Regulation of inositol 1,4,5-trisphosphate-induced Ca2+ release by reversible phosphorylation and dephosphorylation

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1793, Issue 6, 2009, Pages 959-970

  Vanderheyden, Veerle ^a   Devogelaere, Benoit ^a   Missiaen, Ludwig ^a   De Smedt, Humbert ^a   Bultynck, Geert ^a   Parys, Jan B ^a  

^a Laboratory of Molecular and Cellular Signaling   (Belgium)

Author keywords

Ca2+ signaling; Inositol 1,4,5 trisphosphate; Inositol 1,4,5 trisphosphate receptor; Protein kinase; Protein phosphatase

Indexed keywords

BINDING PROTEIN; CALCIUM; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CALCIUM CHANNEL; CYCLIC AMP DEPENDENT PROTEIN KINASE; INOSITOL 1,4,5 TRISPHOSPHATE RECEPTOR; PHOSPHOPROTEIN PHOSPHATASE; PROTEIN BCL 2; PROTEIN KINASE B; PROTEIN KINASE C; PROTEIN TYROSINE KINASE; RHO KINASE;

CALCIUM CELL LEVEL; CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL CYCLE; CELL DEATH; CELL DIFFERENTIATION; CELL DIVISION; CELL MEMBRANE; CELL METABOLISM; CELL MIGRATION; CELL SECRETION; CELL STIMULATION; FERTILIZATION; HUMAN; INFORMATION PROCESSING; MUSCLE CONTRACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEPHOSPHORYLATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN SECRETION; PROTEIN STRUCTURE; REGULATORY MECHANISM; REVIEW;

ANIMALS; CALCIUM; CALCIUM SIGNALING; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CYCLIC AMP-DEPENDENT PROTEIN KINASES; CYCLIC GMP-DEPENDENT PROTEIN KINASES; CYCLIN-DEPENDENT KINASES; HUMANS; INOSITOL 1,4,5-TRISPHOSPHATE; INOSITOL 1,4,5-TRISPHOSPHATE RECEPTORS; LECTINS, C-TYPE; MEMBRANE PROTEINS; PHOSPHORYLATION; PROTEIN KINASE C; PROTEIN-TYROSINE KINASES; PROTO-ONCOGENE PROTEINS C-AKT; PROTO-ONCOGENE PROTEINS C-BCL-2; RHO-ASSOCIATED KINASES;

EID: 67349180713     PISSN: 01674889     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2008.12.003     Document Type: Review

References (198)

1. Berridge M.J. Inositol trisphosphate and calcium signalling. Nature 361 (1993) 315-325
2. Berridge M.J., Lipp P., and Bootman M.D. The versatility and universality of calcium signalling. Nat. Rev. Mol Cell. Biol. 1 (2000) 11-21
3. 2+ release channels. Physiol. Rev. 87 (2007) 593-658
4. 3 receptor. Biochim. Biophys. Acta 1742 (2004) 89-102
5. 3 receptor subtypes. EMBO J. 18 (1999) 1303-1308
6. 3 receptor isoforms. Biochem. J. 346 (2000) 275-280
7. Iwai M., Michikawa T., Bosanac I., Ikura M., and Mikoshiba K. Molecular basis of the isoform-specific ligand-binding affinity of inositol 1,4,5-trisphosphate receptors. J. Biol. Chem. 282 (2007) 12755-12764
8. Missiaen L., De Smedt H., Parys J.B., Sienaert I., Vanlingen S., and Casteels R. Threshold for inositol 1,4,5-trisphosphate action. J. Biol. Chem. 271 (1996) 12287-12293
9. Maes K., Missiaen L., De Smet P., Vanlingen S., Callewaert G., Parys J.B., and De Smedt H. Differential modulation of inositol 1,4,5-trisphosphate receptor type 1 and type 3 by ATP. Cell Calcium 27 (2000) 257-267
10. Maes K., Missiaen L., Parys J.B., De Smet P., Sienaert I., Waelkens E., Callewaert G., and De Smedt H. Mapping of the ATP-binding sites on inositol 1,4,5-trisphosphate receptor type 1 and type 3 homotetramers by controlled proteolysis and photoaffinity labeling. J. Biol. Chem. 276 (2001) 3492-3497
11. 3 receptors. J. Gen. Physiol. 117 (2001) 435-446
12. Vanlingen S., Sipma H., De Smet P., Callewaert G., Missiaen L., De Smedt H., and Parys J.B. Modulation of inositol 1,4,5-trisphosphate binding to the various inositol 1,4,5-trisphosphate receptor isoforms by thimerosal and cyclic ADP-ribose. Biochem. Pharmacol. 61 (2001) 803-809
13. Tu H., Wang Z., and Bezprozvanny I. Modulation of mammalian inositol 1,4,5-trisphosphate receptor isoforms by calcium: a role of calcium sensor region. Biophys. J. 88 (2005) 1056-1069
14. Tu H., Wang Z., Nosyreva E., De Smedt H., and Bezprozvanny I. Functional characterization of mammalian inositol 1,4,5-trisphosphate receptor isoforms. Biophys. J. 88 (2005) 1046-1055
15. 3R: Differing ATP sensitivities and molecular determinants of action. J. Biol. Chem. 283 (2008) 21579-21587
