Intracellular calcium channels: Inositol-1,4,5-trisphosphate receptors

European Journal of Pharmacology

Volumn 739, Issue C, 2014, Pages 39-48

  Fedorenko, Olena A ^a,b   Popugaeva, Elena ^c   Enomoto, Masahiro ^d   Stathopulos, Peter B ^d   Ikura, Mitsuhiko ^d   Bezprozvanny, Ilya ^c,e  

^a BOGOMOLETZ INSTITUTE OF PHYSIOLOGY   (Ukraine)

^b State Key Laboratory for Molecular and Cellular Biology   (Ukraine)

^c PETER THE GREAT ST PETERSBURG POLYTECHNIC UNIVERSITY   (Russian Federation)

^d UNIVERSITY OF TORONTO   (Canada)

^e UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

Ca2+ signaling; Cell nucleus; Inositol 1,4,5 trisphosphate receptors; Neurodegeneration

Indexed keywords

CALCIUM BINDING PROTEIN; CALCIUM BINDING PROTEIN 1; CALCIUM ION; HUNTINGTIN; INOSITOL 1,4,5 TRISPHOSPHATE; INOSITOL 1,4,5 TRISPHOSPHATE RECEPTOR; INOSITOL 1,4,5 TRISPHOSPHATE RECEPTOR TYPE 1; UNCLASSIFIED DRUG;

ALLOSTERISM; ALZHEIMER DISEASE; AMINO TERMINAL SEQUENCE; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL DEATH; CELL DIFFERENTIATION; CELL NUCLEUS MEMBRANE; CELL PROLIFERATION; CHANNEL GATING; CONFORMATIONAL TRANSITION; HUMAN; HUNTINGTON CHOREA; INTRACELLULAR SIGNALING; LEARNING; LIGAND BINDING; LONG TERM MEMORY; NERVE CELL MEMBRANE CONDUCTANCE; NERVE CELL NETWORK; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN TARGETING; REVIEW; SPINOCEREBELLAR DEGENERATION; STRUCTURE ANALYSIS; ANIMAL; BIOPHYSICS; CHEMISTRY; DEGENERATIVE DISEASE; INTRACELLULAR SPACE; METABOLISM;

ANIMALS; BIOPHYSICAL PROCESSES; HUMANS; INOSITOL 1,4,5-TRISPHOSPHATE RECEPTORS; INTRACELLULAR SPACE; NEURODEGENERATIVE DISEASES;

EID: 84924047149     PISSN: 00142999     EISSN: 18790712     Source Type: Journal    
DOI: 10.1016/j.ejphar.2013.10.074     Document Type: Review

References (146)

