IP3 Receptor Plasticity Underlying Diverse Functions

Literature Cited

1. 1. 

   Mikoshiba K, Changeux JP. 1978. Morphological and biochemical studies on isolated molecular and granular layers from bovine cerebellum. Brain Res 142487–504
2. 2. 

   Mikoshiba K, Huchet M, Changeux JP 1979. Biochemical and immunological studies on the P₄₀₀ protein, a protein characteristic of the Purkinje cell from mouse and rat cerebellum. Dev. Neurosci. 2254–75
3. 3. 

   Crepel F, Dupont JL, Gardette R 1984. Selective absence of calcium spikes in Purkinje cells of staggerer mutant mice in cerebellar slices maintained in vitro. J. Physiol. 346111–25
4. 4. 

   Maeda N, Niinobe M, Nakahira K, Mikoshiba K 1988. Purification and characterization of P₄₀₀ protein, a glycoprotein characteristic of Purkinje cell, from mouse cerebellum. J. Neurochem. 511724–30
5. 5. 

   Furuichi T, Yoshikawa S, Miyawaki A, Wada K, Maeda N, Mikoshiba K 1989. Primary structure and functional expression of the inositol 1,4,5-trisphosphate-binding protein P₄₀₀. Nature 34232–38
6. 6. 

   Foskett JK, White C, Cheung KH, Mak DO 2007. Inositol trisphosphate receptor Ca²⁺ release channels. Physiol. Rev. 87593–658
7. 7. 

   Patterson RL, Boehning D, Snyder SH 2004. Inositol 1,4,5-trisphosphate receptors as signal integrators. Annu. Rev. Biochem. 73437–65
8. 8. 

   Berridge MJ. 2016. The inositol trisphosphate/calcium signaling pathway in health and disease. Physiol. Rev. 961261–96
9. 9. 

   Iino M. 1990. Biphasic Ca²⁺ dependence of inositol 1,4,5-trisphosphate-induced Ca release in smooth muscle cells of the guinea pig taenia caeci. J. Gen. Physiol. 951103–22
10. 10. 

    Bezprozvanny I, Watras J, Ehrlich BE 1991. Bell-shaped calcium-response curves of Ins(1,4,5)P₃- and calcium-gated channels from endoplasmic reticulum of cerebellum. Nature 351751–54
11. 11. 

    Matsumoto M, Nakagawa T, Inoue T, Nagata E, Tanaka K et al. 1996. Ataxia and epileptic seizures in mice lacking type 1 inositol 1,4,5-trisphosphate receptor. Nature 379168–71
12. 12. 

    Inoue T, Kato K, Kohda K, Mikoshiba K 1998. Type 1 inositol 1,4,5-trisphosphate receptor is required for induction of long-term depression in cerebellar Purkinje neurons. J. Neurosci. 185366–73
13. 13. 

    Hisatsune C, Kuroda Y, Akagi T, Torashima T, Hirai H et al. 2006. Inositol 1,4,5-trisphosphate receptor type 1 in granule cells, not in Purkinje cells, regulates the dendritic morphology of Purkinje cells through brain-derived neurotrophic factor production. J. Neurosci. 2610916–24
14. 14. 

    Hisatsune C, Miyamoto H, Hirono M, Yamaguchi N, Sugawara T et al. 2013. IP₃R1 deficiency in the cerebellum/brainstem causes basal ganglia-independent dystonia by triggering tonic Purkinje cell firings in mice. Front. Neural Circuits 7156
15. 15. 

    Sugawara T, Hisatsune C, Le TD, Hashikawa T, Hirono M et al. 2013. Type 1 inositol trisphosphate receptor regulates cerebellar circuits by maintaining the spine morphology of purkinje cells in adult mice. J. Neurosci. 3312186–96
16. 16. 

    Sugawara T, Hisatsune C, Miyamoto H, Ogawa N, Mikoshiba K 2017. Regulation of spinogenesis in mature Purkinje cells via mGluR/PKC-mediated phosphorylation of CaMKIIβ. PNAS 114E5256–65
17. 17. 

    Tsuboi D, Kuroda K, Tanaka M, Namba T, Iizuka Y et al. 2015. Disrupted-in-schizophrenia 1 regulates transport of ITPR1 mRNA for synaptic plasticity. Nat. Neurosci. 18698–707
18. 18. 

    Monai H, Ohkura M, Tanaka M, Oe Y, Konno A et al. 2016. Calcium imaging reveals glial involvement in transcranial direct current stimulation-induced plasticity in mouse brain. Nat. Commun. 711100
19. 19. 

    Nizar K, Uhlirova H, Tian P, Saisan PA, Cheng Q et al. 2013. In vivo stimulus-induced vasodilation occurs without IP₃ receptor activation and may precede astrocytic calcium increase. J. Neurosci. 338411–22
20. 20. 

    Petravicz J, Fiacco TA, McCarthy KD 2008. Loss of IP₃ receptor-dependent Ca²⁺ increases in hippocampal astrocytes does not affect baseline CA1 pyramidal neuron synaptic activity. J. Neurosci. 284967–73
21. 21. 

    Sherwood MW, Arizono M, Hisatsune C, Bannai H, Ebisui E et al. 2017. Astrocytic IP₃Rs: contribution to Ca²⁺ signalling and hippocampal LTP. Glia 65502–13
22. 22. 

    Okubo Y, Kanemaru K, Suzuki J, Kobayashi K, Hirose K, Iino M 2019. Inositol 1,4,5-trisphosphate receptor type 2-independent Ca²⁺ release from the endoplasmic reticulum in astrocytes. Glia 67113–24
23. 23. 

    Satoh T, Ross CA, Villa A, Supattapone S, Pozzan T et al. 1990. The inositol 1,4,5,-trisphosphate receptor in cerebellar Purkinje cells: quantitative immunogold labeling reveals concentration in an ER subcompartment. J. Cell Biol. 111615–24
24. 24. 

