hokkaido University.

Biochemical and Biophysical Research Communications

Volumn 460, Issue 1, 2015, Pages 5-21

  Marshall, Christopher B ^a   Nishikawa, Tadateru ^a   Osawa, Masanori ^b   Stathopulos, Peter B ^c   Ikura, Mitsuhiko ^a  

^a PRINCESS MARGARET HOSPITAL   (Canada)

^b UNIVERSITY OF TOKYO   (Japan)

^c WESTERN UNIVERSITY   (Canada)

Author keywords

Atomic resolution structure; Calcium sensing; Calmodulin; Calmodulin target interactions; EF hand; Stromal interaction molecules (STIM)

Indexed keywords

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE; CALCIUM ION; CALMODULIN; PHOSPHATASE; STROMAL INTERACTION MOLECULE 1; STROMAL INTERACTION MOLECULE 2; CALCIUM; CELL ADHESION MOLECULE; MEMBRANE PROTEIN; STIM1 PROTEIN, HUMAN; STIM2 PROTEIN, HUMAN; TUMOR PROTEIN;

CYTOPLASM; DISEASE ASSOCIATION; DNA SEQUENCE; ENDOPLASMIC RETICULUM; ENZYME ACTIVE SITE; HUMAN; MOLECULAR EVOLUTION; NEOPLASM; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN TARGETING; REVIEW; SIGNAL TRANSDUCTION; ANIMAL; BIOLOGICAL MODEL; CALCIUM SIGNALING; GENETICS; HEART ARRHYTHMIA; METABOLISM; PHYSIOLOGY;

EUKARYOTA;

ANIMALS; ARRHYTHMIAS, CARDIAC; CALCIUM; CALCIUM SIGNALING; CALMODULIN; CELL ADHESION MOLECULES; CYTOPLASM; ENDOPLASMIC RETICULUM; HUMANS; MEMBRANE PROTEINS; MODELS, BIOLOGICAL; NEOPLASM PROTEINS;

EID: 84929298570     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2015.01.106     Document Type: Review

References (219)