1. H. Bading Transcription-dependent neuronal plasticity the nuclear calcium hypothesis Eur. J. Biochem. 267 2000 5280 5283
2. K.D. Baker, T.M. Edwards, and N.S. Rickard The role of intracellular calcium stores in synaptic plasticity and memory consolidation Neurosci. Biobehav. Rev. 37 2013 1211 1239
3. S. Bandara, S. Malmersjo, and T. Meyer Regulators of calcium homeostasis identified by inference of kinetic model parameters from live single cells perturbed by siRNA Sci. Signal. 6 2013 ra56
4. N.P. Barrera, B. Morales, and M. Villalon Plasma and intracellular membrane inositol 1,4,5-trisphosphate receptors mediate the Ca(2+) increase associated with the ATP-induced increase in ciliary beat frequency Am. J. Physiol. Cell Physiol. 287 2004 C1114 1124
5. C.P. Bengtson, and H. Bading Nuclear calcium signaling Adv. Exp. Med. Biol. 970 2012 377 405
6. M.J. Berridge Microdomains and elemental events in calcium signalling Cell Calcium 20 1996 95 96
7. M.J. Berridge Elementary and global aspects of calcium signalling J. Exp. Biol. 200 1997 315 319
8. M.J. Berridge Inositol trisphosphate and calcium signalling mechanisms Biochim. Biophys. Acta 1793 2009 933 940
9. M.J. Berridge Calcium signalling remodelling and disease Biochem. Soc. Trans. 40 2012 297 309
10. M.J. Berridge, M.D. Bootman, and P. Lipp Calcium - a life and death signal Nature 395 1998 645 648
11. I. Bezprozvanny The inositol 1,4,5-trisphosphate receptors Cell Calcium 38 2005 261 272
12. I. Bezprozvanny Calcium signaling and neurodegenerative diseases Trends Mol. Med. 15 2009 89 100
13. I. Bezprozvanny Role of inositol 1,4,5-trisphosphate receptors in pathogenesis of Huntington's disease and spinocerebellar ataxias Neurochem. Res. 36 2011 1186 1197
14. I. Bezprozvanny, and B.E. Ehrlich ATP modulates the function of inositol 1,4,5-trisphosphate-gated channels at two sites Neuron 10 1993 1175 1184
15. I. Bezprozvanny, and B.E. Ehrlich Inositol (1,4,5)-trisphosphate (InsP3)-gated Ca channels from cerebellum: conduction properties for divalent cations and regulation by intraluminal calcium J. Gen. Physiol. 104 1994 821 856
16. I. Bezprozvanny, and T. Klockgether Therapeutic prospects for spinocerebellar ataxia type 2 and 3 Drugs Future 34 2010 991 999
17. I. Bezprozvanny, and M.P. Mattson Neuronal calcium mishandling and the pathogenesis of Alzheimer's disease Trends Neurosci. 31 2008 454 463
18. I. Bezprozvanny, J. Watras, and B.E. Ehrlich Bell-shaped calcium-response curves of Ins(1,4,5)P3- and calcium-gated channels from endoplasmic reticulum of cerebellum Nature 351 1991 751 754
19. D. Boehning, S.K. Joseph, D.O. Mak, and J.K. Foskett Single-channel recordings of recombinant inositol trisphosphate receptors in mammalian nuclear envelope Biophys. J. 81 2001 117 124
20. M.D. Bootman, P. Lipp, and M.J. Berridge The organisation and functions of local Ca(2+) signals J. Cell Sci. 114 2001 2213 2222
21. I. Bosanac, J.R. Alattia, T.K. Mal, J. Chan, S. Talarico, F.K. Tong, K.I. Tong, F. Yoshikawa, T. Furuichi, M. Iwai, T. Michikawa, K. Mikoshiba, and M. Ikura Structure of the inositol 1,4,5-trisphosphate receptor binding core in complex with its ligand Nature 420 2002 696 700
22. I. Bosanac, H. Yamazaki, T. Matsu-Ura, T. Michikawa, K. Mikoshiba, and M. Ikura Crystal structure of the ligand binding suppressor domain of type 1 inositol 1,4,5-trisphosphate receptor Mol. Cell 17 2005 193 203
23. K.M. Carlson, J.M. Andresen, and H.T. Orr Emerging pathogenic pathways in the spinocerebellar ataxias Curr. Opin. Genet. Dev. 19 2009 247 253
24. J. Chan, H. Yamazaki, N. Ishiyama, M.D. Seo, T.K. Mal, T. Michikawa, K. Mikoshiba, and M. Ikura Structural studies of inositol 1,4,5-trisphosphate receptor: coupling ligand binding to channel gating J. Biol. Chem. 285 2010 36092 36099