16. Sato C., Hamada K., Ogura T., Miyazawa A., Iwasaki K., Hiroaki Y., Tani K., Terauchi A., Fujiyoshi Y., and Mikoshiba K. Inositol 1,4,5-trisphosphate receptor contains multiple cavities and L-shaped ligand-binding domains. J. Mol. Biol. 336 (2004) 155-164
17. Hamada K., Miyata T., Mayanagi K., Hirota J., and Mikoshiba K. Two-state conformational changes in inositol 1,4,5-trisphosphate receptor regulated by calcium. J. Biol. Chem. 277 (2002) 21115-21118
18. Patterson R.L., Boehning D., and Snyder S.H. Inositol 1,4,5-trisphosphate receptors as signal integrators. Annu. Rev. Biochem. 73 (2004) 437-465
19. Bezprozvanny I. The inositol 1,4,5-trisphosphate receptors. Cell Calcium 38 (2005) 261-272
20. Vermassen E., Parys J.B., and Mauger J.P. Subcellular distribution of the inositol 1,4,5-trisphosphate receptors: functional relevance and molecular determinants. Biol. Cell 96 (2004) 3-17
21. 3 binding to the receptor. J. Biol. Chem. 278 (2003) 10602-10612
22. Devogelaere B., Sammels E., and De Smedt H. The IRBIT domain adds new functions to the AHCY family. Bioessays 30 (2008) 642-652
23. Gomi T., Takusagawa F., Nishizawa M., Agussalim B., Usui I., Sugiyama E., Taki H., Shinoda K., Hounoki H., Miwa T., Tobe K., Kobayashi M., Ishimoto T., Ogawa H., and Mori H. Cloning, bacterial expression, and unique structure of adenosylhomocysteine hydrolase-like protein 1, or inositol 1,4,5-triphosphate receptor-binding protein from mouse kidney. Biochim. Biophys. Acta 1784 (2008) 1786-1794
24. 3 receptor: determinants and functional effects. Biochem. Biophys. Res. Commun. 343 (2006) 49-56
25. Ashworth R., Devogelaere B., Fabes J., Tunwell R.E., Koh K.R., De Smedt H., and Patel S. Molecular and functional characterization of inositol trisphosphate receptors during early zebrafish development. J. Biol. Chem. 282 (2007) 13984-13993
26. Cooper B.J., Key B., Carter A., Angel N.Z., Hart D.N., and Kato M. Suppression and overexpression of adenosylhomocysteine hydrolase-like protein 1 (AHCYL1) influences zebrafish embryo development: a possible role for AHCYL1 in inositol phospholipid signaling. J. Biol. Chem. 281 (2006) 22471-22484
27. Devogelaere B., Beullens M., Sammels E., Derua R., Waelkens E., Van Lint J., Parys J.B., Missiaen L., Bollen M., and De Smedt H. Protein phosphatase-1 is a novel regulator of the interaction between IRBIT and the inositol 1,4,5-trisphosphate receptor. Biochem. J. 407 (2007) 303-311
28. 3 receptor. Mol. Cell 22 (2006) 795-806
29. Collins M.O., Yu L., Coba M.P., Husi H., Campuzano I., Blackstock W.P., Choudhary J.S., and Grant S.G. Proteomic analysis of in vivo phosphorylated synaptic proteins. J. Biol. Chem. 280 (2005) 5972-5982
30. Tang T.S., Tu H., Wang Z., and Bezprozvanny I. Modulation of type 1 inositol (1,4,5)-trisphosphate receptor function by protein kinase A and protein phosphatase 1α. J. Neurosci. 23 (2003) 403-415
31. Tu H., Tang T.S., Wang Z., and Bezprozvanny I. Association of type 1 inositol 1,4,5-trisphosphate receptor with AKAP9 (Yotiao) and protein kinase A. J. Biol. Chem. 279 (2004) 19375-19382
32. 2+ signalling in apoptotic cell death. Calcium Binding Proteins 2 (2007) 21-29
33. 2+ and calmodulin. J. Biol. Chem. 274 (1999) 12157-12162
34. Sienaert I., Nadif Kasri N., Vanlingen S., Parys J.B., Callewaert G., Missiaen L., and De Smedt H. Localization and function of a calmodulin-apocalmodulin-binding domain in the N-terminal part of the type 1 inositol 1,4,5-trisphosphate receptor. Biochem. J. 365 (2002) 269-277
35. - cotransporter 1 (pNBC1). Proc. Natl. Acad. Sci. USA 103 (2006) 9542-9547
36. Youle R.J., and Strasser A. The BCL-2 protein family: opposing activities that mediate cell death. Nat. Rev. Mol. Cell Biol. 9 (2008) 47-59
37. Oakes S.A., Lin S.S., and Bassik M.C. The control of endoplasmic reticulum-initiated apoptosis by the BCL-2 family of proteins. Curr. Mol. Med. 6 (2006) 99-109
38. 2+ release and beyond. Apoptosis 12 (2007) 951-968
39. 3 receptor interaction to reverse Bcl-2's inhibition of apoptotic calcium signals. Mol. Cell 31 (2008) 255-265
40. 3R. Nat. Cell Biol. 7 (2005) 1021-1028
41. Chen R., Valencia I., Zhong F., McColl K.S., Roderick H.L., Bootman M.D., Berridge M.J., Conway S.J., Holmes A.B., Mignery G.A., Velez P., and Distelhorst C.W. Bcl-2 functionally interacts with inositol 1,4,5-trisphosphate receptors to regulate calcium release from the ER in response to inositol 1,4,5-trisphosphate. J. Cell Biol. 166 (2004) 193-203
