Calmodulin-controlled spatial decoding of oscillatory Ca2+ signals by calcineurin

eLife

Volumn 3, Issue July2014, 2014, Pages 1-22

  Mehta, Sohum ^a   Aye Han, Nwe Nwe ^a   Ganesan, Ambhighainath ^b   Oldach, Laurel ^a   Gorshkov, Kirill ^a   Zhang, Jin ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Johns Hopkins University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCINEURIN; CALCIUM; CALMODULIN; CYAN FLUORESCENT PROTEIN; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN;

ANIMAL; CALCIUM SIGNALING; CELL COMPARTMENTALIZATION; CELL LINE; CELL MEMBRANE; CYTOLOGY; CYTOSOL; ENDOPLASMIC RETICULUM; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MITOCHONDRION; MOUSE; PANCREAS ISLET BETA CELL; REPORTER GENE; TIME FACTOR; TRANSGENIC MOUSE;

ANIMALS; CALCINEURIN; CALCIUM; CALCIUM SIGNALING; CALMODULIN; CELL COMPARTMENTATION; CELL LINE; CELL MEMBRANE; CYTOSOL; ENDOPLASMIC RETICULUM; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENE EXPRESSION REGULATION; GENES, REPORTER; GREEN FLUORESCENT PROTEINS; INSULIN-SECRETING CELLS; MICE; MICE, TRANSGENIC; MITOCHONDRIA; RECOMBINANT FUSION PROTEINS; TIME FACTORS;

EID: 84934298462     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.03765     Document Type: Article

References (106)

1. Abrenica B, AlShaaban M, Czubryt MP. 2009. The A-kinase anchor protein AKAP121 is a negative regulator of cardiomyocyte hypertrophy. Journal of Molecular and Cellular Cardiology 46:674-681. doi: 10.1016/j.yjmcc.2009.01.018.
2. Akerboom J, Carreras Calderón N, Tian L, Wabnig S, Prigge M, Tolö J, Gordus A, Orger MB, Severi KE, Macklin JJ, Patel R, Pulver SR, Wardill TJ, Fischer E, Schüler C, Chen TW, Sarkisyan KS, Marvin JS, Bargmann CI, Kim DS, Kügler S, Lagnado L, Hegemann P, Gottschalk A, Schreiter ER, Looger LL. 2013. Genetically encoded calcium indicators for multi-color neural activity imaging and combination with optogenetics. Frontiers in Molecular Neuroscience 6:2. doi: 10.3389/fnmol.2013.00002.
3. Aramburu J, Heitman J, Crabtree GR. 2004. Calcineurin: a central controller of signalling in eukaryotes. EMBO Reports 5:343-348. doi: 10.1038/sj.embor.7400133.
4. Ashcroft FM, Rorsman P. 1989. Electrophysiology of the pancreatic β-cell. Progress in Biophysics and Molecular Biology 54:87-143. doi: 10.1016/0079-6107(89)90013-8.
5. Bading H, Ginty DD, Greenberg ME. 1993. Regulation of gene expression in hippocampal neurons by distinct calcium signaling pathways. Science 260:181-186. doi: 10.1126/science.8097060.
6. Bandyopadhyay A, Shin DW, Ahn JO, Kim DH. 2000. Calcineurin regulates ryanodine receptor/Ca2+-release channels in rat heart. The Biochemical Journal 352:61-70. doi: 10.1042/0264-6021:3520061.
7. Barg S, Ma X, Eliasson L, Galvanovskis J, Göpel SO, Obermüller S, Platzer J, Renström E, Trus M, Atlas D, Striessnig J, Rorsman P. 2001. Fast exocytosis with few Ca2+ channels in insulin-secreting mouse pancreatic B cells. Biophysical Journal 81:3308-3323. doi: 10.1016/S0006-3495(01)75964-4.