1. W.Y. Cheung Cyclic 3′,5′-nucleotide phosphodiesterase. Demonstration of an activator Biochem. Biophys. Res. Commun. 38 1970 533 538
2. S. Kakiuchi, and R. Yamazaki Calcium dependent phosphodiesterase activity and its activating factor (PAF) from brain studies on cyclic 3′,5′-nucleotide phosphodiesterase (3) Biochem. Biophys. Res. Commun. 41 1970 1104 1110
3. C.O. Brostrom, Y.C. Huang, B.M. Breckenridge, and D.J. Wolff Identification of a calcium-binding protein as a calcium-dependent regulator of brain adenylate cyclase Proc. Natl. Acad. Sci. U. S. A. 72 1975 64 68
4. R.M. Gopinath, and F.F. Vincenzi Phosphodiesterase protein activator mimics red blood cell cytoplasmic activator of (Ca2+-Mg2+)ATPase Biochem. Biophys. Res. Commun. 77 1977 1203 1209
5. H.W. Jarrett, and J.T. Penniston Partial purification of the Ca2+-Mg2+ ATPase activator from human erythrocytes: its similarity to the activator of 3′:5′ - cyclic nucleotide phosphodiesterase Biochem. Biophys. Res. Commun. 77 1977 1210 1216
6. M. Yazawa, and K. Yagi Calcium-binding subunit of myosin light chain kinase J. Biochem. 82 1977 287 289
7. E. Carafoli, and C.B. Klee Calcium as a Cellular Regulator 1999 Oxford University Press New York
8. H. Hidaka, and D.J. Hartshorne Calmodulin Antagonists and Cellular Physiology 1985 Academic Press Orlando
9. H. Tidow, and P. Nissen Structural diversity of calmodulin binding to its target sites FEBS J. 280 2013 5551 5565
10. K.P. Hoeflich, and M. Ikura Calmodulin in action: diversity in target recognition and activation mechanisms Cell 108 2002 739 742
11. R.R. Copley, J. Schultz, C.P. Ponting, and P. Bork Protein families in multicellular organisms Curr. Opin. Struct. Biol. 9 1999 408 415
12. M. Ikura, and J.B. Ames Genetic polymorphism and protein conformational plasticity in the calmodulin superfamily: two ways to promote multifunctionality Proc. Natl. Acad. Sci. U. S. A. 103 2006 1159 1164
13. R.H. Kretsinger, V.N. Uversky, and E.A. Permyakov Encyclopedia of Metalloproteins 2013 Springer New York
14. L.J. Van Eldik, and D.M. Watterson Calmodulin and Signal Transduction 1998 Academic Press San Diego
15. K.L. Yap, J. Kim, K. Truong, M. Sherman, T. Yuan, and M. Ikura Calmodulin target database J. Struct. Funct. Genomics 1 2000 8 14
16. J.B. Ames, and S. Lim Molecular structure and target recognition of neuronal calcium sensor proteins Biochim. Biophys. Acta 1820 2012 1205 1213
17. S. Bhattacharya, C.G. Bunick, and W.J. Chazin Target selectivity in EF-hand calcium binding proteins Biochim. Biophys. Acta 1742 2004 69 79
18. J.L. Gifford, M.P. Walsh, and H.J. Vogel Structures and metal-ion-binding properties of the Ca2+-binding helix-loop-helix EF-hand motifs Biochem. J. 405 2007 199 221
19. Z. Grabarek Insights into modulation of calcium signaling by magnesium in calmodulin, troponin C and related EF-hand proteins Biochim. Biophys. Acta 1813 2011 913 921
20. A. Hermann, R. Donato, T.M. Weiger, and W.J. Chazin S100 calcium binding proteins and ion channels Front. Pharmacol. 3 2012 67
21. B. Schwaller Cytosolic Ca2+ buffers Cold Spring Harb. Perspect. Biol. 2 2010 a004051
22. J.W. Putney Jr. A model for receptor-regulated calcium entry Cell Calcium 7 1986 1 12
23. H.E. Collins, X. Zhu-Mauldin, R.B. Marchase, and J.C. Chatham STIM1/Orai1-mediated SOCE: current perspectives and potential roles in cardiac function and pathology Am. J. Physiol. Heart Circ. Physiol. 305 2013 H446 H458
24. S. Feske, E.Y. Skolnik, and M. Prakriya Ion channels and transporters in lymphocyte function and immunity Nat. Rev. Immunol. 12 2012 532 547
25. J. Gruszczynska-Biegala, and J. Kuznicki Native STIM2 and ORAI1 proteins form a calcium-sensitive and thapsigargin-insensitive complex in cortical neurons J. Neurochem. 126 2013 727 738
26. R. Hooper, B.S. Rothberg, and J. Soboloff Neuronal STIMulation at rest Sci. Signal. 7 2014 pe18
27. P.J. Shaw, and S. Feske Physiological and pathophysiological functions of SOCE in the immune system Front. Biosci. (Elite Ed) 4 2012 2253 2268
28. 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 2005 1235 1241
29. 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 2005 435 445 Epub 2005 May 2002
30. Y.S. Babu, C.E. Bugg, and W.J. Cook Structure of calmodulin refined at 2.2 A resolution J. Mol. Biol. 204 1988 191 204
31. O. Herzberg, and M.N. James Structure of the calcium regulatory muscle protein troponin-C at 2.8 A resolution Nature 313 1985 653 659
32. R.H. Kretsinger, and C.E. Nockolds Carp muscle calcium-binding protein. II. Structure determination and general description J. Biol. Chem. 248 1973 3313 3326
33. P.B. Stathopulos, L. Zheng, G.Y. Li, M.J. Plevin, and M. Ikura Structural and mechanistic insights into STIM1-mediated initiation of store-operated calcium entry Cell 135 2008 110 122
34. Y.S. Babu, J.S. Sack, T.J. Greenhough, C.E. Bugg, A.R. Means, and W.J. Cook Three-dimensional structure of calmodulin Nature 315 1985 37 40
35. M.J. Berridge, P. Lipp, and M.D. Bootman The versatility and universality of calcium signalling Nat. Rev. Mol. Cell Biol. 1 2000 11 21
36. M.D. Bootman, O.H. Petersen, and A. Verkhratsky The endoplasmic reticulum is a focal point for co-ordination of cellular activity Cell Calcium 32 2002 231 234
37. S. Linse, A. Helmersson, and S. Forsen Calcium binding to calmodulin and its globular domains J. Biol. Chem. 266 1991 8050 8054
38. P.M. Bayley, W.A. Findlay, and S.R. Martin Target recognition by calmodulin: dissecting the kinetics and affinity of interaction using short peptide sequences Protein Sci. 5 1996 1215 1228
39. G. Barbato, M. Ikura, L.E. Kay, R.W. Pastor, and A. Bax Backbone dynamics of calmodulin studied by 15N relaxation using inverse detected two-dimensional NMR spectroscopy: the central helix is flexible Biochemistry 31 1992 5269 5278
40. M. Ikura, L.E. Kay, and A. Bax A novel approach for sequential assignment of 1H, 13C, and 15N spectra of proteins: heteronuclear triple-resonance three-dimensional NMR spectroscopy. Application to calmodulin Biochemistry 29 1990 4659 4667
41. M. Ikura, L.E. Kay, M. Krinks, and A. Bax Triple-resonance multidimensional NMR study of calmodulin complexed with the binding domain of skeletal muscle myosin light-chain kinase: indication of a conformational change in the central helix Biochemistry 30 1991 5498 5504