42. L modulation of mammalian inositol 1,4,5-trisphosphate receptor channel isoform gating. Proc. Natl. Acad. Sci. USA 104 (2007) 12565-12570
43. 2+ signals according to the strength of T cell receptor activation. J. Cell Biol. 172 (2006) 127-137
44. Rong Y.P., and Distelhorst C.W. Bcl-2 protein family members: versatile regulators of calcium signaling in cell survival and apoptosis. Annu. Rev. Physiol. 70 (2008) 73-91
45. 2+ transfer in the control of apoptosis. Oncogene 27 (2008) 6407-6418
46. Rong Y.P., Barr P., Yee V.C., and Distelhorst C.W. Targeting Bcl-2 based on the interaction of its BH4 domain with the inositol 1,4,5-trisphosphate receptor. Biochim. Biophys. Acta 1793 (2009) 971-978
47. Basu A., DuBois G., and Haldar S. Posttranslational modifications of Bcl2 family members - a potential therapeutic target for human malignancy. Front. Biosci. 11 (2006) 1508-1521
48. Vantieghem A., Xu Y., Assefa Z., Piette J., Vandenheede J.R., Merlevede W., de Witte P.A., and Agostinis P. Phosphorylation of Bcl-2 in G2/M phase-arrested cells following photodynamic therapy with hypericin involves a CDK1-mediated signal and delays the onset of apoptosis. J. Biol. Chem. 277 (2002) 37718-37731
49. L and Bcl-2. EMBO J. 16 (1997) 968-977
50. Haldar S., Basu A., and Croce C.M. Serine-70 is one of the critical sites for drug-induced Bcl2 phosphorylation in cancer cells. Cancer Res. 58 (1998) 1609-1615
51. Srivastava R.K., Mi Q.S., Hardwick J.M., and Longo D.L. Deletion of the loop region of Bcl-2 completely blocks paclitaxel-induced apoptosis. Proc. Natl. Acad. Sci. USA 96 (1999) 3775-3780
52. Yamamoto K., Ichijo H., and Korsmeyer S.J. BCL-2 is phosphorylated and inactivated by an ASK1/Jun N-terminal protein kinase pathway normally activated at G(2)/M. Mol. Cell. Biol. 19 (1999) 8469-8478
53. Shitashige M., Toi M., Yano T., Shibata M., Matsuo Y., and Shibasaki F. Dissociation of Bax from a Bcl-2/Bax heterodimer triggered by phosphorylation of serine 70 of Bcl-2. J. Biochem. 130 (2001) 741-748
54. 2+ homeostasis and apoptosis. EMBO J. 23 (2004) 1207-1216
55. α12 stimulates apoptosis in epithelial cells through JNK1-mediated Bcl-2 degradation and up-regulation of IκBα. J. Biol. Chem. 282 (2007) 24352-24363
56. Shibasaki F., Kondo E., Akagi T., and McKeon F. Suppression of signalling through transcription factor NF-AT by interactions between calcineurin and Bcl-2. Nature 386 (1997) 728-731
57. Srivastava R.K., Sasaki C.Y., Hardwick J.M., and Longo D.L. Bcl-2-mediated drug resistance: inhibition of apoptosis by blocking nuclear factor of activated T lymphocytes (NFAT)-induced Fas ligand transcription. J. Exp. Med. 190 (1999) 253-265
58. Erin N., Bronson S.K., and Billingsley M.L. Calcium-dependent interaction of calcineurin with Bcl-2 in neuronal tissue. Neuroscience 117 (2003) 541-555
59. Erin N., Lehman R.A., Boyer P.J., and Billingsley M.L. In vitro hypoxia and excitotoxicity in human brain induce calcineurin-Bcl-2 interactions. Neuroscience 117 (2003) 557-565
60. Erin N., and Billingsley M.L. Domoic acid enhances Bcl-2-calcineurin-inositol-1,4,5-trisphosphate receptor interactions and delayed neuronal death in rat brain slices. Brain Res. 1014 (2004) 45-52
61. 2+ flux. Cell 83 (1995) 463-472
62. Cameron A.M., Nucifora F.C., Fung E.T., Livingston D.J., Aldape R.A., Ross C.A., and Snyder S.H. FKBP12 binds the inositol 1,4,5-trisphosphate receptor at leucine-proline (1400-1401) and anchors calcineurin to this FK506-like domain. J. Biol. Chem. 272 (1997) 27582-27588
63. Kanoh S., Kondo M., Tamaoki J., Shirakawa H., Aoshiba K., Miyazaki S., Kobayashi H., Nagata N., and Nagai A. Effect of FK506 on ATP-induced intracellular calcium oscillations in cow tracheal epithelium. Am. J. Physiol. 276 (1999) L891-L899
64. 2+ accumulation mechanisms. J. Physiol. (Lond.) 525 (2000) 681-693
65. Bultynck G., De Smet P., Rossi D., Callewaert G., Missiaen L., Sorrentino V., De Smedt H., and Parys J.B. Characterization and mapping of the 12 kDa FK506-binding protein (FKBP12)-binding site on different isoforms of the ryanodine receptor and of the inositol 1,4,5-trisphosphate receptor. Biochem. J. 354 (2001) 413-422