    Pinton P, Pozzan T, Rizzuto R 1998. The Golgi apparatus is an inositol 1,4,5-trisphosphate-sensitive Ca²⁺ store, with functional properties distinct from those of the endoplasmic reticulum. EMBO J 175298–308
25. 25. 

    Gerasimenko OV, Gerasimenko JV, Tepikin AV, Petersen OH 1995. ATP-dependent accumulation and inositol trisphosphate- or cyclic ADP-ribose-mediated release of Ca²⁺ from the nuclear envelope. Cell 80439–44
26. 26. 

    Stehno-Bittel L, Perez-Terzic C, Clapham DE 1995. Diffusion across the nuclear envelope inhibited by depletion of the nuclear Ca²⁺ store. Science 2701835–38
27. 27. 

    Huh YH, Yoo SH. 2003. Presence of the inositol 1,4,5-triphosphate receptor isoforms in the nucleoplasm. FEBS Lett 555411–18
28. 28. 

    Fadool DA, Ache BW. 1992. Plasma membrane inositol 1,4,5-trisphosphate-activated channels mediate signal transduction in lobster olfactory receptor neurons. Neuron 9907–18
29. 29. 

    Kuno M, Maeda N, Mikoshiba K 1994. IP₃-activated calcium-permeable channels in the inside-out patches of cultured cerebellar Purkinje cells. Biochem. Biophys. Res. Commun. 1991128–35
30. 30. 

    Echevarria W, Leite MF, Guerra MT, Zipfel WR, Nathanson MH 2003. Regulation of calcium signals in the nucleus by a nucleoplasmic reticulum. Nat. Cell Biol. 5440–46
31. 31. 

    Bading H. 2013. Nuclear calcium signalling in the regulation of brain function. Nat. Rev. Neurosci. 14593–608
32. 32. 

    Ondrias K, Lencesova L, Sirova M, Labudova M, Pastorekova S et al. 2011. Apoptosis induced clustering of IP₃R1 in nuclei of non-differentiated PC12 cells. J. Cell Physiol. 2263147–55
33. 33. 

    Ikebara JM, Takada SH, Cardoso DS, Dias NM, de Campos BC et al. 2017. Functional role of intracellular calcium receptor inositol 1,4,5-trisphosphate type 1 in rat hippocampus after neonatal anoxia. PLOS ONE 12e0169861
34. 34. 

    Khan AA, Soloski MJ, Sharp AH, Schilling G, Sabatini DM et al. 1996. Lymphocyte apoptosis: mediation by increased type 3 inositol 1,4,5-trisphosphate receptor. Science 273503–7
35. 35. 

    El-Daher SS, Patel Y, Siddiqua A, Hassock S, Edmunds S et al. 2000. Distinct localization and function of ^1,4,5IP₃ receptor subtypes and the ^1,3,4,5IP₄ receptor GAP1^IP4BP in highly purified human platelet membranes. Blood 953412–22
36. 36. 

    Guillemette G, Balla T, Baukal AJ, Catt KJ 1988. Characterization of inositol 1,4,5-trisphosphate receptors and calcium mobilization in a hepatic plasma membrane fraction. J. Biol. Chem. 2634541–48
37. 37. 

    Vazquez G, Wedel BJ, Bird GS, Joseph SK, Putney JW 2002. An inositol 1,4,5-trisphosphate receptor-dependent cation entry pathway in DT40 B lymphocytes. EMBO J 214531–8
38. 38. 

    Dellis O, Dedos SG, Tovey SC, Taufiq-Ur-Rahman, Dubel SJ, Taylor CW 2006. Ca²⁺ entry through plasma membrane IP₃ receptors. Science 313229–33
39. 39. 

    Docampo R, de Souza W, Miranda K, Rohloff P, Moreno SN 2005. Acidocalcisomes—conserved from bacteria to man. Nat. Rev. Microbiol. 3251–61
40. 40. 

    Lander N, Chiurillo MA, Storey M, Vercesi AE, Docampo R 2016. CRISPR/Cas9-mediated endogenous C-terminal tagging of Trypanosoma cruzi genes reveals the acidocalcisome localization of the inositol 1,4,5-trisphosphate receptor. J. Biol. Chem. 29125505–15
41. 41. 

    Huang G, Bartlett PJ, Thomas AP, Moreno SN, Docampo R 2013. Acidocalcisomes of Trypanosoma brucei have an inositol 1,4,5-trisphosphate receptor that is required for growth and infectivity. PNAS 1101887–92
42. 42. 

    Li FJ, He CY. 2014. Acidocalcisome is required for autophagy in Trypanosoma brucei. Autophagy 101978–88
43. 43. 

    Rizzuto R, Pinton P, Carrington W, Fay FS, Fogarty KE et al. 1998. Close contacts with the endoplasmic reticulum as determinants of mitochondrial Ca²⁺ responses. Science 2801763–66
44. 44. 

    Csordas G, Renken C, Varnai P, Walter L, Weaver D et al. 2006. Structural and functional features and significance of the physical linkage between ER and mitochondria. J. Cell Biol. 174915–21
45. 45. 

    Szabadkai G, Bianchi K, Varnai P, De Stefani D, Wieckowski MR et al. 2006. Chaperone-mediated coupling of endoplasmic reticulum and mitochondrial Ca²⁺ channels. J. Cell Biol. 175901–11
46. 46. 

    Betz C, Stracka D, Prescianotto-Baschong C, Frieden M, Demaurex N, Hall MN 2013. mTOR complex 2-Akt signaling at mitochondria-associated endoplasmic reticulum membranes (MAM) regulates mitochondrial physiology. PNAS 11012526–34
47. 47. 

    Hamasaki M, Furuta N, Matsuda A, Nezu A, Yamamoto A et al. 2013. Autophagosomes form at ER-mitochondria contact sites. Nature 495389–93
48. 48. 

    Garvey M, Klose H, Fischer R, Lambertz C, Commandeur U 2013. Cellulases for biomass degradation: comparing recombinant cellulase expression platforms. Trends Biotechnol 31581–93
49. 49. 