8. Beals CR, Sheridan CM, Turck CW, Gardner P, Crabtree GR. 1997. Nuclear export of NF-ATc enhanced by glycogen synthase kinase-3. Science 275:1930-1934. doi: 10.1126/science.275.5308.1930.
9. Bernal-Mizrachi E, Cras-Méneur C, Ye BR, Johnson JD, Permutt MA. 2010. Transgenic overexpression of active calcineurin in β-cells results in decreased β-cell mass and hyperglycemia. PLOS ONE 5:e11969. doi: 10.1371/journal.pone.0011969.
10. Berridge MJ, Lipp P, Bootman MD. 2000. The versatility and universality of calcium signalling. Nature Reviews Molecular Cell Biology 1:11-21. doi: 10.1038/35036035.
11. Bianchi CP, Shanes AM. 1959. Calcium influx in skeletal muscle at rest, during activity, and during potassium contracture. The Journal of General Physiology 42:803-815. doi: 10.1085/jgp.42.4.803.
12. Bokvist K, Eliasson L, Ammälä C, Renström E, Rorsman P. 1995. Co-localization of L-type Ca2+ channels and insulin-containing secretory granules and its significance for the initiation of exocytosis in mouse pancreatic β-cells. The EMBO Journal 14:50-57.
13. Bollo M, Paredes RM, Holstein D, Zheleznova N, Camacho P, Lechleiter JD. 2010. Calcineurin interacts with PERK and dephosphorylates calnexin to relieve ER stress in mammals and frogs. PLOS ONE 5:e11925. doi: 10.1371/journal.pone.0011925.
14. Camello C, Lomax R, Petersen OH, Tepikin AV. 2002. Calcium leak from intracellular stores-the enigma of calcium signalling. Cell Calcium 32:355-361. doi: 10.1016/S0143416002001926.
15. Cameron AM, Steiner JP, Roskams AJ, Ali SM, Ronnett GV, Snyder SH. 1995. Calcineurin associated with the inositol 1,4,5-trisphosphate receptor-FKBP12 complex modulates Ca2+ flux. Cell 83:463-472. doi: 10.1016/0092-8674(95)90124-8.
16. Cereghetti GM, Costa V, Scorrano L. 2010. Inhibition of Drp1-dependent mitochondrial fragmentation and apoptosis by a polypeptide antagonist of calcineurin. Cell Death and Differentiation 17:1785-1794. doi: 10.1038/cdd.2010.61.
17. Cereghetti GM, Stangherlin A, Martins de Brito O, Chang CR, Blackstone C, Bernardi P, Scorrano L. 2008. Dephosphorylation by calcineurin regulates translocation of Drp1 to mitochondria. Proceedings of the National Academy of Sciences of USA 105:15803-15808. doi: 10.1073/pnas.0808249105.
18. Chakkera HA, Mandarino LJ. 2013. Calcineurin inhibition and new-onset diabetes mellitus after transplantation. Transplantation 95:647-652. doi: 10.1097/TP.0b013e31826e592e.
19. Cheong R, Levchenko A. 2010. Oscillatory signaling processes: the how, the why and the where. Current Opinion in Genetics & Development 20:665-669. doi: 10.1016/j.gde.2010.08.007.
20. Colella M, Grisan F, Robert V, Turner JD, Thomas AP, Pozzan T. 2008. Ca2+ oscillation frequency decoding in cardiac cell hypertrophy: role of calcineurin/NFAT as Ca2+ signal integrators. Proceedings of the National Academy of Sciences of USA 105:2859-2864. doi: 10.1073/pnas.0712316105.
21. Crabtree GR, Olson EN. 2002. NFAT signaling: choreographing the social lives of cells. Cell 109(suppl):S67-S79. doi: 10.1016/S0092-8674(02)00699-2.
22. Cribbs JT, Strack S. 2007. Reversible phosphorylation of Drp1 by cyclic AMP-dependent protein kinase and calcineurin regulates mitochondrial fission and cell death. EMBO Reports 8:939-944. doi: 10.1038/sj.embor.7401062.