66. Carmody M., Mackrill J.J., Sorrentino V., and O'Neill C. FKBP12 associates tightly with the skeletal muscle type 1 ryanodine receptor, but not with other intracellular calcium release channels. FEBS Lett. 505 (2001) 97-102
67. 2+ release by mTOR and calcineurin. J. Cell Sci. 118 (2005) 5443-5451
68. 2+-release channels: regulation or association?. Biochem. Biophys. Res. Commun. 311 (2003) 1181-1193
69. 3-mediated calcium release and apoptosis by Bcl-2 involves the participation of protein phosphatase 1. Mol. Cell. Biochem. 295 (2007) 153-165
70. Lin S.S., Bassik M.C., Suh H., Nishino M., Arroyo J.D., Hahn W.C., Korsmeyer S.J., and Roberts T.M. PP2A regulates BCL-2 phosphorylation and proteasome-mediated degradation at the endoplasmic reticulum. J. Biol. Chem. 281 (2006) 23003-23012
71. Oakes S.A., Scorrano L., Opferman J.T., Bassik M.C., Nishino M., Pozzan T., and Korsmeyer S.J. Proapoptotic BAX and BAK regulate the type 1 inositol trisphosphate receptor and calcium leak from the endoplasmic reticulum. Proc. Natl. Acad. Sci. USA 102 (2005) 105-110
72. 2+ release by cAMP-dependent protein kinase. A mechanism for agonist-specific calcium signaling?. Cell Calcium 25 (1999) 219-226
73. Pieper A.A., Brat D.J., O'Hearn E., Krug D.K., Kaplin A.I., Takahashi K., Greenberg J.H., Ginty D., Molliver M.E., and Snyder S.H. Differential neuronal localizations and dynamics of phosphorylated and unphosphorylated type 1 inositol 1,4,5-trisphosphate receptors. Neuroscience 102 (2001) 433-444
74. Walaas S.I., Nairn A.C., and Greengard P. Regional distribution of calcium- and cyclic adenosine 3':5'-monophosphate-regulated protein phosphorylation systems in mammalian brain. I. Particulate systems. J. Neurosci. 3 (1983) 291-301
75. 14C-leucine and phosphorylation. Dev. Neurosci. 7 (1985) 179-187
76. Walaas S.I., Nairn A.C., and Greengard P. PCPP-260, a Purkinje cell-specific cyclic AMP-regulated membrane phosphoprotein of Mr 260,000. J. Neurosci. 6 (1986) 954-961
77. Supattapone S., Danoff S.K., Theibert A., Joseph S.K., Steiner J., and Snyder S.H. Cyclic AMP-dependent phosphorylation of a brain inositol trisphosphate receptor decreases its release of calcium. Proc. Natl. Acad. Sci. USA 85 (1988) 8747-8750
78. 2+/calmodulin-dependent protein kinase II. J. Neurochem. 53 (1989) 917-923
79. 2+ release from platelet internal membranes is regulated by differential phosphorylation. Biochemistry 35 (1996) 6865-6871
80. - inositol 1,4,5-trisphosphate receptor defines susceptibility to phosphorylation by protein kinase A. J. Biol. Chem. 281 (2006) 17410-17419
81. Ferris C.D., Cameron A.M., Bredt D.S., Huganir R.L., and Snyder S.H. Inositol 1,4,5-trisphosphate receptor is phosphorylated by cyclic AMP-dependent protein kinase at serines 1755 and 1589. Biochem. Biophys. Res. Commun. 175 (1991) 192-198
82. Danoff S.K., Ferris C.D., Donath C., Fischer G.A., Munemitsu S., Ullrich A., Snyder S.H., and Ross C.A. Inositol 1,4,5-trisphosphate receptors: distinct neuronal and nonneuronal forms derived by alternative splicing differ in phosphorylation. Proc. Natl. Acad. Sci. USA 88 (1991) 2951-2955
83. 2+ signaling. J. Cell Biol. 169 (2005) 657-667
84. 2+ flux in reconstituted lipid vesicles. J. Biol. Chem. 269 (1994) 6735-6742
85. - splice variants. J. Biol. Chem. 278 (2003) 45811-45817
86. Wagner II L.E., Li W.H., Joseph S.K., and Yule D.I. Functional consequences of phosphomimetic mutations at key cAMP-dependent protein kinase phosphorylation sites in the type 1 inositol 1,4,5-trisphosphate receptor. J. Biol. Chem. 279 (2004) 46242-46252
87. Wagner L.E., Joseph S.K., and Yule D.I. Regulation of single inositol 1,4,5-trisphosphate receptor channel activity by protein kinase A phosphorylation. J. Physiol. (Lond.) 586 (2008) 3577-3596
88. Lin C., Widjaja J., and Joseph S.K. The interaction of calmodulin with alternatively spliced isoforms of the type-I inositol trisphosphate receptor. J. Biol. Chem. 275 (2000) 2305-2311
89. Jang D.J., Guo M., and Wang D. Proteomic and biochemical studies of calcium- and phosphorylation-dependent calmodulin complexes in mammalian cells. J. Proteome Res. 6 (2007) 3718-3728