    Iwasawa R, Mahul-Mellier AL, Datler C, Pazarentzos E, Grimm S 2011. Fis1 and Bap31 bridge the mitochondria-ER interface to establish a platform for apoptosis induction. EMBO J 30556–68
50. 50. 

    Cárdenas C, Müller M, McNeal A, Lovy A, Jaňa F et al. 2016. Selective vulnerability of cancer cells by inhibition of Ca²⁺ transfer from endoplasmic reticulum to mitochondria. Cell Rep 142313–24
51. 51. 

    Bonneau B, Ando H, Kawaai K, Hirose M, Takahashi-Iwanaga H, Mikoshiba K 2016. IRBIT controls apoptosis by interacting with the Bcl-2 homolog, Bcl2l10, and by promoting ER-mitochondria contact. eLife 5e19896
52. 52. 

    Hayashi T, Su TP. 2007. Sigma-1 receptor chaperones at the ER-mitochondrion interface regulate Ca²⁺ signaling and cell survival. Cell 131596–610
53. 53. 

    Brailoiu E, Chakraborty S, Brailoiu GC, Zhao P, Barr JL et al. 2019. Choline is an intracellular messenger linking extracellular stimuli to IP₃-evoked Ca²⁺ signals through sigma-1 receptors. Cell Rep 26330–37.e4
54. 54. 

    Petkovic M, Jemaiel A, Daste F, Specht CG, Izeddin I et al. 2014. The SNARE Sec22b has a non-fusogenic function in plasma membrane expansion. Nat. Cell Biol. 16434–44
55. 55. 

    Fernandez-Busnadiego R, Saheki Y, De Camilli P 2015. Three-dimensional architecture of extended synaptotagmin-mediated endoplasmic reticulum-plasma membrane contact sites. PNAS 112E2004–13
56. 56. 

    Lur G, Sherwood MW, Ebisui E, Haynes L, Feske S et al. 2011. InsP₃ receptors and Orai channels in pancreatic acinar cells: co-localization and its consequences. Biochem. J. 436231–39
57. 57. 

    Okeke E, Parker T, Dingsdale H, Concannon M, Awais M et al. 2016. Epithelial-mesenchymal transition, IP₃ receptors and ER-PM junctions: translocation of Ca²⁺ signalling complexes and regulation of migration. Biochem. J. 473757–67
58. 58. 

    Wang Q, Wang Y, Downey GP, Plotnikov S, McCulloch CA 2016. A ternary complex comprising FAK, PTPα and IP₃ receptor 1 functionally engages focal adhesions and the endoplasmic reticulum to mediate IL-1-induced Ca²⁺ signalling in fibroblasts. Biochem. J. 473397–410
59. 59. 

    Otsu H, Yamamoto A, Maeda N, Mikoshiba K, Tashiro Y 1990. Immunogold localization of inositol 1, 4, 5-trisphosphate (InsP₃) receptor in mouse cerebellar Purkinje cells using three monoclonal antibodies. Cell Struct. Funct. 15163–73
60. 60. 

    Yamamoto A, Otsu H, Yoshimori T, Maeda N, Mikoshiba K, Tashiro Y 1991. Stacks of flattened smooth endoplasmic reticulum highly enriched in inositol 1,4,5-trisphosphate (InsP₃) receptor in mouse cerebellar Purkinje cells. Cell Struct. Funct. 16419–32
61. 61. 

    Rusakov DA, Podini P, Villa A, Meldolesi J 1993. Tridimensional organization of Purkinje neuron cisternal stacks, a specialized endoplasmic-reticulum subcompartment rich in inositol 1,4,5-trisphosphate receptors. J. Neurocytol. 22273–82
62. 62. 

    Takei K, Mignery GA, Mugnaini E, Sudhof TC, De Camilli P 1994. Inositol 1,4,5-trisphosphate receptor causes formation of ER cisternal stacks in transfected fibroblasts and in cerebellar Purkinje cells. Neuron 12327–42
63. 63. 

    Banno T, Kohno K. 1996. Conformational changes of smooth endoplasmic reticulum induced by brief anoxia in rat Purkinje cells. J. Comp. Neurol. 369462–71
64. 64. 

    Ikemoto T, Yorifuji H, Satoh T, Vizi ES 2003. Reversibility of cisternal stack formation during hypoxic hypoxia and subsequent reoxygenation in cerebellar Purkinje cells. Neurochem. Res. 281535–42
65. 65. 

    Varadarajan S, Bampton ET, Smalley JL, Tanaka K, Caves RE et al. 2012. A novel cellular stress response characterised by a rapid reorganisation of membranes of the endoplasmic reticulum. Cell Death Differ 191896–907
66. 66. 

    Varadarajan S, Tanaka K, Smalley JL, Bampton ET, Pellecchia M et al. 2013. Endoplasmic reticulum membrane reorganization is regulated by ionic homeostasis. PLOS ONE 8e56603
67. 67. 

    Morgan AJ, Platt FM, Lloyd-Evans E, Galione A 2011. Molecular mechanisms of endolysosomal Ca²⁺ signalling in health and disease. Biochem. J. 439349–74
68. 68. 

    Prinz WA. 2014. Bridging the gap: membrane contact sites in signaling, metabolism, and organelle dynamics. J. Cell Biol. 205759–69
69. 69. 

    Elbaz Y, Schuldiner M. 2011. Staying in touch: the molecular era of organelle contact sites. Trends Biochem. Sci. 36616–23
70. 70. 

    Mignery GA, Newton CL, Archer BT 3rd, Sudhof TC 1990. Structure and expression of the rat inositol 1,4,5-trisphosphate receptor. J. Biol. Chem. 26512679–85
71. 71. 

    Ross CA, Danoff SK, Schell MJ, Snyder SH, Ullrich A 1992. Three additional inositol 1,4,5-trisphosphate receptors: molecular cloning and differential localization in brain and peripheral tissues. PNAS 894265–69
72. 72. 