25. R. Chen, I. Valencia, F. Zhong, K.S. McColl, H.L. Roderick, M.D. Bootman, M.J. Berridge, S.J. Conway, A.B. Holmes, G.A. Mignery, P. Velez, and C.W. Distelhorst 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
26. X. Chen, J. Wu, S. Lvovskaya, E. Herndon, C. Supnet, and I. Bezprozvanny Dantrolene is neuroprotective in Huntington's disease transgenic mouse model Mol. Neurodegener. 6 2011 81
27. K.H. Cheung, L. Mei, D.O. Mak, I. Hayashi, T. Iwatsubo, D.E. Kang, and J.K. Foskett Gain-of-function enhancement of IP3 receptor modal gating by familial Alzheimer's disease-linked presenilin mutants in human cells and mouse neurons Sci. Signal. 3 2010 ra22
28. 2+ disruption in Alzheimer's disease by presenilin regulation of InsP(3) receptor channel gating Neuron 58 2008 871 883
29. P.C. da Fonseca, S.A. Morris, E.P. Nerou, C.W. Taylor, and E.P. Morris Domain organization of the type 1 inositol 1,4,5-trisphosphate receptor as revealed by single-particle analysis Proc. Natl. Acad. Sci. USA 100 2003 3936 3941
30. E. Decrock, M. De Bock, N. Wang, A.K. Gadicherla, M. Bol, T. Delvaeye, P. Vandenabeele, M. Vinken, G. Bultynck, D.V. Krysko, and L. Leybaert IP3, a small molecule with a powerful message Biochim. Biophys. Acta 1833 2013 1772 1786
31. 2+ entry through plasma membrane IP3 receptors Science 313 2006 229 233
32. N. DeSouza, S. Reiken, K. Ondrias, Y.M. Yang, S. Matkovich, and A.R. Marks Protein kinase A and two phosphatases are components of the inositol 1,4,5-trisphosphate receptor macromolecular signaling complex J. Biol. Chem. 277 2002 39397 39400
33. G.D. Dickinson, D. Swaminathan, and I. Parker The probability of triggering calcium puffs is linearly related to the number of inositol trisphosphate receptors in a cluster Biophys. J. 102 2012 1826 1836
34. O.A. Fedorenko, DIe Duzhy, and S.M. Marchenko Nuclear ionic channels of the granule cells from the dentate gyrus Fiziol Zh 53 2007 9 15
35. O.A. Fedorenko, DIe Duzhy, and S.M. Marchenko Calcium channels in the nuclear envelope of pyramidal neurons of the hippocampus Neurophysiology 40 2008 238 242
36. C.D. Ferris, R.L. Huganir, D.S. Bredt, A.M. Cameron, and S.H. Snyder 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
37. C.D. Ferris, R.L. Huganir, and S.H. Snyder Calcium flux mediated by purified inositol 1,4,5-trisphosphate receptor in reconstituted lipid vesicles is allosterically regulated by adenine nucleotides Proc. Natl. Acad. Sci. USA 87 1990 2147 2151
38. C.D. Ferris, R.L. Huganir, S. Supattapone, and S.H. Snyder Purified inositol 1,4,5-trisphosphate receptor mediates calcium flux in reconstituted lipid vesicles Nature 342 1989 87 89
39. A. Filla, G. De Michele, L. Santoro, O. Calabrese, I. Castaldo, S. Giuffrida, D. Restivo, L. Serlenga, D.F. Condorelli, U. Bonuccelli, R. Scala, G. Coppola, G. Caruso, and S. Cocozza Spinocerebellar ataxia type 2 in southern Italy: a clinical and molecular study of 30 families J. Neurol. 246 1999 467 471
40. E.A. Finch, T.J. Turner, and S.M. Goldin Calcium as a coagonist of inositol 1,4,5-trisphosphate-induced calcium release Science 252 1991 443 446
41. 2+ Release Channels Physiol. Rev. 87 2007 593 658
42. T. Furuichi, K. Kohda, A. Miyawaki, and K. Mikoshiba Intracellular channels Curr. Opin. Neurobiol. 4 1994 294 303
43. T. Furuichi, S. Yoshikawa, A. Miyawaki, K. Wada, N. Maeda, and K. Mikoshiba Primary structure and functional expression of the inositol 1,4,5-trisphosphate-binding protein P400 Nature 342 1989 32 38
44. D.A. Gomes, M.F. Leite, A.M. Bennett, and M.H. Nathanson Calcium signaling in the nucleus Can. J. Physiol. Pharmacol. 84 2006 325 332
45. P.L. Greer, and M.E. Greenberg From synapse to nucleus: calcium-dependent gene transcription in the control of synapse development and function Neuron 59 2008 846 860
