Inositol 1,4,5-trisphosphate receptors in the endoplasmic reticulum: A single-channel point of view.

As an intracellular Ca(2+) release channel at the endoplasmic reticulum membrane, the ubiquitous inositol 1,4,5-trisphosphate (InsP3) receptor (InsP3R) plays a crucial role in the generation, propagation and regulation of intracellular Ca(2+) signals that regulate numerous physiological and pathophysiological processes. This review provides a concise account of the fundamental single-channel properties of the InsP3R channel: its conductance properties and its regulation by InsP3 and Ca(2+), its physiological ligands, studied using nuclear patch clamp electrophysiology.

[1]  A. M. Riley,et al.  Synthetic partial agonists reveal key steps in IP3 receptor activation , 2009, Nature chemical biology.

[2]  J. Watras,et al.  Inositol 1,4,5-trisphosphate activates a channel from smooth muscle sarcoplasmic reticulum , 1988, Nature.

[3]  M. Fill,et al.  Identification and Functional Reconstitution of the Type 2 Inositol 1,4,5-Trisphosphate Receptor from Ventricular Cardiac Myocytes* , 1997, The Journal of Biological Chemistry.

[4]  Colin W. Taylor,et al.  Structural organization of signalling to and from IP3 receptors. , 2014, Biochemical Society transactions.

[5]  J. Watras,et al.  Inositol 1,4,5-Trisphosphate (InsP3) and Calcium Interact to Increase the Dynamic Range of InsP3 Receptor-dependent Calcium Signaling , 1997, The Journal of general physiology.

[6]  S. Morris,et al.  Expression of inositol trisphosphate receptors. , 1999, Cell calcium.

[7]  M. Betzenhauser,et al.  ATP Regulation of Type-1 Inositol 1,4,5-Trisphosphate Receptor Activity Does Not Require Walker A-type ATP-binding Motifs* , 2009, The Journal of Biological Chemistry.

[8]  S. Ludtke,et al.  Single-particle cryo-EM of calcium release channels: structural validation. , 2013, Current opinion in structural biology.

[9]  D. Mak,et al.  Single-channel recordings of recombinant inositol trisphosphate receptors in mammalian nuclear envelope. , 2001, Biophysical journal.

[10]  J. Foskett,et al.  Novel Regulation of Calcium Inhibition of the Inositol 1,4,5-trisphosphate Receptor Calcium-release Channel , 2003, The Journal of general physiology.

[11]  Ian Parker,et al.  Imaging the quantal substructure of single IP3R channel activity during Ca2+ puffs in intact mammalian cells , 2009, Proceedings of the National Academy of Sciences.

[12]  D. Boehning Molecular architecture of the inositol 1,4,5-trisphosphate receptor pore. , 2010, Current topics in membranes.

[13]  K. Mikoshiba,et al.  Molecular Basis of the Isoform-specific Ligand-binding Affinity of Inositol 1,4,5-Trisphosphate Receptors* , 2007, Journal of Biological Chemistry.

[14]  Ian Parker,et al.  Modeling Ca2+ feedback on a single inositol 1,4,5-trisphosphate receptor and its modulation by Ca2+ buffers. , 2008, Biophysical journal.

[15]  M. J. Berridge,et al.  Release of Ca2+ from a nonmitochondrial intracellular store in pancreatic acinar cells by inositol-1,4,5-trisphosphate , 1983, Nature.

[16]  S. W. Sernett,et al.  Isolation, characterization, and localization of the inositol 1,4,5-trisphosphate receptor protein in Xenopus laevis oocytes. , 1992, The Journal of biological chemistry.

[17]  S. Orrenius,et al.  ATP stimulates Ca2+ uptake and increases the free Ca2+ concentration in isolated rat liver nuclei. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[18]  M. Betzenhauser,et al.  Regulation of inositol 1,4,5-trisphosphate receptors by phosphorylation and adenine nucleotides. , 2010, Current topics in membranes.

[19]  M. Ikura,et al.  Intracellular calcium channels: inositol-1,4,5-trisphosphate receptors. , 2014, European journal of pharmacology.

[20]  Martin Falcke,et al.  Clustering of IP3 receptors by IP3 retunes their regulation by IP3 and Ca2+ , 2009, Nature.