    Yamamoto-Hino M, Sugiyama T, Hikichi K, Mattei MG, Hasegawa K et al. 1994. Cloning and characterization of human type 2 and type 3 inositol 1,4,5-trisphosphate receptors. Recept. Channels 29–22
73. 73. 

    Iwai M, Tateishi Y, Hattori M, Mizutani A, Nakamura T et al. 2005. Molecular cloning of mouse type 2 and type 3 inositol 1,4,5-trisphosphate receptors and identification of a novel type 2 receptor splice variant. J. Biol. Chem. 28010305–17
74. 74. 

    Nakagawa T, Okano H, Furuichi T, Aruga J, Mikoshiba K 1991. The subtypes of the mouse inositol 1,4,5-trisphosphate receptor are expressed in a tissue-specific and developmentally specific manner. PNAS 886244–48
75. 75. 

    Danoff SK, Ferris CD, Donath C, Fischer GA, Munemitsu S et al. 1991. Inositol 1,4,5-trisphosphate receptors: distinct neuronal and nonneuronal forms derived by alternative splicing differ in phosphorylation. PNAS 882951–55
76. 76. 

    Yamada N, Makino Y, Clark RA, Pearson DW, Mattei MG et al. 1994. Human inositol 1,4,5-trisphosphate type-1 receptor, InsP₃R1: structure, function, regulation of expression and chromosomal localization. Biochem. J. 302Part 3781–90
77. 77. 

    Regan MR, Lin DD, Emerick MC, Agnew WS 2005. The effect of higher order RNA processes on changing patterns of protein domain selection: a developmentally regulated transcriptome of type 1 inositol 1,4,5-trisphosphate receptors. Proteins 59312–31
78. 78. 

    Yoshikawa F, Morita M, Monkawa T, Michikawa T, Furuichi T, Mikoshiba K 1996. Mutational analysis of the ligand binding site of the inositol 1,4,5-trisphosphate receptor. J. Biol. Chem. 27118277–84
79. 79. 

    Uchida K, Miyauchi H, Furuichi T, Michikawa T, Mikoshiba K 2003. Critical regions for activation gating of the inositol 1,4,5-trisphosphate receptor. J. Biol. Chem. 27816551–60
80. 80. 

    Bosanac I, Alattia JR, Mal TK, Chan J, Talarico S et al. 2002. Structure of the inositol 1,4,5-trisphosphate receptor binding core in complex with its ligand. Nature 420696–700
81. 81. 

    Hamada K, Terauchi A, Mikoshiba K 2003. Three-dimensional rearrangements within inositol 1,4,5-trisphosphate receptor by calcium. J. Biol. Chem. 27852881–89
82. 82. 

    Sato C, Hamada K, Ogura T, Miyazawa A, Iwasaki K et al. 2004. Inositol 1,4,5-trisphosphate receptor contains multiple cavities and L-shaped ligand-binding domains. J. Mol. Biol. 336155–64
83. 83. 

    Fan G, Baker MR, Wang Z, Seryshev AB, Ludtke SJ et al. 2018. Cryo-EM reveals ligand induced allostery underlying InsP₃R channel gating. Cell Res 281158–70
84. 84. 

    Fan G, Baker ML, Wang Z, Baker MR, Sinyagovskiy PA et al. 2015. Gating machinery of InsP₃R channels revealed by electron cryomicroscopy. Nature 527336–41
85. 85. 

    Paknejad N, Hite RK. 2018. Structural basis for the regulation of inositol trisphosphate receptors by Ca²⁺ and IP₃. Nat. Struct. Mol. Biol. 25660–68
86. 86. 

    Sudhof TC, Newton CL, Archer BT 3rd, Ushkaryov YA, Mignery GA 1991. Structure of a novel InsP₃ receptor. EMBO J 103199–206
87. 87. 

    Ida Y, Kidera A. 2013. The conserved Arg241-Glu439 salt bridge determines flexibility of the inositol 1,4,5-trisphosphate receptor binding core in the ligand-free state. Proteins 811699–708
88. 88. 

    Bosanac I, Yamazaki H, Matsu-Ura T, Michikawa T, Mikoshiba K, Ikura M 2005. Crystal structure of the ligand binding suppressor domain of type 1 inositol 1,4,5-trisphosphate receptor. Mol. Cell 17193–203
89. 89. 

    Yamazaki H, Chan J, Ikura M, Michikawa T, Mikoshiba K 2010. 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. 28536081–91
90. 90. 

    Iwai M, Michikawa T, Bosanac I, Ikura M, Mikoshiba K 2007. Molecular basis of the isoform-specific ligand-binding affinity of inositol 1,4,5-trisphosphate receptors. J. Biol. Chem. 28212755–64
91. 91. 

    Lin CC, Baek K, Lu Z 2011. Apo and InsP₃-bound crystal structures of the ligand-binding domain of an InsP₃ receptor. Nat. Struct. Mol. Biol. 181172–74
92. 92. 

    Seo MD, Velamakanni S, Ishiyama N, Stathopulos PB, Rossi AM et al. 2012. Structural and functional conservation of key domains in InsP₃ and ryanodine receptors. Nature 483108–12
93. 93. 

    Chandran A, Chee X, Prole DL, Rahman T 2019. Exploration of inositol 1,4,5-trisphosphate (IP₃) regulated dynamics of N-terminal domain of IP₃ receptor reveals early phase molecular events during receptor activation. Sci. Rep. 92454
94. 94. 

    Ando H, Hirose M, Mikoshiba K 2018. Aberrant IP₃ receptor activities revealed by comprehensive analysis of pathological mutations causing spinocerebellar ataxia 29. PNAS 11512259–64
95. 95. 

    Ladenburger EM, Korn I, Kasielke N, Wassmer T, Plattner H 2006. An Ins(1,4,5)P₃ receptor in Paramecium is associated with the osmoregulatory system. J. Cell Sci. 1193705–17
96. 96. 