90. Wojcikiewicz R.J., and Luo S.G. Phosphorylation of inositol 1,4,5-trisphosphate receptors by cAMP-dependent protein kinase. Type I, II, and III receptors are differentially susceptible to phosphorylation and are phosphorylated in intact cells. J. Biol. Chem. 273 (1998) 5670-5677
91. 2+ signaling. J. Biol. Chem. 277 (2002) 1340-1348
92. 2+ release in AR4-2J cells. J. Cell. Biochem. 101 (2007) 609-618
93. LeBeau A.P., Yule D.I., Groblewski G.E., and Sneyd J. Agonist-dependent phosphorylation of the inositol 1,4,5-trisphosphate receptor: A possible mechanism for agonist-specific calcium oscillations in pancreatic acinar cells. J. Gen. Physiol. 113 (1999) 851-872
94. 2+ signals. J. Biol. Chem. 275 (2000) 33704-33711
95. Straub S.V., Giovannucci D.R., Bruce J.I., and Yule D.I. A role for phosphorylation of inositol 1,4,5-trisphosphate receptors in defining calcium signals induced by peptide agonists in pancreatic acinar cells. J. Biol. Chem. 277 (2002) 31949-31956
96. 3 receptors. Biochem. Biophys. Res. Commun. 302 (2003) 121-126
97. 2+ release activity of the inositol 1,4,5-trisphosphate receptor type 3 in RINm5F cells. Biol. Cell 99 (2007) 379-388
98. Soulsby M.D., and Wojcikiewicz R.J. The type III inositol 1,4,5-trisphosphate receptor is phosphorylated by cAMP-dependent protein kinase at three sites. Biochem. J. 392 (2005) 493-497
99. Soulsby M.D., and Wojcikiewicz R.J. Calcium mobilization via type III inositol 1,4,5-trisphosphate receptors is not altered by PKA-mediated phosphorylation of serines 916, 934, and 1832. Cell Calcium 42 (2007) 261-270
100. Scott J.D. Cyclic nucleotide-dependent protein kinases. Pharmacol. Ther. 50 (1991) 123-145
101. Komalavilas P., and Lincoln T.M. Phosphorylation of the inositol 1,4,5-trisphosphate receptor by cyclic GMP-dependent protein kinase. J. Biol. Chem. 269 (1994) 8701-8707
102. Koga T., Yoshida Y., Cai J.Q., Islam M.O., and Imai S. Purification and characterization of 240-kDa cGMP-dependent protein kinase substrate of vascular smooth muscle. Close resemblance to inositol 1,4,5-trisphosphate receptor. J. Biol. Chem. 269 (1994) 11640-11647
103. Komalavilas P., and Lincoln T.M. Phosphorylation of the inositol 1,4,5-trisphosphate receptor. Cyclic GMP-dependent protein kinase mediates cAMP and cGMP dependent phosphorylation in the intact rat aorta. J. Biol. Chem. 271 (1996) 21933-21938
104. 3R-I in vivo by cGMP-dependent protein kinase in smooth muscle. Am. J. Physiol. 284 (2003) G221-G230
105. Haug L.S., Jensen V., Hvalby O., Walaas S.I., and Ostvold A.C. Phosphorylation of the inositol 1,4,5-trisphosphate receptor by cyclic nucleotide-dependent kinases in vitro and in rat cerebellar slices in situ. J. Biol. Chem. 274 (1999) 7467-7473
106. 3 receptor and cGMP kinase Iβ. Nature 404 (2000) 197-201
107. Ammendola A., Geiselhoringer A., Hofmann F., and Schlossmann J. Molecular determinants of the interaction between the inositol 1,4,5-trisphosphate receptor-associated cGMP kinase substrate (IRAG) and cGMP kinase Iβ. J. Biol. Chem. 276 (2001) 24153-24159
108. 2+ release in guinea-pig hepatocytes. Biochem. J. 318 (1996) 849-855
109. 2+ release by preferential activation of cGMP-primed PKG. Am. J. Physiol. 281 (2001) G1238-G1245
110. 2+ release in intact rat megakaryocytes via cGMP- and cAMP-dependent protein kinases. J. Physiol. (Lond.) 512 (1998) 89-96
111. 2+ stores in smooth muscle. Am. J. Physiol. 274 (1998) C1199-C1205
112. 2+/calmodulin-dependent protein kinase II. Biochem. J. 364 (2002) 593-611
113. 2+. In: Pochet R., Donato R., Haiech J., Heizmann C.W., and Gerke V. (Eds). Calcium: the molecular basis of calcium action in biology and medicine (2000), Kluwer Academic Publishers, Dordrecht 179-190
114. 2+. Cell Calcium 32 (2002) 321-334
115. Nadif Kasri N., Bultynck G., Sienaert I., Callewaert G., Erneux C., Missiaen L., Parys J.B., and De Smedt H. The role of calmodulin for inositol 1,4,5-trisphosphate receptor function. Biochim. Biophys. Acta 1600 (2002) 19-31
116. 3 receptor channel gating in native endoplasmic reticulum. Biol. Res. 37 (2004) 513-519
117. 2+ release from inositol trisphosphate-sensitive calcium stores. Pflugers Arch. 432 (1996) 359-367