42. B.E. Finn, J. Evenas, T. Drakenberg, J.P. Waltho, E. Thulin, and S. Forsen Calcium-induced structural changes and domain autonomy in calmodulin Nat. Struct. Biol. 2 1995 777 783
43. H. Kuboniwa, N. Tjandra, S. Grzesiek, H. Ren, C.B. Klee, and A. Bax Solution structure of calcium-free calmodulin Nat. Struct. Biol. 2 1995 768 776
44. M. Zhang, T. Tanaka, and M. Ikura Calcium-induced conformational transition revealed by the solution structure of apo calmodulin Nat. Struct. Biol. 2 1995 758 767
45. H.J. Vogel, and M. Zhang Protein engineering and NMR studies of calmodulin Mol. Cell. Biochem. 149-150 1995 3 15
46. A. Villarroel, M. Taglialatela, G. Bernardo-Seisdedos, A. Alaimo, J. Agirre, A. Alberdi, C. Gomis-Perez, M.V. Soldovieri, P. Ambrosino, C. Malo, and P. Areso The ever changing moods of calmodulin: how structural plasticity entails transductional adaptability J. Mol. Biol. 426 2014 2717 2735
47. R. Buratti, G. Prestipino, P. Menegazzi, S. Treves, and F. Zorzato Calcium dependent activation of skeletal muscle Ca2+ release channel (ryanodine receptor) by calmodulin Biochem. Biophys. Res. Commun. 213 1995 1082 1090
48. O. Fuentes, C. Valdivia, D. Vaughan, R. Coronado, and H.H. Valdivia Calcium-dependent block of ryanodine receptor channel of swine skeletal muscle by direct binding of calmodulin Cell Calcium 15 1994 305 316
49. T. Ikemoto, M. Iino, and M. Endo Enhancing effect of calmodulin on Ca(2+)-induced Ca2+ release in the sarcoplasmic reticulum of rabbit skeletal muscle fibres J. Physiol. 487 Pt. 3 1995 573 582
50. A. Tripathy, L. Xu, G. Mann, and G. Meissner Calmodulin activation and inhibition of skeletal muscle Ca2+ release channel (ryanodine receptor) Biophys. J. 69 1995 106 119
51. K. Lau, M.M. Chan, and F. Van Petegem Lobe-specific calmodulin binding to different ryanodine receptor isoforms Biochemistry 53 2014 932 946
52. C.E. Adkins, S.A. Morris, H. De Smedt, I. Sienaert, K. Torok, and C.W. Taylor Ca2+-calmodulin inhibits Ca2+ release mediated by type-1, -2 and -3 inositol trisphosphate receptors Biochem. J. 345 Pt. 2 2000 357 363
53. T. Michikawa, J. Hirota, S. Kawano, M. Hiraoka, M. Yamada, T. Furuichi, and K. Mikoshiba Calmodulin mediates calcium-dependent inactivation of the cerebellar type 1 inositol 1,4,5-trisphosphate receptor Neuron 23 1999 799 808
54. L. Missiaen, H. DeSmedt, G. Bultynck, S. Vanlingen, P. Desmet, G. Callewaert, and J.B. Parys Calmodulin increases the sensitivity of type 3 inositol-1,4, 5-trisphosphate receptors to Ca(2+) inhibition in human bronchial mucosal cells Mol. Pharmacol. 57 2000 564 567
55. T.J. Cardy, and C.W. Taylor A novel role for calmodulin: Ca2+-independent inhibition of type-1 inositol trisphosphate receptors Biochem. J. 334 Pt. 2 1998 447 455
56. S. Patel, S.A. Morris, C.E. Adkins, G. O'Beirne, and C.W. Taylor Ca2+-independent inhibition of inositol trisphosphate receptors by calmodulin: redistribution of calmodulin as a possible means of regulating Ca2+ mobilization Proc. Natl. Acad. Sci. U. S. A. 94 1997 11627 11632
57. S. Kang, H. Kwon, H. Wen, Y. Song, D. Frueh, H.C. Ahn, S.H. Yoo, G. Wagner, and S. Park Global dynamic conformational changes in the suppressor domain of IP3 receptor by stepwise binding of the two lobes of calmodulin FASEB J. 25 2011 840 850
58. B. Elshorst, M. Hennig, H. Forsterling, A. Diener, M. Maurer, P. Schulte, H. Schwalbe, C. Griesinger, J. Krebs, H. Schmid, T. Vorherr, and E. Carafoli NMR solution structure of a complex of calmodulin with a binding peptide of the Ca2+ pump Biochemistry 38 1999 12320 12332
59. D. Guerini, J. Krebs, and E. Carafoli Stimulation of the purified erythrocyte Ca2+-ATPase by tryptic fragments of calmodulin J. Biol. Chem. 259 1984 15172 15177
60. M. Kataoka, J.F. Head, T. Vorherr, J. Krebs, and E. Carafoli Small-angle X-ray scattering study of calmodulin bound to two peptides corresponding to parts of the calmodulin-binding domain of the plasma membrane Ca2+ pump Biochemistry 30 1991 6247 6251
61. A.R. Penheiter, A.G. Filoteo, J.T. Penniston, and A.J. Caride Kinetic analysis of the calmodulin-binding region of the plasma membrane calcium pump isoform 4b Biochemistry 44 2005 2009 2020
62. A.K. Verma, A.G. Filoteo, D.R. Stanford, E.D. Wieben, J.T. Penniston, E.E. Strehler, R. Fischer, R. Heim, G. Vogel, and S. Mathews Complete primary structure of a human plasma membrane Ca2+ pump J. Biol. Chem. 263 1988 14152 14159
63. N. Juranic, E. Atanasova, A.G. Filoteo, S. Macura, F.G. Prendergast, J.T. Penniston, and E.E. Strehler Calmodulin wraps around its binding domain in the plasma membrane Ca2+ pump anchored by a novel 18-1 motif J. Biol. Chem. 285 2010 4015 4024
64. M.G. Erickson, H. Liang, M.X. Mori, and D.T. Yue FRET two-hybrid mapping reveals function and location of L-type Ca2+ channel CaM preassociation Neuron 39 2003 97 107
65. A.P. Yamniuk, and H.J. Vogel Calmodulin's flexibility allows for promiscuity in its interactions with target proteins and peptides Mol. Biotechnol. 27 2004 33 57
66. M. Ikura, G.M. Clore, A.M. Gronenborn, G. Zhu, C.B. Klee, and A. Bax Solution structure of a calmodulin-target peptide complex by multidimensional NMR Science 256 1992 632 638
67. W.E. Meador, A.R. Means, and F.A. Quiocho Target enzyme recognition by calmodulin: 2.4 A structure of a calmodulin-peptide complex Science 257 1992 1251 1255
68. A.R. Rhoads, and F. Friedberg Sequence motifs for calmodulin recognition FASEB J. 11 1997 331 340
69. W.E. Meador, A.R. Means, and F.A. Quiocho Modulation of calmodulin plasticity in molecular recognition on the basis of x-ray structures Science 262 1993 1718 1721
70. M. Osawa, H. Tokumitsu, M.B. Swindells, H. Kurihara, M. Orita, T. Shibanuma, T. Furuya, and M. Ikura A novel target recognition revealed by calmodulin in complex with Ca2+-calmodulin-dependent kinase kinase Nat. Struct. Biol. 6 1999 819 824
71. E. Franco-Echevarria, J.I. Banos-Sanz, B. Monterroso, A. Round, J. Sanz-Aparicio, and B. Gonzalez A new calmodulin-binding motif for inositol 1,4,5-trisphosphate 3-kinase regulation Biochem. J. 463 2014 319 328