23. de Brito OM, Scorrano L. 2010. An intimate liaison: spatial organization of the endoplasmic reticulum-mitochondria relationship. The EMBO Journal 29:2715-2723. doi: 10.1038/emboj.2010.177.
24. Deisseroth K, Heist EK, Tsien RW. 1998. Translocation of calmodulin to the nucleus supports CREB phosphorylation in hippocampal neurons. Nature 392:198-202. doi: 10.1038/32448.
25. Depry C, Allen MD, Zhang J. 2011. Visualization of PKA activity in plasma membrane microdomains. Molecular Biosystems 7:52-58. doi: 10.1039/c0mb00079e.
26. DiPilato LM, Cheng X, Zhang J. 2004. Fluorescent indicators of cAMP and Epac activation reveal differential dynamics of cAMP signaling within discrete subcellular compartments. Proceedings of the National Academy of Sciences of USA 101:16513-16518. doi: 10.1073/pnas.0405973101.
27. Dolmetsch RE, Xu K, Lewis RS. 1998. Calcium oscillations increase the efficiency and specificity of gene expression. Nature 392:933-936. doi: 10.1038/31960.
28. Dupont G, Lokenye EF, Challiss RA. 2011. A model for Ca2+ oscillations stimulated by the type 5 metabotropic glutamate receptor: an unusual mechanism based on repetitive, reversible phosphorylation of the receptor. Biochimie 93:2132-2138. doi: 10.1016/j.biochi.2011.09.010.
29. Everett KL, Cooper DM. 2013. An improved targeted cAMP sensor to study the regulation of adenylyl cyclase 8 by Ca2+ entry through voltage-gated channels. PLOS ONE 8:e75942. doi: 10.1371/journal.pone.0075942.
30. Friedman JR, Lackner LL, West M, DiBenedetto JR, Nunnari J, Voeltz GK. 2011. ER tubules mark sites of mitochondrial division. Science 334:358-362. doi: 10.1126/science.1207385.
31. Fujii H, Inoue M, Okuno H, Sano Y, Takemoto-Kimura S, Kitamura K, Kano M, Bito H. 2013. Nonlinear decoding and asymmetric representation of neuronal input information by CaMKIIα and calcineurin. Cell Reports 3:978-987. doi: 10.1016/j.celrep.2013.03.033.
32. Ganesan A, Zhang J. 2012. How cells process information: quantification of spatiotemporal signaling dynamics. Protein Science 21:918-928. doi: 10.1002/pro.2089.
33. Gao X, Zhang J. 2008. Spatiotemporal analysis of differential Akt regulation in plasma membrane microdomains. Molecular Biology of the Cell 19:4366-4373. doi: 10.1091/mbc.E08-05-0449.
34. Gold MG, Stengel F, Nygren PJ, Weisbrod CR, Bruce JE, Robinson CV, Barford D, Scott JD. 2011. Architecture and dynamics of an A-kinase anchoring protein 79 (AKAP79) signaling complex. Proceedings of the National Academy of Sciences of USA 108:6426-6431. doi: 10.1073/pnas.1014400108.
35. Graef IA, Mermelstein PG, Stankunas K, Neilson JR, Deisseroth K, Tsien RW, Crabtree GR. 1999. L-type calcium channels and GSK-3 regulate the activity of NF-ATc4 in hippocampal neurons. Nature 401:703-708. doi: 10.1038/44378.
36. Hammadi M, Oulidi A, Gackiere F, Katsogiannou M, Slomianny C, Roudbaraki M, Dewailly E, Delcourt P, Lepage G, Lotteau S, Ducreux S, Prevarskaya N, Van Coppenolle F. 2013. Modulation of ER stress and apoptosis by endoplasmic reticulum calcium leak via translocon during unfolded protein response: involvement of GRP78. FASEB Journal 27:1600-1609. doi: 10.1096/fj.12-218875.