118. Yamada M., Miyawaki A., Saito K., Nakajima T., Yamamoto Hino M., Ryo Y., Furuichi T., and Mikoshiba K. The calmodulin-binding domain in the mouse type 1 inositol 1,4,5-trisphosphate receptor. Biochem. J. 308 (1995) 83-88
119. 2+-independent inhibition of type-1 inositol trisphosphate receptors. Biochem. J. 334 (1998) 447-455
120. Kasri N.N., Török K., Galione A., Garnham C., Callewaert G., Missiaen L., Parys J.B., and De Smedt H. Endogenously bound calmodulin is essential for the function of the inositol 1,4,5-trisphosphate receptor. J. Biol. Chem. 281 (2006) 8332-8338
121. 2+/calmodulin. J. Biol. Chem. 274 (1999) 13748-13751
122. Michikawa T., Hirota J., Kawano S., Hiraoka M., Yamada M., Furuichi T., and Mikoshiba K. Calmodulin mediates calcium-dependent inactivation of the cerebellar type 1 inositol 1,4,5-trisphosphate receptor. Neuron 23 (1999) 799-808
123. 2+ release mediated by type-1, -2 and -3 inositol trisphosphate receptors. Biochem. J. 345 (2000) 357-363
124. 2+ inhibition in human bronchial mucosal cells. Mol. Pharmacol. 57 (2000) 564-567
125. Sun Y., and Taylor C.W. A calmodulin antagonist reveals a calmodulin-independent interdomain interaction essential for activation of inositol 1,4,5-trisphosphate receptors. Biochem. J. 416 (2008) 243-253
126. Ferris C.D., Huganir R.L., Bredt D.S., Cameron A.M., and Snyder S.H. Inositol trisphosphate receptor: phosphorylation by protein kinase C and calcium calmodulin-dependent protein kinases in reconstituted lipid vesicles. Proc. Natl. Acad. Sci. USA 88 (1991) 2232-2235
127. Colbran R.J., Schworer C.M., Hashimoto Y., Fong Y.L., Rich D.P., Smith M.K., and Soderling T.R. Calcium/calmodulin-dependent protein kinase II. Biochem. J. 258 (1989) 313-325
128. Patel S., Joseph S.K., and Thomas A.P. Molecular properties of inositol 1,4,5-trisphosphate receptors. Cell Calcium 25 (1999) 247-264
129. Doppler H., Storz P., Li J., Comb M.J., and Toker A. A phosphorylation state-specific antibody recognizes Hsp27, a novel substrate of protein kinase D. J. Biol. Chem. 280 (2005) 15013-15019
130. - efflux in Xenopus oocytes. Neurosci. Lett. 129 (1991) 47-50
131. 2+ release. Modification by agonist stimulation. J. Biol. Chem. 268 (1993) 10997-11001
132. 2+ entry by CaMKII inhibitors in bovine vascular endothelial cells. Am. J. Physiol. 289 (2005) C1426-C1436
133. 2+ signaling in bovine vascular endothelial cells. Am. J. Physiol. 293 (2007) C106-C118
134. Zhu D.M., Tekle E., Chock P.B., and Huang C.Y. Reversible phosphorylation as a controlling factor for sustaining calcium oscillations in HeLa cells: Involvement of calmodulin-dependent kinase II and a calyculin A-inhibitable phosphatase. Biochemistry 35 (1996) 7214-7223
135. 2+/calmodulin-dependent protein kinase II mRNA association to polysomes. J. Neurosci. (Online) 20 (2000) RC76
136. 2+ release by CaMKII in Xenopus oocytes. Pflugers Arch. 441 (2001) 796-801
137. 2+ release. FEBS Lett. 449 (1999) 70-74
138. 3. Curr. Mol. Med. 4 (2004) 277-290
139. 2+/calmodulin-dependent protein kinase II antagonism. J. Biol. Chem. 277 (2002) 35061-35070
140. Matovcik L.M., Maranto A.R., Soroka C.J., Gorelick F.S., Smith J., and Goldenring J.R. Co-distribution of calmodulin-dependent protein kinase II and inositol trisphosphate receptors in an apical domain of gastrointestinal mucosal cells. J. Histochem. Cytochem. 44 (1996) 1243-1250
141. Bare D.J., Kettlun C.S., Liang M., Bers D.M., and Mignery G.A. Cardiac type 2 inositol 1,4,5-trisphosphate receptor: interaction and modulation by calcium/calmodulin-dependent protein kinase II. J. Biol. Chem. 280 (2005) 15912-15920
142. 2+ signalling in the mammalian heart. J. Physiol. (Lond.) 584 (2007) 601-611
143. 2+/calmodulin-dependent kinase II mediate acute potentiation of neurotransmitter release by neurotrophin-3. J. Cell Biol. 149 (2000) 783-792
144. 2+ signaling in cardiac myocyte excitation-transcription coupling. J. Clin. Invest. 116 (2006) 675-682
145. West A.E., Griffith E.C., and Greenberg M.E. Regulation of transcription factors by neuronal activity. Nat. Rev. Neurosci. 3 (2002) 921-931