72. A.A. Maximciuc, J.A. Putkey, Y. Shamoo, and K.R. Mackenzie Complex of calmodulin with a ryanodine receptor target reveals a novel, flexible binding mode Structure 14 2006 1547 1556
73. H. Ishida, and H.J. Vogel The solution structure of a plant calmodulin and the CaM-binding domain of the vacuolar calcium-ATPase BCA1 reveals a new binding and activation mechanism J. Biol. Chem. 285 2010 38502 38510
74. H. Tidow, L.R. Poulsen, A. Andreeva, M. Knudsen, K.L. Hein, C. Wiuf, M.G. Palmgren, and P. Nissen A bimodular mechanism of calcium control in eukaryotes Nature 491 2012 468 472
75. E. Yamauchi, T. Nakatsu, M. Matsubara, H. Kato, and H. Taniguchi Crystal structure of a MARCKS peptide containing the calmodulin-binding domain in complex with Ca2+-calmodulin Nat. Struct. Biol. 10 2003 226 231
76. K.L. Yap, T. Yuan, T.K. Mal, H.J. Vogel, and M. Ikura Structural basis for simultaneous binding of two carboxy-terminal peptides of plant glutamate decarboxylase to calmodulin J. Mol. Biol. 328 2003 193 204
77. Q. Ye, X. Li, A. Wong, Q. Wei, and Z. Jia Structure of calmodulin bound to a calcineurin peptide: a new way of making an old binding mode Biochemistry 45 2006 738 745
78. V. Majava, and P. Kursula Domain swapping and different oligomeric states for the complex between calmodulin and the calmodulin-binding domain of calcineurin a PLoS One 4 2009 e5402
79. T.B. Dunlap, H.F. Guo, E.C. Cook, E. Holbrook, J. Rumi-Masante, T.E. Lester, C.L. Colbert, C.W. Vander Kooi, and T.P. Creamer Stoichiometry of the calcineurin regulatory domain-calmodulin complex Biochemistry 53 2014 5779 5790
80. E.M. Espreafico, R.E. Cheney, M. Matteoli, A.A. Nascimento, P.V. De Camilli, R.E. Larson, and M.S. Mooseker Primary structure and cellular localization of chicken brain myosin-V (p190), an unconventional myosin with calmodulin light chains J. Cell Biol. 119 1992 1541 1557
81. J. Ruan, Q. Xie, N. Hutchinson, H. Cho, G.C. Wolfe, and C. Nathan Inducible nitric oxide synthase requires both the canonical calmodulin-binding domain and additional sequences in order to bind calmodulin and produce nitric oxide in the absence of free Ca2+ J. Biol. Chem. 271 1996 22679 22686
82. T. Yuan, M.P. Walsh, C. Sutherland, H. Fabian, and H.J. Vogel Calcium-dependent and -independent interactions of the calmodulin-binding domain of cyclic nucleotide phosphodiesterase with calmodulin Biochemistry 38 1999 1446 1455
83. M. Dasgupta, T. Honeycutt, and D.K. Blumenthal The gamma-subunit of skeletal muscle phosphorylase kinase contains two noncontiguous domains that act in concert to bind calmodulin J. Biol. Chem. 264 1989 17156 17163
84. J. Baudier, J.C. Deloulme, A. Van Dorsselaer, D. Black, and H.W. Matthes Purification and characterization of a brain-specific protein kinase C substrate, neurogranin (p17). Identification of a consensus amino acid sequence between neurogranin and neuromodulin (GAP43) that corresponds to the protein kinase C phosphorylation site and the calmodulin-binding domain J. Biol. Chem. 266 1991 229 237
85. S. Pathmanathan, E. Hamilton, E. Atcheson, and D.J. Timson The interaction of IQGAPs with calmodulin-like proteins Biochem. Soc. Trans. 39 2011 694 699
86. A. Houdusse, J.F. Gaucher, E. Krementsova, S. Mui, K.M. Trybus, and C. Cohen Crystal structure of apo-calmodulin bound to the first two IQ motifs of myosin V reveals essential recognition features Proc. Natl. Acad. Sci. U. S. A. 103 2006 19326 19331
87. M.D. Feldkamp, L. Yu, and M.A. Shea Structural and energetic determinants of apo calmodulin binding to the IQ motif of the Na(V)1.2 voltage-dependent sodium channel Structure 19 2011 733 747
88. B. Chagot, and W.J. Chazin Solution NMR structure of apo-calmodulin in complex with the IQ motif of human cardiac sodium channel NaV1.5 J. Mol. Biol. 406 2011 106 119
89. C. Wang, B.C. Chung, H. Yan, H.G. Wang, S.Y. Lee, and G.S. Pitt Structural analyses of Ca(2)(+)/CaM interaction with NaV channel C-termini reveal mechanisms of calcium-dependent regulation Nat. Commun. 5 2014 4896
90. F. Van Petegem, F.C. Chatelain, and D.L. Minor Jr. Insights into voltage-gated calcium channel regulation from the structure of the CaV1.2 IQ domain-Ca2+/calmodulin complex Nat. Struct. Mol. Biol. 12 2005 1108 1115
91. J.L. Fallon, D.B. Halling, S.L. Hamilton, and F.A. Quiocho Structure of calmodulin bound to the hydrophobic IQ domain of the cardiac Ca(v)1.2 calcium channel Structure 13 2005 1881 1886
92. E.Y. Kim, C.H. Rumpf, Y. Fujiwara, E.S. Cooley, F. Van Petegem, and D.L. Minor Jr. Structures of CaV2 Ca2+/CaM-IQ domain complexes reveal binding modes that underlie calcium-dependent inactivation and facilitation Structure 16 2008 1455 1467
93. V. Kumar, V.P. Chichili, L. Zhong, X. Tang, A. Velazquez-Campoy, F.S. Sheu, J. Seetharaman, N.Z. Gerges, and J. Sivaraman Structural basis for the interaction of unstructured neuron specific substrates neuromodulin and neurogranin with calmodulin Sci. Rep. 3 2013 1392
94. D. Chin, and A.R. Means Calmodulin: a prototypical calcium sensor Trends Cell Biol. 10 2000 322 328
95. G. Manning, D.B. Whyte, R. Martinez, T. Hunter, and S. Sudarsanam The protein kinase complement of the human genome Science 298 2002 1912 1934
96. J. Aramburu, A. Rao, and C.B. Klee Calcineurin: from structure to function Curr. Top. Cell. Regul. 36 2000 237 295
97. C.B. Klee, G.F. Draetta, and M.J. Hubbard Calcineurin Adv. Enzymol. Relat. Areas Mol. Biol. 61 1988 149 200
98. F. Rusnak, and P. Mertz Calcineurin: form and function Physiol. Rev. 80 2000 1483 1521
99. A. Crivici, and M. Ikura Molecular and structural basis of target recognition by calmodulin Annu. Rev. Biophys. Biomol. Struct. 24 1995 85 116
100. I. de Diego, J. Kuper, N. Bakalova, P. Kursula, and M. Wilmanns Molecular basis of the death-associated protein kinase-calcium/calmodulin regulator complex Sci. Signal. 3 2010 ra6
101. Y. Lai, A.C. Nairn, and P. Greengard Autophosphorylation reversibly regulates the Ca2+/calmodulin-dependence of Ca2+/calmodulin-dependent protein kinase II Proc. Natl. Acad. Sci. U. S. A. 83 1986 4253 4257
102. S.G. Miller, and M.B. Kennedy Regulation of brain type II Ca2+/calmodulin-dependent protein kinase by autophosphorylation: a Ca2+-triggered molecular switch Cell 44 1986 861 870