37. Heineke J, Ritter O. 2012. Cardiomyocyte calcineurin signaling in subcellular domains: from the sarcolemma to the nucleus and beyond. Journal of Molecular and Cellular Cardiology 52:62-73. doi: 10.1016/j.yjmcc.2011.10.018.
38. Heisel O, Heisel R, Balshaw R, Keown P. 2004. New onset diabetes mellitus in patients receiving calcineurin inhibitors: a systematic review and meta-analysis. American Journal of Transplantation 4:583-595. doi: 10.1046/j.1600-6143.2003.00372.x.
39. Heit JJ, Apelqvist AA, Gu X, Winslow MM, Neilson JR, Crabtree GR, Kim SK. 2006. Calcineurin/NFAT signalling regulates pancreatic β-cell growth and function. Nature 443:345-349. doi: 10.1038/nature05097.
40. Hellman B, Gylfe E, Grapengiesser E, Lund PE, Berts A. 1992. Cytoplasmic Ca2+ oscillations in pancreatic β-cells. Biochimica et Biophysica Acta 1113:295-305. doi: 10.1016/0304-4157(92)90003-S.
41. Hilioti Z, Cunningham KW. 2003. Calcineurin: roles of the Ca2+/calmodulin-dependent protein phosphatase in diverse eukaryotes. Topics in Current Genetics 5:73-90. doi: 10.1007/978-3-540-40035-6_4.
42. Hille B. 1967. The selective inhibition of delayed potassium currents in nerve by tetraethylammonium ion. The Journal of General Physiology 50:1287-1302. doi: 10.1085/jgp.50.5.1287.
43. Hinke SA, Navedo MF, Ulman A, Whiting JL, Nygren PJ, Tian G, Jimenez-Caliani AJ, Langeberg LK, Cirulli V, Tengholm A, Dell'Acqua ML, Santana LF, Scott JD. 2012. Anchored phosphatases modulate glucose homeostasis. The EMBO Journal 31:3991-4004. doi: 10.1038/emboj.2012.244.
44. Hogan PG, Chen L, Nardone J, Rao A. 2003. Transcriptional regulation by calcium, calcineurin, and NFAT. Genes & Development 17:2205-2232. doi: 10.1101/gad.1102703.
45. Horikawa K, Yamada Y, Matsuda T, Kobayashi K, Hashimoto M, Matsu-ura T, Miyawaki A, Michikawa T, Mikoshiba K, Nagai T. 2010. Spontaneous network activity visualized by ultrasensitive Ca(2+) indicators, yellow Cameleon-Nano. Nature Methods 7:729-732. doi: 10.1038/nmeth.1488.
46. Hubbard MJ, Klee CB. 1987. Calmodulin binding by calcineurin. Ligand-induced renaturation of protein immobilized on nitrocellulose. The Journal of Biological Chemistry 262:15062-15070.
47. Kozak M. 1987. An analysis of 5'-noncoding sequences from 699 vertebrate messenger RNAs. Nucleic Acids Research 15:8125-8148. doi: 10.1093/nar/15.20.8125.
48. Kupzig S, Walker SA, Cullen PJ. 2005. The frequencies of calcium oscillations are optimized for efficient calcium-mediated activation of Ras and the ERK/MAPK cascade. Proceedings of the National Academy of Sciences of USA 102:7577-7582. doi: 10.1073/pnas.0409611102.
49. Landa LR, Harbeck MC, Kaihara K, Chepurny OG, Kitiphongspattana K, Graf O, Nikolaev VO, Lohse MJ, Holz GG, Roe MW. 2005. Interplay of Ca2+ and cAMP signaling in the insulin-secreting MIN6 β-cell line. The Journal of Biological Chemistry 280:31294-31302. doi: 10.1074/jbc.M505657200.