46. K. Hamada, T. Miyata, K. Mayanagi, J. Hirota, and K. Mikoshiba Two-state conformational changes in inositol 1,4,5-trisphosphate receptor regulated by calcium J. Biol. Chem. 277 2002 21115 21118
47. K. Hara, A. Shiga, H. Nozaki, J. Mitsui, Y. Takahashi, H. Ishiguro, H. Yomono, H. Kurisaki, J. Goto, T. Ikeuchi, S. Tsuji, M. Nishizawa, and O. Onodera Total deletion and a missense mutation of ITPR1 in Japanese SCA15 families Neurology 71 2008 547 551
48. L.S. Haug, V. Jensen, O. Hvalby, S.I. Walaas, and A.C. Ostvold 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
49. L.P. Haynes, A.V. Tepikin, and R.D. Burgoyne Calcium-binding protein 1 is an inhibitor of agonist-evoked, inositol 1,4,5-trisphosphate-mediated calcium signaling J. Biol. Chem. 279 2004 547 555
50. T. Higo, K. Hamada, C. Hisatsune, N. Nukina, T. Hashikawa, M. Hattori, T. Nakamura, and K. Mikoshiba Mechanism of ER stress-induced brain damage by IP(3) receptor Neuron 68 2010 865 878
51. D.P. Huynh, K. Figueroa, N. Hoang, and S.M. Pulst Nuclear localization or inclusion body formation of ataxin-2 are not necessary for SCA2 pathogenesis in mouse or human Nat. Genet. 26 2000 44 50
52. 2+ dependence of inositol 1,4,5-trisphosphate-induced Ca release in smooth muscle cells of the guinea pig taenia caeci J. Gen. Physiol. 95 1990 1103 1122
53. M. Iino Effects of adenine nucleotides on inositol 1,4,5-trisphosphate-induced calcium release in vascular smooth muscle cells J. Gen. Physiol. 98 1991 681 698
54. G. Imbert, F. Saudou, G. Yvert, D. Devys, Y. Trottier, J.M. Garnier, C. Weber, J.L. Mandel, G. Cancel, N. Abbas, A. Durr, O. Didierjean, G. Stevanin, Y. Agid, and A. Brice Cloning of the gene for spinocerebellar ataxia 2 reveals a locus with high sensitivity to expanded CAG/glutamine repeats Nat. Genet. 14 1996 285 291
55. 2+ mobilization is altered in fibroblasts from patients with Alzheimer disease Proc. Natl. Acad. Sci. USA 91 1994 534 538
56. A. Iwaki, Y. Kawano, S. Miura, H. Shibata, D. Matsuse, W. Li, H. Furuya, Y. Ohyagi, T. Taniwaki, J. Kira, and Y. Fukumaki Heterozygous deletion of ITPR1, but not SUMF1, in spinocerebellar ataxia type 16 J. Med. Genet. 45 2008 32 35
57. Q.X. Jiang, E.C. Thrower, D.W. Chester, B.E. Ehrlich, and F.J. Sigworth Three-dimensional structure of the type 1 inositol 1,4,5-trisphosphate receptor at 24 A resolution EMBO J. 21 2002 3575 3581
58. L.S. Kaltenbach, E. Romero, R.R. Becklin, R. Chettier, R. Bell, A. Phansalkar, A. Strand, C. Torcassi, J. Savage, A. Hurlburt, G.H. Cha, L. Ukani, C.L. Chepanoske, Y. Zhen, S. Sahasrabudhe, J. Olson, C. Kurschner, L.M. Ellerby, J.M. Peltier, J. Botas, and R.E. Hughes Huntingtin interacting proteins are genetic modifiers of neurodegeneration PLoS Genet. 3 2007 e82
59. 2+ Mol. Pharmacol. 66 2004 276 284
60. 2+-binding proteins EMBO J. 23 2004 312 321
61. A. Kasumu, and I. Bezprozvanny Deranged calcium signaling in purkinje cells and pathogenesis in spinocerebellar ataxia 2 (SCA2) and other ataxias Cerebellum (Lond., Engl.) 11 2012 630 639
62. A.W. Kasumu, X. Liang, P. Egorova, D. Vorontsova, and I. Bezprozvanny Chronic suppression of inositol 1,4,5-triphosphate receptor-mediated calcium signaling in cerebellar purkinje cells alleviates pathological phenotype in spinocerebellar ataxia 2 mice J. Neurosci. 32 2012 12786 12796
63. J.A. Kerner, D.G. Standaert, J.B. Penney Jr., A.B. Young, and G.B. Landwehrmeyer Expression of group one metabotropic glutamate receptor subunit mRNAs in neurochemically identified neurons in the rat neostriatum, neocortex, and hippocampus Brain Res. Mol. Brain Res. 48 1997 259 269
64. 2+ release in rat cerebellar Purkinje neurones J. Physiol. (Lond.) 487 1995 343 358