103. K. Shen, and T. Meyer Dynamic control of CaMKII translocation and localization in hippocampal neurons by NMDA receptor stimulation Science 284 1999 162 166
104. S.J. Coultrap, K. Barcomb, and K.U. Bayer A significant but rather mild contribution of T286 autophosphorylation to Ca2+/CaM-stimulated CaMKII activity PLoS One 7 2012 e37176
105. T. Meyer, P.I. Hanson, L. Stryer, and H. Schulman Calmodulin trapping by calcium-calmodulin dependent protein-kinase Science 256 1992 1199 1202
106. S.I. Singla, A. Hudmon, J.M. Goldberg, J.L. Smith, and H. Schulman Molecular characterization of calmodulin trapping by calcium/calmodulin-dependent protein kinase II J. Biol. Chem. 276 2001 29353 29360
107. M.M. Stratton, L.H. Chao, H. Schulman, and J. Kuriyan Structural studies on the regulation of Ca2+/calmodulin dependent protein kinase II Curr. Opin. Struct. Biol. 23 2013 292 301
108. L.H. Chao, M.M. Stratton, I.H. Lee, O.S. Rosenberg, J. Levitz, D.J. Mandell, T. Kortemme, J.T. Groves, H. Schulman, and J. Kuriyan A mechanism for tunable autoinhibition in the structure of a human Ca2+/calmodulin- dependent kinase II holoenzyme Cell 146 2011 732 745
109. O.S. Rosenberg, S. Deindl, R.J. Sung, A.C. Nairn, and J. Kuriyan Structure of the autoinhibited kinase domain of CaMKII and SAXS analysis of the holoenzyme Cell 123 2005 849 860
110. P. Rellos, A.C. Pike, F.H. Niesen, E. Salah, W.H. Lee, F. von Delft, and S. Knapp Structure of the CaMKIIdelta/calmodulin complex reveals the molecular mechanism of CaMKII kinase activation PLoS Biol. 8 2010 e1000426
111. R.J. Colbran, and T.R. Soderling Calcium/calmodulin-independent autophosphorylation sites of calcium/calmodulin-dependent protein kinase II. Studies on the effect of phosphorylation of threonine 305/306 and serine 314 on calmodulin binding using synthetic peptides J. Biol. Chem. 265 1990 11213 11219
112. Q. Huai, H.Y. Kim, Y.D. Liu, Y.D. Zhao, A. Mondragon, J.O. Liu, and H.M. Ke Crystal structure of calcineurin-cyclophilin-cyclosporin shows common but distinct recognition of immunophilin-drug complexes Proc. Natl. Acad. Sci. U. S. A. 99 2002 12037 12042
113. L. Jin, and S.C. Harrison Crystal structure of human calcineurin complexed with cyclosporin A and human cyclophilin Proc. Natl. Acad. Sci. U. S. A. 99 2002 13522 13526
114. P.M. Stemmer, and C.B. Klee Dual calcium-ion regulation of calcineurin by calmodulin and calcineurin-B Biochemistry 33 1994 6859 6866
115. C. Xia, I. Misra, T. Iyanagi, and J.J. Kim Regulation of interdomain interactions by calmodulin in inducible nitric-oxide synthase J. Biol. Chem. 284 2009 30708 30717
116. C.L. Drum, S.Z. Yan, J. Bard, Y.Q. Shen, D. Lu, S. Soelaiman, Z. Grabarek, A. Bohm, and W.J. Tang Structural basis for the activation of anthrax adenylyl cyclase exotoxin by calmodulin Nature 415 2002 396 402
117. M.A. Schumacher, A.F. Rivard, H.P. Bachinger, and J.P. Adelman Structure of the gating domain of a Ca2+-activated K+ channel complexed with Ca2+/calmodulin Nature 410 2001 1120 1124
118. M.A. Schumacher, M. Crum, and M.C. Miller Crystal structures of apocalmodulin and an apocalmodulin/SK potassium channel gating domain complex Structure 12 2004 849 860
119. M. Zhang, C. Abrams, L. Wang, A. Gizzi, L. He, R. Lin, Y. Chen, P.J. Loll, J.M. Pascal, and J.F. Zhang Structural basis for calmodulin as a dynamic calcium sensor Structure 20 2012 911 923
120. J.L. Fallon, M.R. Baker, L. Xiong, R.E. Loy, G. Yang, R.T. Dirksen, S.L. Hamilton, and F.A. Quiocho Crystal structure of dimeric cardiac L-type calcium channel regulatory domains bridged by Ca2+∗calmodulins Proc. Natl. Acad. Sci. U. S. A. 106 2009 5135 5140
121. E.Y. Kim, C.H. Rumpf, F. Van Petegem, R.J. Arant, F. Findeisen, E.S. Cooley, E.Y. Isacoff, and D.L. Minor Jr. Multiple C-terminal tail Ca(2+)/CaMs regulate Ca(V)1.2 function but do not mediate channel dimerization EMBO J. 29 2010 3924 3938
122. P.J. Adams, M. Ben-Johny, I.E. Dick, T. Inoue, and D.T. Yue Apocalmodulin itself promotes ion channel opening and ca(2+) regulation Cell 159 2014 608 622
123. M.W. Berchtold, R. Egli, J.A. Rhyner, H. Hameister, and E.E. Strehler Localization of the human bona fide calmodulin genes CALM1, CALM2, and CALM3 to chromosomes 14q24-q31, 2p21.1-p21.3, and 19q13.2-q13.3 Genomics 16 1993 461 465
124. M. Nyegaard, M.T. Overgaard, M.T. Sondergaard, M. Vranas, E.R. Behr, L.L. Hildebrandt, J. Lund, P.L. Hedley, A.J. Camm, G. Wettrell, I. Fosdal, M. Christiansen, and A.D. Borglum Mutations in calmodulin cause ventricular tachycardia and sudden cardiac death Am. J. Hum. Genet. 91 2012 703 712
125. S.G. Priori, C. Napolitano, N. Tiso, M. Memmi, G. Vignati, R. Bloise, V. Sorrentino, and G.A. Danieli Mutations in the cardiac ryanodine receptor gene (hRyR2) underlie catecholaminergic polymorphic ventricular tachycardia Circulation 103 2001 196 200
126. L. Crotti, C.N. Johnson, E. Graf, G.M. De Ferrari, B.F. Cuneo, M. Ovadia, J. Papagiannis, M.D. Feldkamp, S.G. Rathi, J.D. Kunic, M. Pedrazzini, T. Wieland, P. Lichtner, B.M. Beckmann, T. Clark, C. Shaffer, D.W. Benson, S. Kaab, T. Meitinger, T.M. Strom, W.J. Chazin, P.J. Schwartz, and A.L. George Jr. Calmodulin mutations associated with recurrent cardiac arrest in infants Circulation 127 2013 1009 1017
127. J.R. Giudicessi, and M.J. Ackerman Potassium-channel mutations and cardiac arrhythmias-diagnosis and therapy Nat. Rev. Cardiol. 9 2012 319 332
128. Y. Ruan, N. Liu, and S.G. Priori Sodium channel mutations and arrhythmias Nat. Rev. Cardiol. 6 2009 337 348
129. N. Makita, N. Yagihara, L. Crotti, C.N. Johnson, B.M. Beckmann, M.S. Roh, D. Shigemizu, P. Lichtner, T. Ishikawa, T. Aiba, T. Homfray, E.R. Behr, D. Klug, I. Denjoy, E. Mastantuono, D. Theisen, T. Tsunoda, W. Satake, T. Toda, H. Nakagawa, Y. Tsuji, T. Tsuchiya, H. Yamamoto, Y. Miyamoto, N. Endo, A. Kimura, K. Ozaki, H. Motomura, K. Suda, T. Tanaka, P.J. Schwartz, T. Meitinger, S. Kaab, P. Guicheney, W. Shimizu, Z.A. Bhuiyan, H. Watanabe, W.J. Chazin, and A.L. George Jr. Novel calmodulin mutations associated with congenital arrhythmia susceptibility Circ. Cardiovasc. Genet. 7 2014 466 474
130. G.J. Reed, N.J. Boczek, S.P. Etheridge, and M.J. Ackerman CALM3 mutation associated with long QT syndrome Heart Rhythm 12 2015 419 422