146. Choi J.Y., Beaman-Hall C.M., and Vallano M.L. Granule neurons in cerebellum express distinct splice variants of the inositol trisphosphate receptor that are modulated by calcium. Am. J. Physiol. 287 (2004) C971-C980
147. Newton A.C. Regulation of the ABC kinases by phosphorylation: protein kinase C as a paradigm. Biochem. J. 370 (2003) 361-371
148. 3 rises again... and again. Curr. Biol. 11 (2001) R352-R355
149. Vermassen E., Van Acker K., Annaert W.G., Himpens B., Callewaert G., Missiaen L., De Smedt H., and Parys J.B. Microtubule-dependent redistribution of the type-1 inositol 1,4,5-trisphosphate receptor in A7r5 smooth muscle cells. J. Cell Sci. 116 (2003) 1269-1277
150. rd FEPS Congress (2003), Monduzzi Editore, Bologna 79-82
151. 2+ signalling in rat vascular smooth muscle cells: a role for protein kinase C at physiological vasoconstrictor concentrations of vasopressin. J. Physiol. (Lond.) 524 (2000) 821-831
152. 2+ signals by protein kinase C isozymes. J. Cell Biol. 165 (2004) 223-232
153. Kennelly P.J., and Krebs E.G. Consensus sequences as substrate specificity determinants for protein kinases and protein phosphatases. J. Biol. Chem. 266 (1991) 15555-15558
154. 2+ release. Proc. Natl. Acad. Sci. USA 101 (2004) 2328-2332
155. Matter N., Ritz M.F., Freyermuth S., Rogue P., and Malviya A.N. Stimulation of nuclear protein kinase C leads to phosphorylation of nuclear inositol 1,4,5-trisphosphate receptor and accelerated calcium release by inositol 1,4,5-trisphosphate from isolated rat liver nuclei. J. Biol. Chem. 268 (1993) 732-736
156. Bandyopadhyay A., Shin D.W., and Kim D.H. Regulation of ATP-induced calcium release in COS-7 cells by calcineurin. Biochem. J. 348 (2000) 173-181
157. 2+ oscillations in bovine adrenal glomerulosa cells. Biochemistry 40 (2001) 6486-6492
158. Vermassen E., Fissore R.A., Nadif Kasri N., Vanderheyden V., Callewaert G., Missiaen L., Parys J.B., and De Smedt H. Regulation of the phosphorylation of the inositol 1,4,5-trisphosphate receptor by protein kinase C. Biochem. Biophys. Res. Commun. 319 (2004) 888-893
159. 2+ in pancreatoma AR4-2J cells. J. Endocrinol. 192 (2007) 659-668
160. Caron A.Z., Chaloux B., Arguin G., and Guillemette G. Protein kinase C decreases the apparent affinity of the inositol 1,4,5-trisphosphate receptor type 3 in RINm5F cells. Cell Calcium 42 (2007) 323-331
161. Song G., Ouyang G., and Bao S. The activation of Akt/PKB signaling pathway and cell survival. J. Cell. Mol. Med. 9 (2005) 59-71
162. Sale E.M., and Sale G.J. Protein kinase B: signalling roles and therapeutic targeting. Cell. Mol. Life Sci. 65 (2008) 113-127
163. Distelhorst C.W., and Shore G.C. Bcl-2 and calcium: controversy beneath the surface. Oncogene 23 (2004) 2875-2880
164. Khan M.T., Wagner II L., Yule D.I., Bhanumathy C., and Joseph S.K. Akt kinase phosphorylation of inositol 1,4,5-trisphosphate receptors. J. Biol. Chem. 281 (2006) 3731-3737
165. Assefa Z., Bultynck G., Szlufcik K., Nadif Kasri N., Vermassen E., Goris J., Missiaen L., Callewaert G., Parys J.B., and De Smedt H. Caspase-3-induced truncation of type 1 inositol trisphosphate receptor accelerates apoptotic cell death and induces inositol trisphosphate-independent calcium release during apoptosis. J. Biol. Chem. 279 (2004) 43227-43236
166. 2+ release and apoptosis. Proc. Natl. Acad. Sci. USA 105 (2008) 2427-2432
167. 2+-dependent apoptotic stimuli. Biochem. Biophys. Res. Commun. 375 (2008) 501-505
168. Nigg E.A. Mitotic kinases as regulators of cell division and its checkpoints. Nat. Rev. Mol. Cell Biol. 2 (2001) 21-32
169. Barr F.A., Sillje H.H., and Nigg E.A. Polo-like kinases and the orchestration of cell division. Nat. Rev. Mol. Cell Biol. 5 (2004) 429-440
170. MacCorkle R.A., and Tan T.H. Mitogen-activated protein kinases in cell-cycle control. Cell. Biochem. Biophys. 43 (2005) 451-461
171. Verlhac M.H., Kubiak J.Z., Clarke H.J., and Maro B. Microtubule and chromatin behavior follow MAP kinase activity but not MPF activity during meiosis in mouse oocytes. Development 120 (1994) 1017-1025
172. Pahlavan G., Polanski Z., Kalab P., Golsteyn R., Nigg E.A., and Maro B. Characterization of polo-like kinase 1 during meiotic maturation of the mouse oocyte. Dev. Biol. 220 (2000) 392-400