65. C. Klein, and A.N. Malviya Mechanism of nuclear calcium signaling by inositol 1,4,5-trisphosphate produced in the nucleus, nuclear located protein kinase C and cyclic AMP-dependent protein kinase Front. Biosci. 13 2008 1206 1226
66. P. Komalavilas, and T.M. Lincoln Phosphorylation of the inositol 1,4,5-trisphosphate receptor by cyclic GMP-dependent protein kinase J. Biol. Chem. 269 1994 8701 8707
67. 2+ signals Semin. Cell Dev. Biol. 23 2012 172 180
68. A.K. Lam, and A. Galione The endoplasmic reticulum and junctional membrane communication during calcium signaling Biochim. Biophys. Acta 1833 2013 2542 2559
69. I. Lastres-Becker, U. Rub, and G. Auburger Spinocerebellar ataxia 2 (SCA2) Cerebellum 7 2008 115 124
70. 2+ sensor protein, inhibits inositol trisphosphate receptors by clamping intersubunit interactions Proc. Natl. Acad. Sci. USA 110 2013 8507 8512
71. C.C. Lin, K. Baek, and Z. Lu Apo and InsP(3)-bound crystal structures of the ligand-binding domain of an InsP(3) receptor Nat. Struct. Mol. Biol. 18 2011 1172 1174
72. J. Liu, T.S. Tang, H. Tu, O. Nelson, E. Herndon, D.P. Huynh, S.M. Pulst, and I. Bezprozvanny Deranged calcium signaling and neurodegeneration in spinocerebellar ataxia type 2 J. Neurosci. 29 2009 9148 9162
73. S.J. Ludtke, T.P. Tran, Q.T. Ngo, V.Y. Moiseenkova-Bell, W. Chiu, and I.I. Serysheva Flexible architecture of IP3R1 by Cryo-EM Structure 19 2011 1192 1199
74. D.O. Mak, and J.K. Foskett Single-channel kinetics, inactivation, and spatial distribution of inositol trisphosphate (IP3) receptors in Xenopus oocyte nucleus J. Gen. Physiol. 109 1997 571 587
75. 2+ inhibition Proc. Natl. Acad. Sci. USA 95 1998 15821 15825
76. D.O. Mak, S. McBride, and J.K. Foskett ATP regulation of type 1 inositol 1,4,5-trisphosphate receptor channel gating by allosteric tuning of Ca(2+) activation J. Biol. Chem. 274 1999 22231 22237
77. L. Mao, and J.Q. Wang Upregulation of preprodynorphin and preproenkephalin mRNA expression by selective activation of group I metabotropic glutamate receptors in characterized primary cultures of rat striatal neurons Brain Res. Mol. Brain Res. 86 2001 125 137
78. L. Mao, and J.Q. Wang Glutamate cascade to cAMP response element-binding protein phosphorylation in cultured striatal neurons through calcium-coupled group I metabotropic glutamate receptors Mol. Pharmacol. 62 2002 473 484
79. S.M. Marchenko, V.V. Yarotskyy, T.N. Kovalenko, P.G. Kostyuk, and R.C. Thomas Spontaniously active and InsP3-activated ion channels in cell nuclei from rat cerebellar Purkinje and granule neurons J. Physiol. 563 2005 897 910
80. A. Matilla-Duenas, I. Sanchez, M. Corral-Juan, A. Davalos, R. Alvarez, and P. Latorre Cellular and molecular pathways triggering neurodegeneration in the spinocerebellar ataxias Cerebellum 10 2010 148 166
81. M. Matsumoto, T. Nakagawa, T. Inoue, E. Nagata, K. Tanaka, H. Takano, O. Minowa, J. Kuno, S. Sakakibara, M. Yamada, H. Yoneshima, A. Miyawaki, Y. Fukuuchi, T. Furuichi, H. Okano, K. Mikoshiba, and T. Noda Ataxia and epileptic seizures in mice lacking type 1 inositol 1,4,5-trisphosphate receptor Nature 379 1996 168 171
82. A. Maximov, T.-S. Tang, and I. Bezprozvanny Association of the type 1 inositol (1,4,5)-trisphosphate receptor with 4.1N protein in neurons Mol. Cell. Neurosci. 22 2003 271 283
83. 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
84. G.A. Mignery, C.L. Newton, B.T. Archer, and T.C. Sudhof Structure and expression of the rat inositol 1,4,5-trisphosphate receptor J. Biol. Chem. 265 1990 12679 12685
85. G.A. Mignery, and T.C. Sudhof The ligand binding site and transduction mechanism in the inositol-1,4,5-triphosphate receptor EMBO J. 9 1990 3893 3898
86. 2+ channel: from discovery to new signaling concepts J. Neurochem. 102 2007 1426 1446