131. H.S. Hwang, F.R. Nitu, Y. Yang, K. Walweel, L. Pereira, C.N. Johnson, M. Faggioni, W.J. Chazin, D. Laver, A.L. George Jr., R.L. Cornea, D.M. Bers, and B.C. Knollmann Divergent regulation of ryanodine receptor 2 calcium release channels by arrhythmogenic human calmodulin missense mutants Circ. Res. 114 2014 1114 1124
132. R.F. Marsman, J. Barc, L. Beekman, M. Alders, D. Dooijes, A. van den Wijngaard, I. Ratbi, A. Sefiani, Z.A. Bhuiyan, A.A. Wilde, and C.R. Bezzina A mutation in CALM1 encoding calmodulin in familial idiopathic ventricular fibrillation in childhood and adolescence J. Am. Coll. Cardiol. 63 2014 259 266
133. H. Okano, M.S. Cyert, and Y. Ohya Importance of phenylalanine residues of yeast calmodulin for target binding and activation J. Biol. Chem. 273 1998 26375 26382
134. A.B. Sorensen, M.T. Sondergaard, and M.T. Overgaard Calmodulin in a heartbeat FEBS J. 280 2013 5511 5532
135. N. Chopra, and B.C. Knollmann Genetics of sudden cardiac death syndromes Curr. Opin. Cardiol. 26 2011 196 203
136. X. Xu, M. Yano, H. Uchinoumi, A. Hino, T. Suetomi, M. Ono, H. Tateishi, T. Oda, S. Okuda, M. Doi, S. Kobayashi, T. Yamamoto, Y. Ikeda, N. Ikemoto, and M. Matsuzaki Defective calmodulin binding to the cardiac ryanodine receptor plays a key role in CPVT-associated channel dysfunction Biochem. Biophys. Res. Commun. 394 2010 660 666
137. M. Samso, and T. Wagenknecht Apocalmodulin and Ca2+-calmodulin bind to neighboring locations on the ryanodine receptor J. Biol. Chem. 277 2002 1349 1353
138. D.M. Balshaw, L. Xu, N. Yamaguchi, D.A. Pasek, and G. Meissner Calmodulin binding and inhibition of cardiac muscle calcium release channel (ryanodine receptor) J. Biol. Chem. 276 2001 20144 20153
139. H. Zhang, J.Z. Zhang, C.I. Danila, and S.L. Hamilton A noncontiguous, intersubunit binding site for calmodulin on the skeletal muscle Ca2+ release channel J. Biol. Chem. 278 2003 8348 8355
140. L.W. Xiong, R.A. Newman, G.G. Rodney, O. Thomas, J.Z. Zhang, A. Persechini, M.A. Shea, and S.L. Hamilton Lobe-dependent regulation of ryanodine receptor type 1 by calmodulin J. Biol. Chem. 277 2002 40862 40870
141. W.B. Limpitikul, I.E. Dick, R. Joshi-Mukherjee, M.T. Overgaard, A.L. George Jr., and D.T. Yue Calmodulin mutations associated with long QT syndrome prevent inactivation of cardiac L-type Ca(2+) currents and promote proarrhythmic behavior in ventricular myocytes J. Mol. Cell. Cardiol. 74 2014 115 124
142. M.G. Erickson, B.A. Alseikhan, B.Z. Peterson, and D.T. Yue Preassociation of calmodulin with voltage-gated Ca(2+) channels revealed by FRET in single living cells Neuron 31 2001 973 985
143. G. Yin, F. Hassan, A.R. Haroun, L.L. Murphy, L. Crotti, P.J. Schwartz, A.L. George, and J. Satin Arrhythmogenic calmodulin mutations disrupt intracellular cardiomyocyte Ca2+ regulation by distinct mechanisms J. Am. Heart Assoc. 3 2014 e000996
144. N.J. Boczek, M.L. Will, C.G. Lopocaro, D.J. Tester, and M.J. Ackerman Abstract 14699: spectrum and prevalence of CALM1, CALM2, and CALM3 mutations in long QT syndrome, catecholaminergic polymorphic ventricular tachycardia, idiopathic ventricular fibrillation, and sudden unexplained death in the Young Circulation 128 2013
145. I.A. Prior, P.D. Lewis, and C. Mattos A comprehensive survey of Ras mutations in cancer Cancer Res. 72 2012 2457 2467
146. C. Lopez-Alcala, B. Alvarez-Moya, P. Villalonga, M. Calvo, O. Bachs, and N. Agell Identification of essential interacting elements in K-Ras/calmodulin binding and its role in K-Ras localization J. Biol. Chem. 283 2008 10621 10631
147. P. Bhagatji, R. Leventis, R. Rich, C.J. Lin, and J.R. Silvius Multiple cellular proteins modulate the dynamics of K-ras association with the plasma membrane Biophys. J. 99 2010 3327 3335
148. S.J. Abraham, R.P. Nolet, R.J. Calvert, L.M. Anderson, and V. Gaponenko The hypervariable region of K-Ras4B is responsible for its specific interactions with calmodulin Biochemistry 48 2009 7575 7583
149. R.S. Sidhu, R.R. Clough, and R.P. Bhullar Ca2+/calmodulin binds and dissociates K-RasB from membrane Biochem. Biophys. Res. Commun. 304 2003 655 660
150. M. Fivaz, and T. Meyer Reversible intracellular translocation of KRas but not HRas in hippocampal neurons regulated by Ca2+/calmodulin J. Cell Biol. 170 2005 429 441
151. J.F. Hancock, H. Paterson, and C.J. Marshall A polybasic domain or palmitoylation is required in addition to the CAAX motif to localize p21ras to the plasma membrane Cell 63 1990 133 139
152. J.R. Silvius, P. Bhagatji, R. Leventis, and D. Terrone K-ras4B and prenylated proteins lacking "second signals" associate dynamically with cellular membranes Mol. Biol. Cell 17 2006 192 202
153. T.G. Bivona, S.E. Quatela, B.O. Bodemann, I.M. Ahearn, M.J. Soskis, A. Mor, J. Miura, H.H. Wiener, L. Wright, S.G. Saba, D. Yim, A. Fein, I. Perez de Castro, C. Li, C.B. Thompson, A.D. Cox, and M.R. Philips PKC regulates a farnesyl-electrostatic switch on K-Ras that promotes its association with Bcl-XL on mitochondria and induces apoptosis Mol. Cell 21 2006 481 493
154. P.J. Sung, F.D. Tsai, H. Vais, H. Court, J. Yang, N. Fehrenbacher, J.K. Foskett, and M.R. Philips Phosphorylated K-Ras limits cell survival by blocking Bcl-xL sensitization of inositol trisphosphate receptors Proc. Natl. Acad. Sci. U. S. A. 110 2013 20593 20598
155. B. Alvarez-Moya, C. Barcelo, F. Tebar, M. Jaumot, and N. Agell CaM interaction and Ser181 phosphorylation as new K-Ras signaling modulators Small GTPases 2 2011 99 103
156. M. Matsubara, T. Nakatsu, H. Kato, and H. Taniguchi Crystal structure of a myristoylated CAP-23/NAP-22 N-terminal domain complexed with Ca2+/calmodulin EMBO J. 23 2004 712 718
157. M. Matsubara, K. Titani, H. Taniguchi, and N. Hayashi Direct involvement of protein myristoylation in myristoylated alanine-rich C kinase substrate (MARCKS)-calmodulin interaction J. Biol. Chem. 278 2003 48898 48902
158. 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 2005 902 905
159. O. Mignen, J.L. Thompson, and T.J. Shuttleworth Orai1 subunit stoichiometry of the mammalian CRAC channel pore J. Physiol. 586 2008 419 425
160. 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 2006 2073 2079