50. Lester LB, Faux MC, Nauert JB, Scott JD. 2001. Targeted protein kinase A and PP-2B regulate insulin secretion through reversible phosphorylation. Endocrinology 142:1218-1227. doi: 10.1210/endo.142.3.8023.
51. Lewis RS. 2003. Calcium oscillations in T-cells: mechanisms and consequences for gene expression. Biochemical Society Transactions 31:925-929. doi: 10.1042/BST0310925.
52. Li H, Pink MD, Murphy JG, Stein A, Dell'Acqua ML, Hogan PG. 2012a. Balanced interactions of calcineurin with AKAP79 regulate Ca2+-calcineurin-NFAT signaling. Nature Structural & Molecular Biology 19:337-345. doi: 10.1038/nsmb.2238.
53. Li L, Stefan MI, Le Novère N. 2012b. Calcium input frequency, duration and amplitude differentially modulate the relative activation of calcineurin and CaMKII. PLOS ONE 7:e43810. doi: 10.1371/journal.pone.0043810.
54. Li W, Llopis J, Whitney M, Zlokarnik G, Tsien RY. 1998. Cell-permeant caged InsP3 ester shows that Ca2+ spike frequency can optimize gene expression. Nature 392:936-941. doi: 10.1038/31965.
55. Ma Y, Taylor SS. 2008. A molecular switch for targeting between endoplasmic reticulum (ER) and mitochondria: conversion of a mitochondria-targeting element into an ER-targeting signal in DAKAP1. The Journal of Biological Chemistry 283:11743-11751. doi: 10.1074/jbc.M710494200.
56. Macías W, Carlson R, Rajadhyaksha A, Barczak A, Konradi C. 2001. Potassium chloride depolarization mediates CREB phosphorylation in striatal neurons in an NMDA receptor-dependent manner. Brain Research 890:222-232. doi: 10.1016/S0006-8993(00)03163-2.
57. Maltsev VA, Lakatta EG. 2007. Normal heart rhythm is initiated and regulated by an intracellular calcium clock within pacemaker cells. Heart, Lung & Circulation 16:335-348. doi: 10.1016/j.hlc.2007.07.005.
58. Markwardt ML, Kremers G-J, Kraft CA, Ray K, Cranfill PJC, Wilson KA, Day RN, Wachter RM, Davidson MW, Rizzo MA. 2011. An improved cerulean fluorescent protein with enhanced brightness and reduced reversible photoswitching. PLOS ONE 6:e17896. doi: 10.1371/journal.pone.0017896.
59. Mears D. 2004. Regulation of insulin secretion in islets of Langerhans by Ca2+ channels. The Journal of Membrane Biology 200:57-66. doi: 10.1007/s00232-004-0692-9.
60. Mehta S, Zhang J. 2010. Reporting from the field: genetically encoded fluorescent reporters uncover signaling dynamics in living biological systems. Annual Review of Biochemistry 80:375-401. doi: 10.1146/annurev-biochem-060409-093259.
61. Mondragon A, Griffith EC, Sun L, Xiong F, Armstrong C, Liu JO. 1997. Overexpression and purification of human calcineurin α from Escherichia coli and assessment of catalytic functions of residues surrounding the binuclear metal center. Biochemistry 36:4934-4942. doi: 10.1021/bi9631935.
62. Mori MX. 2004. Functional stoichiometry and local enrichment of calmodulin interacting with Ca2+ channels. Science 304:432-435. doi: 10.1126/science.1093490.
63. Nagai T, Yamada S, Tominaga T, Ichikawa M, Miyawaki A. 2004. Expanded dynamic range of fluorescent indicators for Ca2+ by circularly permuted yellow fluorescent proteins. Proceedings of the National Academy of Sciences of USA 101:10554-10559. doi: 10.1073/pnas.0400417101.