87. K. Mikoshiba The discovery and structural investigation of the IP(3) receptor and the associated IRBIT protein Adv. Exp. Med. Biol. 740 2012 281 304
88. A. Miyawaki, T. Furuichi, Y. Ryou, S. Yoshikawa, T. Nakagawa, T. Saitoh, and K. Mikoshiba Structure-function relationships of the mouse inositol 1,4,5-trisphosphate receptor Proc. Natl. Acad. Sci. USA 88 1991 4911 4915
89. S.C. Murray, J. Flanagan, O.B. Popova, W. Chiu, S.J. Ludtke, and I.I. Serysheva Validation of cryo-EM structure of IP(3)R1 channel Structure 21 2013 900 909
90. 2+ leak function of presenilin 1 J. Clin. Invest. 117 2007 1230 1239
91. A.B. Parekh, and S. Muallem Ca(2+) signalling and gene regulation Cell Calcium 49 2011 279
92. 2+ transients associated with openings of inositol trisphosphate-gated channels in Xenopus oocytes J. Physiol. (Lond.) 491 1996 663 668
93. S.M. Pulst, A. Nechiporuk, T. Nechiporuk, S. Gispert, X.N. Chen, I. Lopes-Cendes, S. Pearlman, S. Starkman, G. Orozco-Diaz, A. Lunkes, P. DeJong, G.A. Rouleau, G. Auburger, J.R. Korenberg, C. Figueroa, and S. Sahba Moderate expansion of a normally biallelic trinucleotide repeat in spinocerebellar ataxia type 2 Nat. Genet. 14 1996 269 276
94. S.M. Pulst, N. Santos, D. Wang, H. Yang, D. Huynh, L. Velazquez, and K.P. Figueroa Spinocerebellar ataxia type 2: polyQ repeat variation in the CACNA1A calcium channel modifies age of onset Brain 128 2005 2297 2303
95. T. Rahman Dynamic clustering of IP3 receptors by IP3 Biochem. Soc. Trans. 40 2012 325 330
96. T. Rahman, and C.W. Taylor Dynamic regulation of IP3 receptor clustering and activity by IP3 Channels (Austin) 3 2009 226 232
97. M.A. Rodrigues, D.A. Gomes, M.H. Nathanson, and M.F. Leite Nuclear calcium signaling: a cell within a cell Braz. J. Med. Biol. Res. 42 2009 17 20
98. C.A. Ross, J. Meldolesi, T.A. Milner, T. Satoh, S. Supattapone, and S.H. Snyder Inositol 1,4,5-trisphosphate receptor localized to endoplasmic reticulum in cerebellar Purkinje neurons Nature 339 1989 468 470
99. A.M. Rossi, A.M. Riley, S.C. Tovey, T. Rahman, O. Dellis, E.J. Taylor, V.G. Veresov, B.V. Potter, and C.W. Taylor Synthetic partial agonists reveal key steps in IP3 receptor activation Nat. Chem. Biol. 5 2009 631 639
100. K. Sanpei, H. Takano, S. Igarashi, T. Sato, M. Oyake, H. Sasaki, A. Wakisaka, K. Tashiro, Y. Ishida, T. Ikeuchi, R. Koide, M. Saito, A. Sato, T. Tanaka, S. Hanyu, Y. Takiyama, M. Nishizawa, N. Shimizu, Y. Nomura, M. Segawa, K. Iwabuchi, I. Eguchi, H. Tanaka, H. Takahashi, and S. Tsuji Identification of the spinocerebellar ataxia type 2 gene using a direct identification of repeat expansion and cloning technique, DIRECT Nat. Genet. 14 1996 277 284
101. C. Sato, K. Hamada, T. Ogura, A. Miyazawa, K. Iwasaki, Y. Hiroaki, K. Tani, A. Terauchi, Y. Fujiyoshi, and K. Mikoshiba Inositol 1,4,5-trisphosphate receptor contains multiple cavities and L-shaped ligand-binding domains J. Mol. Biol 336 2004 155 164
102. L. Schols, P. Bauer, T. Schmidt, T. Schulte, and O. Riess Autosomal dominant cerebellar ataxias: clinical features, genetics, and pathogenesis Lancet Neurol. 3 2004 291 304
103. M.D. Seo, S. Velamakanni, N. Ishiyama, P.B. Stathopulos, A.M. Rossi, S.A. Khan, P. Dale, C. Li, J.B. Ames, M. Ikura, and C.W. Taylor Structural and functional conservation of key domains in InsP3 and ryanodine receptors Nature 483 2012 108 112
104. I.I. Serysheva, D.J. Bare, S.J. Ludtke, C.S. Kettlun, W. Chiu, and G.A. Mignery Structure of the type 1 inositol 1,4,5-trisphosphate receptor revealed by electron cryomicroscopy J. Biol. Chem. 278 2003 21319 21322
105. A.H. Sharp, T.M. Dawson, C.A. Ross, M. Fotuhi, R.J. Mourey, and S.H. Snyder Inositol 1,4,5-trisphosphate receptors: immunohistochemical localization to discrete areas of rat central nervous system Neuroscience 53 1993 927 942