    Hashimoto M, Enomoto M, Morales J, Kurebayashi N, Sakurai T et al. 2013. Inositol 1,4,5-trisphosphate receptor regulates replication, differentiation, infectivity and virulence of the parasitic protist Trypanosoma cruzi. Mol. Microbiol 871133–50
97. 97. 

    Hashimoto M, Doi M, Kurebayashi N, Furukawa K, Hirawake-Mogi H et al. 2016. Inositol 1,4,5-trisphosphate receptor determines intracellular Ca²⁺ concentration in Trypanosoma cruzi throughout its life cycle. FEBS Open Bio 61178–85
98. 98. 

    Morales-Perez CL, Noviello CM, Hibbs RE 2016. X-ray structure of the human α4β2 nicotinic receptor. Nature 538411–15
99. 99. 

    Zhu S, Stein RA, Yoshioka C, Lee CH, Goehring A et al. 2016. Mechanism of NMDA receptor inhibition and activation. Cell 165704–14
100. 100. 

     Chen L, Durr KL, Gouaux E 2014. X-ray structures of AMPA receptor-cone snail toxin complexes illuminate activation mechanism. Science 3451021–26
101. 101. 

     Miller PS, Aricescu AR. 2014. Crystal structure of a human GABA_A receptor. Nature 512270–75
102. 102. 

     Hassaine G, Deluz C, Grasso L, Wyss R, Tol MB et al. 2014. X-ray structure of the mouse serotonin 5-HT3 receptor. Nature 512276–81
103. 103. 

     Mansoor SE, Lu W, Oosterheert W, Shekhar M, Tajkhorshid E, Gouaux E 2016. X-ray structures define human P2X₃ receptor gating cycle and antagonist action. Nature 53866–71
104. 104. 

     des Georges A, Clarke OB, Zalk R, Yuan Q, Condon KJ et al. 2016. Structural basis for gating and activation of RyR1. Cell 167145–57.e17
105. 105. 

     Chadwick CC, Saito A, Fleischer S 1990. Isolation and characterization of the inositol trisphosphate receptor from smooth muscle. PNAS 872132–36
106. 106. 

     Hamada K, Miyata T, Mayanagi K, Hirota J, Mikoshiba K 2002. Two-state conformational changes in inositol 1,4,5-trisphosphate receptor regulated by calcium. J. Biol. Chem. 27721115–18
107. 107. 

     da Fonseca PC, Morris SA, Nerou EP, Taylor CW, Morris EP 2003. Domain organization of the type 1 inositol 1,4,5-trisphosphate receptor as revealed by single-particle analysis. PNAS 1003936–41
108. 108. 

     Jiang QX, Thrower EC, Chester DW, Ehrlich BE, Sigworth FJ 2002. Three-dimensional structure of the type 1 inositol 1,4,5-trisphosphate receptor at 24 Å resolution. EMBO J 213575–81
109. 109. 

     Serysheva II, Bare DJ, Ludtke SJ, Kettlun CS, Chiu W, Mignery GA 2003. Structure of the type 1 inositol 1,4,5-trisphosphate receptor revealed by electron cryomicroscopy. J. Biol. Chem. 27821319–22
110. 110. 

     Henderson R, Sali A, Baker ML, Carragher B, Devkota B et al. 2012. Outcome of the first electron microscopy validation task force meeting. Structure 20205–14
111. 111. 

     Henderson R. 2013. Avoiding the pitfalls of single particle cryo-electron microscopy: Einstein from noise. PNAS 11018037–41
112. 112. 

     Hamada K, Miyatake H, Terauchi A, Mikoshiba K 2017. IP₃-mediated gating mechanism of the IP₃ receptor revealed by mutagenesis and X-ray crystallography. PNAS 1144661–66
113. 113. 

     Anyatonwu G, Khan MT, Schug ZT, da Fonseca PC, Morris EP, Joseph SK 2010. Calcium-dependent conformational changes in inositol trisphosphate receptors. J. Biol. Chem. 28525085–93
114. 114. 

     Shinohara T, Michikawa T, Enomoto M, Goto J, Iwai M et al. 2011. Mechanistic basis of bell-shaped dependence of inositol 1,4,5-trisphosphate receptor gating on cytosolic calcium. PNAS 10815486–91
115. 115. 

     Sienaert I, Missiaen L, De Smedt H, Parys JB, Sipma H, Casteels R 1997. Molecular and functional evidence for multiple Ca²⁺-binding domains in the type 1 inositol 1,4,5-trisphosphate receptor. J. Biol. Chem. 27225899–906
116. 116. 

     Miyakawa T, Mizushima A, Hirose K, Yamazawa T, Bezprozvanny I et al. 2001. Ca²⁺-sensor region of IP₃ receptor controls intracellular Ca²⁺ signaling. EMBO J 201674–80
117. 117. 

     Alzayady KJ, Sebe-Pedros A, Chandrasekhar R, Wang L, Ruiz-Trillo I, Yule DI 2015. Tracing the evolutionary history of inositol, 1,4,5-trisphosphate receptor: insights from analyses of Capsaspora owczarzaki Ca²⁺ release channel orthologs. Mol. Biol. Evol. 322236–53
118. 118. 

     Nunn DL, Taylor CW. 1990. Liver inositol, 1,4,5-trisphosphate-binding sites are the Ca²⁺-mobilizing receptors. Biochem. J. 270227–32
119. 119. 

     Alzayady KJ, Wang L, Chandrasekhar R, Wagner LE 2nd, Van Petegem F, Yule DI 2016. Defining the stoichiometry of inositol 1,4,5-trisphosphate binding required to initiate Ca²⁺ release. Sci. Signal. 9ra35
120. 120. 

     Takahashi M, Tanzawa K, Takahashi S 1994. Adenophostins, newly discovered metabolites of Penicillium brevicompactum, act as potent agonists of the inositol 1,4,5-trisphosphate receptor. J. Biol. Chem. 269369–72
121. 121. 