64. Negulescu PA, Shastri N, Cahalan MD. 1994. Intracellular calcium dependence of gene expression in single T lymphocytes. Proceedings of the National Academy of Sciences of USA 91:2873-2877. doi: 10.1073/pnas.91.7.2873.
65. Newman RH, Zhang J. 2008. Visualization of phosphatase activity in living cells with a FRET-based calcineurin activity sensor. Molecular Biosystems 4:496-501. doi: 10.1039/b720034j.
66. Nguyen AW, Daugherty PS. 2005. Evolutionary optimization of fluorescent proteins for intracellular FRET. Nature Biotechnology 23:355-360. doi: 10.1038/nbt1066.
67. Ni Q, Ganesan A, Aye-Han N-N, Gao X, Allen MD, Levchenko A, Zhang J. 2010. Signaling diversity of PKA achieved via a Ca2+-cAMP-PKA oscillatory circuit. Nature Chemical Biology 7:34-40. doi: 10.1038/nchembio.478.
68. Okamura H, Aramburu J, Garcia-Rodriguez C, Viola JP, Raghavan A, Tahiliani M, Zhang X, Qin J, Hogan PG, Rao A. 2000. Concerted dephosphorylation of the transcription factor NFAT1 induces a conformational switch that regulates transcriptional activity. Molecular Cell 6:539-550. doi: 10.1016/S1097-2765(00)00053-8.
69. Oliveria SF, Dell'Acqua ML, Sather WA. 2007. AKAP79/150 anchoring of calcineurin controls neuronal L-type Ca2+ channel activity and nuclear signaling. Neuron 55:261-275. doi: 10.1016/j.neuron.2007.06.032.
70. Parekh AB. 2011. Decoding cytosolic Ca2+ oscillations. Trends in Biochemical Sciences 36:78-87. doi: 10.1016/j.tibs.2010.07.013.
71. Pasti L, Zonta M, Pozzan T, Vicini S, Carmignoto G. 2001. Cytosolic calcium oscillations in astrocytes may regulate exocytotic release of glutamate. The Journal of Neuroscience 21:477-484.
72. Persechini A, Cronk B. 1999. The relationship between the free concentrations of Ca2+ and Ca2+-calmodulin in intact cells. The Journal of Biological Chemistry 274:6827-6830. doi: 10.1074/jbc.274.11.6827.
73. Persechini A, Stemmer PM. 2002. Calmodulin is a limiting factor in the cell. Trends in Cardiovascular Medicine 12:32-37. doi: 10.1016/S1050-1738(01)00144-X.
74. Powell T, Tatham PE, Twist VW. 1984. Cytoplasmic free calcium measured by quin2 fluorescence in isolated ventricular myocytes at rest and during potassium-depolarization. Biochemical and Biophysical Research Communications 122:1012-1020. doi: 10.1016/0006-291X(84)91192-6.
75. Quintana AR, Wang D, Forbes JE, Waxham MN. 2005. Kinetics of calmodulin binding to calcineurin. Biochemical and Biophysical Research Communications 334:674-680. doi: 10.1016/j.bbrc.2005.06.152.
76. Rizzo MA, Springer GH, Granada B, Piston DW. 2004. An improved cyan fluorescent protein variant useful for FRET. Nature Biotechnology 22:445-449. doi: 10.1038/nbt945.
77. Rowland AA, Voeltz GK. 2012. Endoplasmic reticulum-mitochondria contacts: function of the junction. Nature Reviews Molecular Cell Biology 13:607-615. doi: 10.1038/nrm3440.
78. Rumi-Masante J, Rusinga FI, Lester TE, Dunlap TB, Williams TD, Dunker AK, Weis DD, Creamer TP. 2012. Structural basis for activation of calcineurin by calmodulin. Journal of Molecular Biology 415:307-317. doi: 10.1016/j.jmb.2011.11.008.