106. 2+ release channels in rat brain J. Neurosci. 13 1993 3051 3063
107. J. Shuai, H.J. Rose, and I. Parker The number and spatial distribution of IP3 receptors underlying calcium puffs in Xenopus oocytes Biophys. J. 91 2006 4033 4044
108. J.W. Shuai, and P. Jung Optimal ion channel clustering for intracellular calcium signaling Proc. Natl. Acad. Sci. USA 100 2003 506 510
109. G. Solovey, and S.P. Dawson Intra-cluster percolation of calcium signals PLoS One 5 2010 e8997
110. 2+] recordings in single rat sensory neurones Pflugers Arch. 446 2003 447 454
111. P.B. Stathopulos, M.D. Seo, M. Enomoto, F.J. Amador, N. Ishiyama, and M. Ikura Themes and variations in ER/SR calcium release channels: structure and function Physiology (Bethesda) 27 2012 331 342
112. V.A. Street, M.M. Bosma, V.P. Demas, M.R. Regan, D.D. Lin, L.C. Robinson, W.S. Agnew, and B.L. Tempel The type 1 inositol 1,4,5-trisphosphate receptor gene is altered in the opisthotonos mouse J. Neurosci. 17 1997 635 645
113. G.E. Stutzmann The pathogenesis of Alzheimers disease is it a lifelong «calciumopathy»? Neuroscientist 13 2007 546 559
114. T. Sugawara, C. Hisatsune, T.D. Le, T. Hashikawa, M. Hirono, M. Hattori, S. Nagao, and K. Mikoshiba Type 1 inositol trisphosphate receptor regulates cerebellar circuits by maintaining the spine morphology of purkinje cells in adult mice J. Neurosci.: Off. J. Soc. Neurosci. 33 2013 12186 12196
115. S. Supattapone, P.F. Worley, J.M. Baraban, and S.H. Snyder Solubilization, purification, and characterization of an inositol trisphosphate receptor J. Biol. Chem. 263 1988 1530 1534
116. S.J. Tallaksen-Greene, K.W. Kaatz, C. Romano, and R.L. Albin Localization of mGluR1a-like immunoreactivity and mGluR5-like immunoreactivity in identified populations of striatal neurons Brain Res. 780 1998 210 217
117. T.S. Tang, C. Guo, H. Wang, X. Chen, and I. Bezprozvanny Neuroprotective effects of inositol 1,4,5-trisphosphate receptor C-terminal fragment in a Huntington's disease mouse model J. Neurosci. 29 2009 1257 1266
118. 2+ signaling and apoptosis of medium spiny neurons in Huntington's disease Proc. Natl. Acad. Sci. USA 102 2005 2602 2607
119. T.S. Tang, H. Tu, E.Y. Chan, A. Maximov, Z. Wang, C.L. Wellington, M.R. Hayden, and I. Bezprozvanny Huntingtin and huntingtin-associated protein 1 influence neuronal calcium signaling mediated by inositol-(1,4,5) triphosphate receptor type 1 Neuron 39 2003 227 239
120. T.S. Tang, H. Tu, Z. Wang, and I. Bezprozvanny Modulation of type 1 inositol (1,4,5)-trisphosphate receptor function by protein kinase A and protein phosphatase 1alpha J. Neurosci. 23 2003 403 415
121. A. Tanimura, Y. Tojyo, and R.J. Turner Evidence that type I, II, and III inositol 1,4,5-trisphosphate receptors can occur as integral plasma membrane proteins J. Biol. Chem. 275 2000 27488 27493
122. C.W. Taylor, A.A. Genazzani, and S.A. Morris Expression of inositol trisphosphate receptors Cell Calcium 26 1999 237 251
123. 2+ signals Chaos 19 2009 037102
124. C.M. Testa, D.G. Standaert, G.B. Landwehrmeyer, J.B. Penney Jr., and A.B. Young Differential expression of mGluR5 metabotropic glutamate receptor mRNA by rat striatal neurons J. Comp. Neurol. 354 1995 241 252
125. A.J. Tobin, and E.R. Signer Huntington's disease: the challenge for cell biologists Trends Cell Biol. 10 2000 531 536
126. H. Tu, O. Nelson, A. Bezprozvanny, Z. Wang, S.-F. Lee, Y.H. Hao, L. Serneels, B. De Strooper, G. Yu, and I. Bezprozvanny Presenilins form ER calcium leak channels, a function disrupted by mutations linked to familial Alzheimer's disease Cell 126 2006 981 993
127. H. Tu, T.S. Tang, Z. Wang, and I. Bezprozvanny Association of type 1 inositol 1,4,5-trisphosphate receptor with AKAP9 (Yotiao) and protein kinase A J. Biol. Chem. 279 2004 19375 19382