     Boehning D, Joseph SK. 2000. Direct association of ligand-binding and pore domains in homo- and heterotetrameric inositol 1,4,5-trisphosphate receptors. EMBO J 195450–59
122. 122. 

     Hamada K, Mikoshiba K. 2012. Revisiting channel allostery: a coherent mechanism in IP₃ and ryanodine receptors. Sci. Signal. 5pe24
123. 123. 

     Schug ZT, Joseph SK. 2006. The role of the S4-S5 linker and C-terminal tail in inositol 1,4,5-trisphosphate receptor function. J. Biol. Chem. 28124431–40
124. 124. 

     Galvan DL, Mignery GA. 2002. Carboxyl-terminal sequences critical for inositol 1,4,5-trisphosphate receptor subunit assembly. J. Biol. Chem. 27748248–60
125. 125. 

     Boehning D, Patterson RL, Sedaghat L, Glebova NO, Kurosaki T, Snyder SH 2003. Cytochrome c binds to inositol (1,4,5) trisphosphate receptors, amplifying calcium-dependent apoptosis. Nat. Cell Biol. 51051–61
126. 126. 

     Boehning D, van Rossum DB, Patterson RL, Snyder SH 2005. A peptide inhibitor of cytochrome c/inositol 1,4,5-trisphosphate receptor binding blocks intrinsic and extrinsic cell death pathways. PNAS 1021466–71
127. 127. 

     White C, Li C, Yang J, Petrenko NB, Madesh M et al. 2005. The endoplasmic reticulum gateway to apoptosis by Bcl-X_L modulation of the InsP₃R. Nat. Cell Biol. 71021–28
128. 128. 

     Yang J, Vais H, Gu W, Foskett JK 2016. Biphasic regulation of InsP₃ receptor gating by dual Ca²⁺ release channel BH3-like domains mediates Bcl-x_L control of cell viability. PNAS 113E1953–62
129. 129. 

     Mery L, Magnino F, Schmidt K, Krause KH, Dufour JF 2001. Alternative splice variants of hTrp4 differentially interact with the C-terminal portion of the Inositol 1,4,5-trisphosphate receptors. FEBS Lett 487377–83
130. 130. 

     Fredericks GJ, Hoffmann FW, Rose AH, Osterheld HJ, Hess FM et al. 2014. Stable expression and function of the inositol 1,4,5-triphosphate receptor requires palmitoylation by a DHHC6/selenoprotein K complex. PNAS 11116478–83
131. 131. 

     Szado T, Vanderheyden V, Parys JB, De Smedt H, Rietdorf K et al. 2008. Phosphorylation of inositol 1,4,5-trisphosphate receptors by protein kinase B/Akt inhibits Ca²⁺ release and apoptosis. PNAS 1052427–32
132. 132. 

     Khan MT, Wagner L 2nd, Yule DI, Bhanumathy C, Joseph SK 2006. Akt kinase phosphorylation of inositol 1,4,5-trisphosphate receptors. J. Biol. Chem. 2813731–37
133. 133. 

     Hornbeck PV, Kornhauser JM, Tkachev S, Zhang B, Skrzypek E et al. 2012. PhosphoSitePlus: a comprehensive resource for investigating the structure and function of experimentally determined post-translational modifications in man and mouse. Nucleic Acids Res 40D261–70
134. 134. 

     Mertins P, Yang F, Liu T, Mani DR, Petyuk VA et al. 2014. Ischemia in tumors induces early and sustained phosphorylation changes in stress kinase pathways but does not affect global protein levels. Mol. Cell. Proteom. 131690–704
135. 135. 

     McEntagart M, Williamson KA, Rainger JK, Wheeler A, Seawright A et al. 2016. A restricted repertoire of de novo mutations in ITPR1 cause Gillespie syndrome with evidence for dominant-negative effect. Am. J. Hum. Genet. 98981–92
136. 136. 

     Gerber S, Alzayady KJ, Burglen L, Brémond-Gignac D, Marchesin V et al. 2016. Recessive and dominant de novo ITPR1 mutations cause Gillespie syndrome. Am. J. Hum. Genet. 98971–80
137. 137. 

     Ando H, Mizutani A, Kiefer H, Tsuzurugi D, Michikawa T, Mikoshiba K 2006. IRBIT suppresses IP₃ receptor activity by competing with IP₃ for the common binding site on the IP₃ receptor. Mol. Cell 22795–806
138. 138. 

     Kawaai K, Ando H, Satoh N, Yamada H, Ogawa N et al. 2017. Splicing variation of Long-IRBIT determines the target selectivity of IRBIT family proteins. PNAS 1143921–26
139. 139. 

     Bonneau B, Nougarede A, Prudent J, Popgeorgiev N, Peyrieras N et al. 2014. The Bcl-2 homolog Nrz inhibits binding of IP₃ to its receptor to control calcium signaling during zebrafish epiboly. Sci. Signal. 7ra14
140. 140. 

     Fos C, Becart S, Canonigo Balancio AJ, Boehning D, Altman A 2014. Association of the EF-hand and PH domains of the guanine nucleotide exchange factor SLAT with IP₃ receptor 1 promotes Ca²⁺ signaling in T cells. Sci. Signal. 7ra93
141. 141. 

     Tu JC, Xiao B, Yuan JP, Lanahan AA, Leoffert K et al. 1998. Homer binds a novel proline-rich motif and links group 1 metabotropic glutamate receptors with IP₃ receptors. Neuron 21717–26
142. 142. 

     Kang S, Kwon H, Wen H, Song Y, Frueh D et al. 2011. Global dynamic conformational changes in the suppressor domain of IP₃ receptor by stepwise binding of the two lobes of calmodulin. FASEB J 25840–50
143. 143. 

     Geyer M, Huang F, Sun Y, Vogel SM, Malik AB et al. 2015. Microtubule-associated protein EB3 regulates IP₃ receptor clustering and Ca²⁺ signaling in endothelial cells. Cell Rep 1279–89
144. 144. 