173. Ledan E., Polanski Z., Terret M.E., and Maro B. Meiotic maturation of the mouse oocyte requires an equilibrium between cyclin B synthesis and degradation. Dev. Biol. 232 (2001) 400-413
174. Mehlmann L.M., and Kline D. Regulation of intracellular calcium in the mouse egg: calcium release in response to sperm or inositol trisphosphate is enhanced after meiotic maturation. Biol. Reprod. 51 (1994) 1088-1098
175. 2+ signalling at fertilization in mammals. Semin. Cell Dev. Biol. 12 (2001) 37-43
176. i oscillations in mouse zygotes and function of the inositol 1,4,5-trisphosphate receptor-1. Dev. Biol. 274 (2004) 94-109
177. i oscillations in mammalian eggs: a multi-pronged approach. Semin. Cell Dev. Biol. 17 (2006) 274-284
178. Kapur N., Mignery G.A., and Banach K. Cell cycle-dependent calcium oscillations in mouse embryonic stem cells. Am. J. Physiol. 292 (2007) C1510-C1518
179. Nigg E.A. The substrates of the cdc2 kinase. Semin. Cell Biol. 2 (1991) 261-270
180. Malathi K., Kohyama S., Ho M., Soghoian D., Li X., Silane M., Berenstein A., and Jayaraman T. Inositol 1,4,5-trisphosphate receptor (type 1) phosphorylation and modulation by cdc2. J. Cell. Biochem. 90 (2003) 1186-1196
181. Li X., Malathi K., Krizanova O., Ondrias K., Sperber K., Ablamunits V., and Jayaraman T. Cdc2/cyclin B1 interacts with and modulates inositol 1,4,5-trisphosphate receptor (type 1) functions. J. Immunol. 175 (2005) 6205-6210
182. Soghoian D., Jayaraman V., Silane M., Berenstein A., and Jayaraman T. Inositol 1,4,5-trisphosphate receptor phosphorylation in breast cancer. Tumour Biol. 26 (2005) 207-212
183. Bai G.R., Yang L.H., Huang X.Y., and Sun F.Z. Inositol 1,4,5-trisphosphate receptor type 1 phosphorylation and regulation by extracellular signal-regulated kinase. Biochem. Biophys. Res. Commun. 348 (2006) 1319-1327
184. i responses at fertilization: a role for the MAP kinase pathway. Development 133 (2006) 4355-4365
185. 3 type 1 receptor and regulates intracellular calcium dynamics in DT40 cells. Biochem. Biophys. Res. Commun. 349 (2006) 1339-1344
186. Fissore R.A., Longo F.J., Anderson E., Parys J.B., and Ducibella T. Differential distribution of inositol trisphosphate receptor isoforms in mouse oocytes. Biol. Reprod. 60 (1999) 49-57
187. Westendorf J.M., Rao P.N., and Gerace L. Cloning of cDNAs for M-phase phosphoproteins recognized by the MPM2 monoclonal antibody and determination of the phosphorylated epitope. Proc. Natl. Acad. Sci. USA 91 (1994) 714-718
188. 2+ channel, is a novel substrate of polo-like kinase 1 in eggs. Dev. Biol. 320 (2008) 402-413
189. Logarinho E., and Sunkel C.E. The Drosophila POLO kinase localises to multiple compartments of the mitotic apparatus and is required for the phosphorylation of MPM2 reactive epitopes. J. Cell Sci. 111 (1998) 2897-2909
190. Nakajima H., Toyoshima-Morimoto F., Taniguchi E., and Nishida E. Identification of a consensus motif for Plk (Polo-like kinase) phosphorylation reveals Myt1 as a Plk1 substrate. J. Biol. Chem. 278 (2003) 25277-25280
191. 2+ signaling during hyaluronan (HA)-induced endothelial cell migration. Cell Motil. Cytoskeleton 53 (2002) 293-316
192. Tsygankov A.Y. Non-receptor protein tyrosine kinases. Front. Biosci. 8 (2003) s595-s635
193. Harnick D.J., Jayaraman T., Ma Y., Mulieri P., Go L.O., and Marks A.R. The human type 1 inositol 1,4,5-trisphosphate receptor from T lymphocytes. Structure, localization, and tyrosine phosphorylation. J. Biol. Chem. 270 (1995) 2833-2840
194. Jayaraman T., Ondrias K., Ondriasova E., and Marks A.R. Regulation of the inositol 1,4,5-trisphosphate receptor by tyrosine phosphorylation. Science 272 (1996) 1492-1494
195. Cui J., Matkovich S.J., deSouza N., Li S., Rosemblit N., and Marks A.R. Regulation of the type 1 inositol 1,4,5-trisphosphate receptor by phosphorylation at tyrosine 353. J. Biol. Chem. 279 (2004) 16311-16316
196. 3 receptor: localization to plasma membrane of T cells and cocapping with the T cell receptor. Science 257 (1992) 815-818
197. deSouza N., Cui J., Dura M., McDonald T.V., and Marks A.R. A function for tyrosine phosphorylation of type 1 inositol 1,4,5-trisphosphate receptor in lymphocyte activation. J. Cell Biol. 179 (2007) 923-934
198. 3 receptor. EMBO J. 21 (2002) 83-92