128. H. Tu, Z. Wang, and I. Bezprozvanny Modulation of mammalian inositol 1,4,5-trisphosphate receptor isoforms by calcium: a role of calcium sensor region Biophys. J. 88 2005 1056 1069
129. H. Tu, Z. Wang, E. Nosyreva, H. De Smedt, and I. Bezprozvanny Functional characterization of mammalian inositol 1,4,5-trisphosphate receptor isoforms Biophys. J. 88 2005 1046 1055
130. K. Uchida, H. Miyauchi, T. Furuichi, T. Michikawa, and K. Mikoshiba Critical regions for activation gating of the inositol 1,4,5-trisphosphate receptor J. Biol. Chem. 278 2003 16551 16560
131. J. van de Leemput, J. Chandran, M.A. Knight, L.A. Holtzclaw, S. Scholz, M.R. Cookson, H. Houlden, K. Gwinn-Hardy, H.C. Fung, X. Lin, D. Hernandez, J. Simon-Sanchez, N.W. Wood, P. Giunti, I. Rafferty, J. Hardy, E. Storey, R.J. Gardner, S.M. Forrest, E.M. Fisher, J.T. Russell, H. Cai, and A.B. Singleton Deletion at ITPR1 underlies ataxia in mice and spinocerebellar ataxia 15 in humans PLoS Genet. 3 2007 e108
132. 2+ release by reversible phosphorylation and dephosphorylation Biochim. Biophys. Acta 1793 2009 959 970
133. J.P. Vonsattel, and M. DiFiglia Huntington disease J. Neuropathol. Exp. Neurol. 57 1998 369 384
134. J.P. Vonsattel, R.H. Myers, T.J. Stevens, R.J. Ferrante, E.D. Bird, and E.P. Richardson Jr. Neuropathological classification of Huntington's disease J. Neuropathol. Exp. Neurol. 44 1985 559 577
135. L.E. Wagner 2nd, W.H. Li, S.K. Joseph, and D.I. Yule 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
136. L.E. Wagner 2nd, W.H. Li, and D.I. Yule Phosphorylation of type-1 inositol 1,4,5-trisphosphate receptors by cyclic nucleotide-dependent protein kinases: a mutational analysis of the functionally important sites in the S2+ and S2- splice variants J. Biol. Chem. 278 2003 45811 45817
137. L.E. Wagner 2nd, and D.I. Yule Differential regulation of the InsP(3) receptor type-1 and -2 single channel properties by InsP(3), Ca(2)(+) and ATP J. Physiol. 590 2012 3245 3259
138. J.S. Wiegert, and H. Bading Activity-dependent calcium signaling and ERK-MAP kinases in neurons: a link to structural plasticity of the nucleus and gene transcription regulation Cell Calcium 49 2011 296 305
139. 2+ mobilization by mediating the interaction between type I inositol 1,4,5-trisphosphate receptor, RACK1, and Orai1 J. Biol. Chem. 285 2010 8045 8053
140. J. Wu, H.P. Shih, V. Vigont, L. Hrdlicka, L. Diggins, C. Singh, M. Mahoney, R. Chesworth, G. Shapiro, O. Zimina, X. Chen, Q. Wu, L. Glushankova, M. Ahlijanian, G. Koenig, G.N. Mozhayeva, E. Kaznacheyeva, and I. Bezprozvanny Neuronal store-operated calcium entry pathway as a novel therapeutic target for Huntington's disease treatment Chem. Biol. 18 2011 777 793
141. M. Yamada, A. Miyawaki, K. Saito, T. Nakajima, M. Yamamoto-Hino, Y. Ryo, T. Furuichi, and K. Mikoshiba The calmodulin-binding domain in the mouse type 1 inositol 1,4,5-trisphosphate receptor Biochem. J. 308 1995 83 88
142. 2+] regulation of InsP3-evoked puffs Biochem. J. 449 2013 167 173
143. H. Yamazaki, J. Chan, M. Ikura, T. Michikawa, and K. Mikoshiba Tyr-167/Trp-168 in type 1/3 inositol 1,4,5-trisphosphate receptor mediates functional coupling between ligand binding and channel opening J. Biol. Chem. 285 2010 36081 36091
144. 2+ evoked by inositol trisphosphate in Xenopus oocytes J. Physiol. (Lond.) 482 1995 533 553
145. F. Yoshikawa, M. Morita, T. Monkawa, T. Michikawa, T. Furuichi, and K. Mikoshiba Mutational analysis of the ligand binding site of the inositol 1,4,5-trisphosphate receptor J. Biol. Chem. 271 1996 18277 18284
146. H. Zhang, S. Sun, A. Herreman, B. De Strooper, and I. Bezprozvanny Role of presenilins in neuronal calcium homeostasis J. Neurosci. 30 2010 8566 8580