     Tu H, Tang TS, Wang Z, Bezprozvanny I 2004. Association of type 1 inositol 1,4,5-trisphosphate receptor with AKAP9 (Yotiao) and protein kinase A. J. Biol. Chem. 27919375–82
145. 145. 

     Ivanova H, Ritaine A, Wagner L, Luyten T, Shapovalov G et al. 2016. The trans-membrane domain of Bcl-2α, but not its hydrophobic cleft, is a critical determinant for efficient IP₃ receptor inhibition. Oncotarget 755704–20
146. 146. 

     Yamada M, Miyawaki A, Saito K, Nakajima T, Yamamoto-Hino M et al. 1995. The calmodulin-binding domain in the mouse type 1 inositol 1,4,5-trisphosphate receptor. Biochem. J. 308Part 183–88
147. 147. 

     Hirota J, Ando H, Hamada K, Mikoshiba K 2003. Carbonic anhydrase-related protein is a novel binding protein for inositol 1,4,5-trisphosphate receptor type 1. Biochem. J. 372435–41
148. 148. 

     Hirota J, Furuichi T, Mikoshiba K 1999. Inositol 1,4,5-trisphosphate receptor type 1 is a substrate for caspase-3 and is cleaved during apoptosis in a caspase-3-dependent manner. J. Biol. Chem. 27434433–37
149. 149. 

     Kopil CM, Vais H, Cheung KH, Siebert AP, Mak DO et al. 2011. Calpain-cleaved type 1 inositol 1,4,5-trisphosphate receptor (InsP₃R1) has InsP₃-independent gating and disrupts intracellular Ca²⁺ homeostasis. J. Biol. Chem. 28635998–6010
150. 150. 

     Schulman JJ, Wright FA, Kaufmann T, Wojcikiewicz RJ 2013. The Bcl-2 protein family member Bok binds to the coupling domain of inositol 1,4,5-trisphosphate receptors and protects them from proteolytic cleavage. J. Biol. Chem. 28825340–49
151. 151. 

     Lee B, Vermassen E, Yoon SY, Vanderheyden V, Ito J et al. 2006. Phosphorylation of IP₃R1 and the regulation of [Ca²⁺]_i responses at fertilization: a role for the MAP kinase pathway. Development 1334355–65
152. 152. 

     Zhang N, Yoon SY, Parys JB, Fissore RA 2015. Effect of M-phase kinase phosphorylations on type 1 inositol 1,4,5-trisphosphate receptor-mediated Ca²⁺ responses in mouse eggs. Cell Calcium 58476–88
153. 153. 

     Cui J, Matkovich SJ, deSouza N, Li S, Rosemblit N, Marks AR 2004. Regulation of the type 1 inositol 1,4,5-trisphosphate receptor by phosphorylation at tyrosine 353. J. Biol. Chem. 27916311–16
154. 154. 

     Kettenbach AN, Schweppe DK, Faherty BK, Pechenick D, Pletnev AA, Gerber SA 2011. Quantitative phosphoproteomics identifies substrates and functional modules of Aurora and Polo-like kinase activities in mitotic cells. Sci. Signal. 4rs5
155. 155. 

     Malathi K, Kohyama S, Ho M, Soghoian D, Li X et al. 2003. Inositol 1,4,5-trisphosphate receptor (type 1) phosphorylation and modulation by Cdc2. J. Cell. Biochem. 901186–96
156. 156. 

     Maxwell JT, Natesan S, Mignery GA 2012. Modulation of inositol 1,4,5-trisphosphate receptor type 2 channel activity by Ca²⁺/calmodulin-dependent protein kinase II (CaMKII)-mediated phosphorylation. J. Biol. Chem. 28739419–28
157. 157. 

     Daub H, Olsen JV, Bairlein M, Gnad F, Oppermann FS et al. 2008. Kinase-selective enrichment enables quantitative phosphoproteomics of the kinome across the cell cycle. Mol. Cell 31438–48
158. 158. 

     Humphrey SJ, Yang G, Yang P, Fazakerley DJ, Stockli J et al. 2013. Dynamic adipocyte phosphoproteome reveals that Akt directly regulates mTORC2. Cell Metab 171009–20
159. 159. 

     Tsai CF, Wang YT, Yen HY, Tsou CC, Ku WC et al. 2015. Large-scale determination of absolute phosphorylation stoichiometries in human cells by motif-targeting quantitative proteomics. Nat. Commun. 66622
160. 160. 

     Sliter DA, Aguiar M, Gygi SP, Wojcikiewicz RJ 2011. Activated inositol 1,4,5-trisphosphate receptors are modified by homogeneous Lys-48- and Lys-63-linked ubiquitin chains, but only Lys-48-linked chains are required for degradation. J. Biol. Chem. 2861074–82
161. 161. 

     Wagner SA, Beli P, Weinert BT, Scholz C, Kelstrup CD et al. 2012. Proteomic analyses reveal divergent ubiquitylation site patterns in murine tissues. Mol. Cell. Proteom. 111578–85
162. 162. 

     Lundby A, Lage K, Weinert BT, Bekker-Jensen DB, Secher A et al. 2012. Proteomic analysis of lysine acetylation sites in rat tissues reveals organ specificity and subcellular patterns. Cell Rep 2419–31
163. 163. 

     Haun S, Sun L, Hubrack S, Yule D, Machaca K 2012. Phosphorylation of the rat Ins(1,4,5)P₃ receptor at T930 within the coupling domain decreases its affinity to Ins(1,4,5)P₃. Channels 6379–84
164. 164. 

     Boutin B, Tajeddine N, Monaco G, Molgo J, Vertommen D et al. 2015. Endoplasmic reticulum Ca²⁺ content decrease by PKA-dependent hyperphosphorylation of type 1 IP₃ receptor contributes to prostate cancer cell resistance to androgen deprivation. Cell Calcium 57312–20
165. 165. 

     Gomez L, Thiebaut PA, Paillard M, Ducreux S, Abrial M et al. 2016. The SR/ER-mitochondria calcium crosstalk is regulated by GSK3β during reperfusion injury. Cell Death Differ 23313–22
166. 166. 