79. Rusnak F, Mertz P. 2000. Calcineurin: form and function. Physiological Reviews 80:1483-1521.
80. San-Antonio B, Iñiguez MA, Fresno M. 2002. Protein kinase Czeta phosphorylates nuclear factor of activated T cells and regulates its transactivating activity. The Journal of Biological Chemistry 277:27073-27080. doi: 10.1074/jbc.M106983200.
81. Santana LF, Chase EG, Votaw VS, Nelson MT, Greven R. 2002. Functional coupling of calcineurin and protein kinase A in mouse ventricular myocytes. The Journal of Physiology 544:57-69. doi: 10.1113/jphysiol.2002.020552.
82. Saucerman JJ, Bers DM. 2008. Calmodulin mediates differential sensitivity of CaMKII and calcineurin to local Ca2+ in cardiac myocytes. Biophysical Journal 95:4597-4612. doi: 10.1529/biophysj.108.128728.
83. Saucerman JJ, Bers DM. 2012. Calmodulin binding proteins provide domains of local Ca2+ signaling in cardiac myocytes. Journal of Molecular and Cellular Cardiology 52:312-316. doi: 10.1016/j.yjmcc.2011.06.005.
84. Sheridan CM, Heist EK, Beals CR, Crabtree GR, Gardner P. 2002. Protein kinase A negatively modulates the nuclear accumulation of NF-ATc1 by priming for subsequent phosphorylation by glycogen synthase kinase-3. The Journal of Biological Chemistry 277:48664-48676. doi: 10.1074/jbc.M207029200.
85. Slavov N, Carey J, Linse S. 2013. Calmodulin transduces Ca2+ oscillations into differential regulation of its target proteins. ACS Chemical Neuroscience 4:601-612. doi: 10.1021/cn300218d.
86. Slupe AM, Merrill RA, Flippo KH, Lobas MA, Houtman JCD, Strack S. 2013. A calcineurin docking motif (LXVP) in dynamin-related protein 1 contributes to mitochondrial fragmentation and ischemic neuronal injury. The Journal of Biological Chemistry 288:12353-12365. doi: 10.1074/jbc.M113.459677.
87. Song Q, Saucerman JJ, Bossuyt J, Bers DM. 2008. Differential integration of Ca2+-calmodulin signal in intact ventricular myocytes at low and high affinity Ca2+-calmodulin targets. The Journal of Biological Chemistry 283:31531-31540. doi: 10.1074/jbc.M804902200.
88. Szczesna-Skorupa E, Chen CD, Rogers S, Kemper B. 1998. Mobility of cytochrome P450 in the endoplasmic reticulum membrane. Proceedings of the National Academy of Sciences of USA 95:14793-14798. doi: 10.1073/pnas.95.25.14793.
89. Szlufcik K, Missiaen L, Parys JB, Callewaert G, Smedt H. 2012. Uncoupled IP3 receptor can function as a Ca2+-leak channel: cell biological and pathological consequences. Biology of the Cell 98:1-14. doi: 10.1042/BC20050031.
90. Tandan S, Wang Y, Wang TT, Jiang N, Hall DD, Hell JW, Luo X, Rothermel BA, Hill JA. 2009. Physical and functional interaction between calcineurin and the cardiac L-type Ca2+ channel. Circulation Research 105:51-60. doi: 10.1161/CIRCRESAHA.109.199828.
91. Tengholm A, Gylfe E. 2008. Oscillatory control of insulin secretion. Molecular and Cellular Endocrinology 297:58-72. doi: 10.1016/j.mce.2008.07.009.
92. Teruel MN, Chen W, Persechini A, Meyer T. 2000. Differential codes for free Ca(2+)-calmodulin signals in nucleus and cytosol. Current Biology 10:86-94. doi: 10.1016/S0960-9822(00)00295-5.
93. Thomas AP, Bird GS, Hajnóczky G, Robb-Gaspers LD, Putney JW. 1996. Spatial and temporal aspects of cellular calcium signaling. FASEB Journal 10:1505-1517.