161. M. Vig, C. Peinelt, A. Beck, D.L. Koomoa, D. Rabah, M. Koblan-Huberson, S. Kraft, H. Turner, A. Fleig, R. Penner, and J.P. Kinet CRACM1 is a plasma membrane protein essential for store-operated Ca2+ entry Science 312 2006 1220 1223
162. 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 2006 226 229
163. T. Hewavitharana, X. Deng, J. Soboloff, and D.L. Gill Role of STIM and Orai proteins in the store-operated calcium signaling pathway Cell Calcium 42 2007 173 182
164. J.C. Mercer, W.I. Dehaven, J.T. Smyth, B. Wedel, R.R. Boyles, G.S. Bird, and J.W. Putney Jr. Large store-operated calcium-selective currents due to co-expression of Orai1 or Orai2 with the intracellular calcium sensor, Stim1 J. Biol. Chem. 281 2006 24979 24990
165. A. Berna-Erro, A. Braun, R. Kraft, C. Kleinschnitz, M.K. Schuhmann, D. Stegner, T. Wultsch, J. Eilers, S.G. Meuth, G. Stoll, and B. Nieswandt STIM2 regulates capacitive Ca2+ entry in neurons and plays a key role in hypoxic neuronal cell death Sci. Signal. 2 2009 ra67
166. O. Brandman, J. Liou, W.S. Park, and T. Meyer STIM2 is a feedback regulator that stabilizes basal cytosolic and endoplasmic reticulum Ca2+ levels Cell 131 2007 1327 1339
167. 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 2008 538 542
168. P.B. Stathopulos, G.Y. Li, M.J. Plevin, J.B. Ames, and M. Ikura Stored Ca2+ depletion-induced oligomerization of stromal interaction molecule 1 (STIM1) via the EF-SAM region: an initiation mechanism for capacitive Ca2+ entry J. Biol. Chem. 281 2006 35855 35862
169. M. Muik, I. Frischauf, I. Derler, M. Fahrner, J. Bergsmann, P. Eder, R. Schindl, C. Hesch, B. Polzinger, R. Fritsch, H. Kahr, J. Madl, H. Gruber, K. Groschner, and C. Romanin Dynamic coupling of the putative coiled-coil domain of ORAI1 with STIM1 mediates ORAI1 channel activation J. Biol. Chem. 283 2008 8014 8022
170. 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 2009 876 890
171. J.P. Yuan, W. Zeng, M.R. Dorwart, Y.J. Choi, P.F. Worley, and S. Muallem SOAR and the polybasic STIM1 domains gate and regulate Orai channels Nat. Cell Biol. 11 2009 337 343
172. L. Zheng, P.B. Stathopulos, G.Y. Li, and M. Ikura Biophysical characterization of the EF-hand and SAM domain containing Ca2+ sensory region of STIM1 and STIM2 Biochem. Biophys. Res. Commun. 369 2008 240 246
173. L. Zheng, P.B. Stathopulos, R. Schindl, G.Y. Li, C. Romanin, and M. Ikura Auto-inhibitory role of the EF-SAM domain of STIM proteins in store-operated calcium entry Proc. Natl. Acad. Sci. U. S. A. 108 2011 1337 1342
174. L. Holm, S. Kaariainen, C. Wilton, and D. Plewczynski Using Dali for structural comparison of proteins Curr. Protoc. Bioinform. Chapter 5 2006 Unit 5 5
175. C.D. Thanos, K.E. Goodwill, and J.U. Bowie Oligomeric structure of the human EphB2 receptor SAM domain Science 283 1999 833 836
176. F. Qiao, and J.U. Bowie The many faces of SAM Sci. STKE 2005 2005 re7
177. Y. Baba, K. Hayashi, Y. Fujii, A. Mizushima, H. Watarai, M. Wakamori, T. Numaga, Y. Mori, M. Iino, M. Hikida, and T. Kurosaki Coupling of STIM1 to store-operated Ca2+ entry through its constitutive and inducible movement in the endoplasmic reticulum Proc. Natl. Acad. Sci. U. S. A. 103 2006 16704 16709
178. E.D. Covington, M.M. Wu, and R.S. Lewis Essential role for the CRAC activation domain in store-dependent oligomerization of STIM1 Mol. Biol. Cell 21 2010 1897 1907
179. Y. Furukawa, S. Teraguchi, T. Ikegami, O. Dagliyan, L. Jin, D. Hall, N.V. Dokholyan, K. Namba, S. Akira, T. Kurosaki, Y. Baba, and D.M. Standley Intrinsic disorder mediates cooperative signal transduction in STIM1 J. Mol. Biol. 426 2014 2082 2097
180. Y. Zhou, P. Srinivasan, S. Razavi, S. Seymour, P. Meraner, A. Gudlur, P.B. Stathopulos, M. Ikura, A. Rao, and P.G. Hogan Initial activation of STIM1, the regulator of store-operated calcium entry Nat. Struct. Mol. Biol. 20 2013 973 981
181. P. Malaney, R.R. Pathak, B. Xue, V.N. Uversky, and V. Dave Intrinsic disorder in PTEN and its interactome confers structural plasticity and functional versatility Sci. Rep. 3 2013 2035
182. A.B. Sigalov, and V.N. Uversky Differential occurrence of protein intrinsic disorder in the cytoplasmic signaling domains of cell receptors Self Nonself 2 2011 55 72
183. A.V. Uversky, B. Xue, Z. Peng, L. Kurgan, and V.N. Uversky On the intrinsic disorder status of the major players in programmed cell death pathways F1000Res. 2 2013 190
184. P.E. Wright, and H.J. Dyson Linking folding and binding Curr. Opin. Struct. Biol. 19 2009 31 38
185. B. Xue, A.K. Dunker, and V.N. Uversky The roles of intrinsic disorder in orchestrating the Wnt-pathway J. Biomol. Struct. Dyn. 29 2012 843 861
186. J. Liou, M. Fivaz, T. Inoue, and T. Meyer Live-cell imaging reveals sequential oligomerization and local plasma membrane targeting of stromal interaction molecule 1 after Ca2+ store depletion Proc. Natl. Acad. Sci. U. S. A. 104 2007 9301 9306
187. R.M. Luik, M.M. Wu, J. Buchanan, and R.S. Lewis The elementary unit of store-operated Ca2+ entry: local activation of CRAC channels by STIM1 at ER-plasma membrane junctions J. Cell Biol. 174 2006 815 825
188. 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 2006 803 813
189. M. Muik, M. Fahrner, I. Derler, R. Schindl, J. Bergsmann, I. Frischauf, K. Groschner, and C. Romanin A cytosolic homomerization and a modulatory domain within STIM1 C terminus determine coupling to ORAI1 channels J. Biol. Chem. 284 2009 8421 8426
190. M. Muik, M. Fahrner, R. Schindl, P. Stathopulos, I. Frischauf, I. Derler, P. Plenk, B. Lackner, K. Groschner, M. Ikura, and C. Romanin STIM1 couples to ORAI1 via an intramolecular transition into an extended conformation EMBO J. 30 2011 1678 1689
191. N. Calloway, T. Owens, K. Corwith, W. Rodgers, D. Holowka, and B. Baird Stimulated association of STIM1 and Orai1 is regulated by the balance of PtdIns(4,5)P(2) between distinct membrane pools J. Cell Sci. 124 2011 2602 2610
192. M.K. Korzeniowski, M.A. Popovic, Z. Szentpetery, P. Varnai, S.S. Stojilkovic, and T. Balla Dependence of STIM1/Orai1-mediated calcium entry on plasma membrane phosphoinositides J. Biol. Chem. 284 2009 21027 21035
193. C.M. Walsh, M. Chvanov, L.P. Haynes, O.H. Petersen, A.V. Tepikin, and R.D. Burgoyne Role of phosphoinositides in STIM1 dynamics and store-operated calcium entry Biochem. J. 425 2010 159 168