     Barresi S, Niceta M, Alfieri P, Brankovic V, Piccini G et al. 2017. Mutations in the IRBIT domain of ITPR1 are a frequent cause of autosomal dominant nonprogressive congenital ataxia. Clin. Genet. 9186–91
167. 167. 

     Ohba C, Osaka H, Iai M, Yamashita S, Suzuki Y et al. 2013. Diagnostic utility of whole exome sequencing in patients showing cerebellar and/or vermis atrophy in childhood. Neurogenetics 14225–32
168. 168. 

     Sasaki M, Ohba C, Iai M, Hirabayashi S, Osaka H et al. 2015. Sporadic infantile-onset spinocerebellar ataxia caused by missense mutations of the inositol 1,4,5-triphosphate receptor type 1 gene. J. Neurol. 2621278–84
169. 169. 

     Huang L, Chardon JW, Carter MT, Friend KL, Dudding TE et al. 2012. Missense mutations in ITPR1 cause autosomal dominant congenital nonprogressive spinocerebellar ataxia. Orphanet J. Rare Dis. 767
170. 170. 

     Hara K, Shiga A, Nozaki H, Mitsui J, Takahashi Y et al. 2008. Total deletion and a missense mutation of ITPR1 in Japanese SCA15 families. Neurology 71547–51
171. 171. 

     Yamazaki H, Nozaki H, Onodera O, Michikawa T, Nishizawa M, Mikoshiba K 2011. Functional characterization of the P1059L mutation in the inositol 1,4,5-trisphosphate receptor type 1 identified in a Japanese SCA15 family. Biochem. Biophys. Res. Commun. 410754–58
172. 172. 

     Schnekenberg RP, Perkins EM, Miller JW, Davies WI, D'Adamo MC et al. 2015. De novo point mutations in patients diagnosed with ataxic cerebral palsy. Brain 1381817–32
173. 173. 

     Hamada K, Terauchi A, Nakamura K, Higo T, Nukina N et al. 2014. Aberrant calcium signaling by transglutaminase-mediated posttranslational modification of inositol 1,4,5-trisphosphate receptors. PNAS 111E3966–75
174. 174. 

     Boulay G, Brown DM, Qin N, Jiang M, Dietrich A et al. 1999. Modulation of Ca²⁺ entry by polypeptides of the inositol 1,4,5-trisphosphate receptor (IP₃R) that bind transient receptor potential (TRP): evidence for roles of TRP and IP₃R in store depletion-activated Ca²⁺ entry. PNAS 9614955–60
175. 175. 

     Bononi A, Giorgi C, Patergnani S, Larson D, Verbruggen K et al. 2017. BAP1 regulates IP₃R3-mediated Ca²⁺ flux to mitochondria suppressing cell transformation. Nature 546549–53
176. 176. 

     Kuchay S, Giorgi C, Simoneschi D, Pagan J, Missiroli S et al. 2017. PTEN counteracts FBXL2 to promote IP₃R3- and Ca²⁺-mediated apoptosis limiting tumour growth. Nature 546554–58
177. 177. 

     Khan MT, Bhanumathy CD, Schug ZT, Joseph SK 2007. Role of inositol 1,4,5-trisphosphate receptors in apoptosis in DT40 lymphocytes. J. Biol. Chem. 28232983–90
178. 178. 

     Matsu-Ura T, Shirakawa H, Suzuki KGN, Miyamoto A, Sugiura K et al. 2019. Dual-FRET imaging of IP₃ and Ca²⁺ revealed Ca²⁺-induced IP₃ production maintains long lasting Ca²⁺ oscillations in fertilized mouse eggs. Sci. Rep. 94829
179. 179. 

     Lock JT, Alzayady KJ, Yule DI, Parker I 2018. All three IP₃ receptor isoforms generate Ca²⁺ puffs that display similar characteristics. Sci. Signal. 11eaau0344
180. 180. 

     Prole DL, Taylor CW. 2019. Structure and function of IP₃ receptors. Cold Spring Harb. Perspect. Biol. 11 https://doi.org/10.1101/cshperspect.a035063
     [Crossref]
181. 181. 

     Uhlén P, Laestadius A, Jahnukainen T, Söderblom T, Bäckhed F et al. 2000. α-Haemolysin of uropathogenic E. coli induces Ca²⁺ oscillations in renal epithelial cells. Nature 405694–97
182. 182. 

     Wang L, Wagner LE 2nd, Alzayady KJ, Yule DI 2017. Region-specific proteolysis differentially regulates type 1 inositol 1,4,5-trisphosphate receptor activity. J. Biol. Chem. 29211714–26
183. 183. 

     Miyamoto A, Miyauchi H, Kogure T, Miyawaki A, Michikawa T, Mikoshiba K 2015. Apoptosis induction-related cytosolic calcium responses revealed by the dual FRET imaging of calcium signals and caspase-3 activation in a single cell. Biochem. Biophys. Res. Commun. 46082–87
184. 184. 

     Mikoshiba K, Okano H, Tsukada Y 1985. P₄₀₀ protein characteristic to Purkinje cells and related proteins in cerebella from neuropathological mutant mice: autoradiographic study by ¹⁴C-leucine and phosphorylation. Dev. Neurosci. 7179–87
185. 185. 

     Pober JS, Sessa WC. 2007. Evolving functions of endothelial cells in inflammation. Nat. Rev. Immunol. 7803–15
186. 186. 

     Minichiello L. 2009. TrkB signalling pathways in LTP and learning. Nat. Rev. Neurosci. 10850–60
187. 187. 

     De Bock M, Wang N, Decrock E, Bol M, Gadicherla AK et al. 2013. Endothelial calcium dynamics, connexin channels and blood-brain barrier function. Prog. Neurobiol. 1081–20
188. 188. 

     Feske S, Skolnik EY, Prakriya M 2012. Ion channels and transporters in lymphocyte function and immunity. Nat. Rev. Immunol. 12532–47