94. Tian L, Hires SA, Mao T, Huber D, Chiappe ME, Chalasani SH, Petreanu L, Akerboom J, McKinney SA, Schreiter ER, Bargmann C, Jayaraman V, Svoboda K, Looger LL. 2009. Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators. Nature Methods 6:875-881. doi: 10.1038/nmeth.1398.
95. Tomida T, Hirose K, Takizawa A, Shibasaki F, Iino M. 2003. NFAT functions as a working memory of Ca2+ signals in decoding Ca2+ oscillation. The EMBO Journal 22:3825-3832. doi: 10.1093/emboj/cdg381.
96. Tran Q-K, Black DJ, Persechini A. 2003. Intracellular coupling via limiting calmodulin. The Journal of Biological Chemistry 278:24247-24250. doi: 10.1074/jbc.C300165200.
97. Tse A, Tse FW, Almers W, Hille B. 1993. Rhythmic exocytosis stimulated by GnRH-induced calcium oscillations in rat gonadotropes. Science 260:82-84. doi: 10.1126/science.8385366.
98. Ullman KS, Powers MA, Forbes DJ. 1997. Nuclear export receptors: from importin to exportin. Cell 90:967-970. doi: 10.1016/S0092-8674(00)80361-X.
99. Viatchenko-Karpinski S, Fleischmann BK, Liu Q, Sauer H, Gryshchenko O, Ji GJ, Hescheler J. 1999. Intracellular Ca2+ oscillations drive spontaneous contractions in cardiomyocytes during early development. Proceedings of the National Academy of Sciences of USA 96:8259-8264. doi: 10.1073/pnas.96.14.8259.
100. Wang HG, Pathan N, Ethell IM, Krajewski S, Yamaguchi Y, Shibasaki F, McKeon F, Bobo T, Franke TF, Reed JC. 1999. Ca2+-induced apoptosis through calcineurin dephosphorylation of BAD. Science 284:339-343. doi: 10.1126/science.284.5412.339.
101. Wang H, Du Y, Xiang B, Lin W, Li X, Wei Q. 2008. A renewed model of CNA regulation involving its C-terminal regulatory domain and CaM. Biochemistry 47:4461-4468. doi: 10.1021/bi702539e.
102. Wang R, McGrath BC, Kopp RF, Roe MW, Tang X, Chen G, Cavener DR. 2013. Insulin secretion and Ca2+ dynamics in β-cells are regulated by PERK EIF2α in concert with calcineurin. The Journal of Biological Chemistry 288:33824-33836. doi: 10.1074/jbc.M113.503664.
103. Wang X, Greer MA. 1995. Blocking K+ channels with TEA induces plasmalemma depolarization, increased [Ca2+]i, and ACTH secretion in AtT-20 cells. Molecular and Cellular Endocrinology 109:11-18. doi: 10.1016/0303-7207(95)03478-P.
104. Wiser O, Trus M, Hernández A, Renström E, Barg S, Rorsman P, Atlas D. 1999. The voltage sensitive Lc-type Ca2+ channel is functionally coupled to the exocytotic machinery. Proceedings of the National Academy of Sciences of USA 96:248-253. doi: 10.1073/pnas.96.1.248.
105. Wu HY, Hudry E, Hashimoto T, Uemura K, Fan ZY, Berezovska O, Grosskreutz CL, Bacskai BJ, Hyman BT. 2012. Distinct dendritic spine and nuclear phases of calcineurin activation after exposure to amyloid-β revealed by a novel fluorescence resonance energy transfer assay. The Journal of Neuroscience 32:5298-5309. doi: 10.1523/JNEUROSCI.0227-12.2012.
106. Wu X, Bers DM. 2007. Free and bound intracellular calmodulin measurements in cardiac myocytes. Cell Calcium 41:353-364. doi: 10.1016/j.ceca.2006.07.011.