194. X. Hou, L. Pedi, M.M. Diver, and S.B. Long Crystal structure of the calcium release-activated calcium channel Orai Science 338 2012 1308 1313
195. P.B. Stathopulos, R. Schindl, M. Fahrner, L. Zheng, G.M. Gasmi-Seabrook, M. Muik, C. Romanin, and M. Ikura STIM1/Orai1 coiled-coil interplay in the regulation of store-operated calcium entry Nat. Commun. 4 2013 2963
196. B. Cui, X. Yang, S. Li, Z. Lin, Z. Wang, C. Dong, and Y. Shen The inhibitory helix controls the intramolecular conformational switching of the C-terminus of STIM1 PLoS One 8 2013 e74735
197. X. Yang, H. Jin, X. Cai, S. Li, and Y. Shen Structural and mechanistic insights into the activation of Stromal interaction molecule 1 (STIM1) Proc. Natl. Acad. Sci. U. S. A. 109 2012 5657 5662
198. M. Fahrner, M. Muik, R. Schindl, C. Butorac, P. Stathopulos, L. Zheng, I. Jardin, M. Ikura, and C. Romanin A coiled-coil clamp controls both conformation and clustering of stromal interaction molecule 1 (STIM1) J. Biol. Chem. 289 2014 33231 33244
199. P.J. Shaw, B. Qu, M. Hoth, and S. Feske Molecular regulation of CRAC channels and their role in lymphocyte function Cell. Mol. Life Sci. 70 2013 2637 2656
200. P.B. Stathopulos, and M. Ikura Structure and function of endoplasmic reticulum STIM calcium sensors Curr. Top. Membr. 71 2013 59 93
201. P.B. Stathopulos, L. Zheng, and M. Ikura Stromal interaction molecule (STIM) 1 and STIM2 calcium sensing regions exhibit distinct unfolding and oligomerization kinetics J. Biol. Chem. 284 2009 728 732
202. 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 2006 179 185
203. W. Bergmeier, C. Weidinger, I. Zee, and S. Feske Emerging roles of store-operated Ca(2)(+) entry through STIM and ORAI proteins in immunity, hemostasis and cancer Channels (Austin) 7 2013 379 391
204. S. Feske ORAI1 and STIM1 deficiency in human and mice: roles of store-operated Ca2+ entry in the immune system and beyond Immunol. Rev. 231 2009 189 209
205. F. Le Deist, C. Hivroz, M. Partiseti, C. Thomas, H.A. Buc, M. Oleastro, B. Belohradsky, D. Choquet, and A. Fischer A primary T-cell immunodeficiency associated with defective transmembrane calcium influx Blood 85 1995 1053 1062
206. C.A. McCarl, C. Picard, S. Khalil, T. Kawasaki, J. Rother, A. Papolos, J. Kutok, C. Hivroz, F. Ledeist, K. Plogmann, S. Ehl, G. Notheis, M.H. Albert, B.H. Belohradsky, J. Kirschner, A. Rao, A. Fischer, and S. Feske ORAI1 deficiency and lack of store-operated Ca2+ entry cause immunodeficiency, myopathy, and ectodermal dysplasia J. Allergy Clin. Immunol. 124 2009 1311 1318 e1317
207. M. Partiseti, F. Le Deist, C. Hivroz, A. Fischer, H. Korn, and D. Choquet The calcium current activated by T cell receptor and store depletion in human lymphocytes is absent in a primary immunodeficiency J. Biol. Chem. 269 1994 32327 32335
208. M. Byun, A. Abhyankar, V. Lelarge, S. Plancoulaine, A. Palanduz, L. Telhan, B. Boisson, C. Picard, S. Dewell, C. Zhao, E. Jouanguy, S. Feske, L. Abel, and J.L. Casanova Whole-exome sequencing-based discovery of STIM1 deficiency in a child with fatal classic Kaposi sarcoma J. Exp. Med. 207 2010 2307 2312
209. C. Picard, C.A. McCarl, A. Papolos, S. Khalil, K. Luthy, C. Hivroz, F. LeDeist, F. Rieux-Laucat, G. Rechavi, A. Rao, A. Fischer, and S. Feske STIM1 mutation associated with a syndrome of immunodeficiency and autoimmunity N. Engl. J. Med. 360 2009 1971 1980
210. K.T. Cheng, I. Alevizos, X. Liu, W.D. Swaim, H. Yin, S. Feske, M. Oh-hora, and I.S. Ambudkar STIM1 and STIM2 protein deficiency in T lymphocytes underlies development of the exocrine gland autoimmune disease, Sjogren's syndrome Proc. Natl. Acad. Sci. U. S. A. 109 2012 14544 14549
211. S. Fuchs, A. Rensing-Ehl, C. Speckmann, B. Bengsch, A. Schmitt-Graeff, I. Bondzio, A. Maul-Pavicic, T. Bass, T. Vraetz, B. Strahm, T. Ankermann, M. Benson, A. Caliebe, R. Folster-Holst, P. Kaiser, R. Thimme, W.W. Schamel, K. Schwarz, S. Feske, and S. Ehl Antiviral and regulatory T cell immunity in a patient with stromal interaction molecule 1 deficiency J. Immunol. 188 2012 1523 1533
212. D. Misceo, A. Holmgren, W.E. Louch, P.A. Holme, M. Mizobuchi, R.J. Morales, A.M. De Paula, A. Stray-Pedersen, R. Lyle, B. Dalhus, G. Christensen, H. Stormorken, G.E. Tjonnfjord, and E. Frengen A dominant STIM1 mutation causes Stormorken syndrome Hum. Mutat. 35 2014 556 564
213. G. Morin, N.O. Bruechle, A.R. Singh, C. Knopp, G. Jedraszak, M. Elbracht, D. Bremond-Gignac, K. Hartmann, H. Sevestre, P. Deutz, D. Herent, P. Nurnberg, B. Romeo, K. Konrad, M. Mathieu-Dramard, J. Oldenburg, E. Bourges-Petit, Y. Shen, K. Zerres, H. Ouadid-Ahidouch, and J. Rochette Gain-of-Function mutation in STIM1 (P.R304W) is associated with Stormorken syndrome Hum. Mutat. 35 2014 1221 1232
214. S.A. Forbes, D. Beare, P. Gunasekaran, K. Leung, N. Bindal, H. Boutselakis, M. Ding, S. Bamford, C. Cole, S. Ward, C.Y. Kok, M. Jia, T. De, J.W. Teague, M.R. Stratton, U. McDermott, and P.J. Campbell COSMIC: exploring the world's knowledge of somatic mutations in human cancer Nucleic Acids Res. 43(Database issue) 2015 D805 D811
215. P.B. Stathopulos, and M. Ikura Structurally delineating stromal interaction molecules as the endoplasmic reticulum calcium sensors and regulators of calcium release-activated calcium entry Immunol. Rev. 231 2009 113 131
216. M.C. Bauer, D. O'Connell, D.J. Cahill, and S. Linse Calmodulin binding to the polybasic C-termini of STIM proteins involved in store-operated calcium entry Biochemistry 47 2008 6089 6091
217. F.M. Mullins, C.Y. Park, R.E. Dolmetsch, and R.S. Lewis STIM1 and calmodulin interact with Orai1 to induce Ca2+-dependent inactivation of CRAC channels Proc. Natl. Acad. Sci. U. S. A. 106 2009 15495 15500
218. Y. Liu, X. Zheng, G.A. Mueller, M. Sobhany, E.F. DeRose, Y. Zhang, R.E. London, and L. Birnbaumer Crystal structure of calmodulin binding domain of orai1 in complex with Ca2+ calmodulin displays a unique binding mode J. Biol. Chem. 287 2012 43030 43041
219. B.J. Marsden, G.S. Shaw, and B.D. Sykes Calcium binding proteins. Elucidating the contributions to calcium affinity from an analysis of species variants and peptide fragments Biochem. Cell Biol. 68 1990 587 601