[21]  J. Foskett,et al.  Graded recruitment and inactivation of single InsP3 receptor Ca2+‐release channels: implications for quartal Ca2+release , 2006, The Journal of physiology.

[22]  Barbara E. Ehrlich,et al.  Type III InsP3 receptor channel stays open in the presence of increased calcium , 1998, Nature.

[23]  J. Foskett,et al.  Atp Regulation of Recombinant Type 3 Inositol 1,4,5-Trisphosphate Receptor Gating , 2001, The Journal of general physiology.

[24]  O. Fedorenko,et al.  Ion channels of the nuclear membrane of hippocampal neurons , 2014, Hippocampus.

[25]  James Watras,et al.  Bell-shaped calcium-response curves of lns(l,4,5)P3- and calcium-gated channels from endoplasmic reticulum of cerebellum , 1991, Nature.

[26]  D. Yule,et al.  Differential regulation of the InsP3 receptor type‐1 and ‐2 single channel properties by InsP3, Ca2+ and ATP , 2012, The Journal of physiology.

[27]  T. Kurosaki,et al.  Genetic evidence for involvement of type 1, type 2 and type 3 inositol 1,4,5‐trisphosphate receptors in signal transduction through the B‐cell antigen receptor , 1997, The EMBO journal.

[28]  D. Gillespie,et al.  Intracellular calcium release channels mediate their own countercurrent: the ryanodine receptor case study. , 2008, Biophysical journal.

[29]  S. Caenepeel,et al.  Single channel function of recombinant type-1 inositol 1,4,5-trisphosphate receptor ligand binding domain splice variants. , 1998, Biophysical journal.

[30]  Marja-Leena Linne,et al.  Comparison of Models for IP3 Receptor Kinetics Using Stochastic Simulations , 2013, PloS one.

[31]  J. Putney,et al.  The inositol phosphate-calcium signaling system in nonexcitable cells. , 1993, Endocrine reviews.

[32]  T. Iwatsubo,et al.  Gain-of-Function Enhancement of IP3 Receptor Modal Gating by Familial Alzheimer’s Disease–Linked Presenilin Mutants in Human Cells and Mouse Neurons , 2010, Science Signaling.

[33]  P. Kostyuk,et al.  Spontaneously active and InsP3‐activated ion channels in cell nuclei from rat cerebellar Purkinje and granule neurones , 2005, The Journal of physiology.

[34]  M. Berridge Inositol trisphosphate and calcium signalling , 1993, Nature.

[35]  I. Bezprozvanny,et al.  Inositol (1,4,5)-trisphosphate (InsP3)-gated Ca channels from cerebellum: conduction properties for divalent cations and regulation by intraluminal calcium , 1994, The Journal of general physiology.

[36]  R. Wojcikiewicz,et al.  Type I, II, and III inositol 1,4,5-trisphosphate receptors are unequally susceptible to down-regulation and are expressed in markedly different proportions in different cell types , 1995, The Journal of Biological Chemistry.

[37]  D. Mak,et al.  Effects of divalent cations on single-channel conduction properties of Xenopus IP3 receptor. , 1998, The American journal of physiology.

[38]  I. Parker,et al.  Role of cytosolic Ca2+ in inhibition of InsP3‐evoked Ca2+ release in Xenopus oocytes. , 1994, The Journal of physiology.

[39]  S. Muallem,et al.  Hormone-evoked calcium release from intracellular stores is a quantal process. , 1989, The Journal of biological chemistry.

[40]  D. Gillespie Energetics of divalent selectivity in a calcium channel: the ryanodine receptor case study. , 2008, Biophysical journal.

[41]  D. Mak,et al.  Single-channel inositol 1,4,5-trisphosphate receptor currents revealed by patch clamp of isolated Xenopus oocyte nuclei. , 1994, The Journal of biological chemistry.

[42]  D. Clapham,et al.  Calcium release from the nucleus by InsP3 receptor channels , 1995, Neuron.

[43]  Ian Parker,et al.  Mode Switching Is the Major Mechanism of Ligand Regulation of InsP3 Receptor Calcium Release Channels , 2007, The Journal of general physiology.

[44]  Don-On Daniel Mak,et al.  Patch-clamp electrophysiology of intracellular Ca2+ channels. , 2013, Cold Spring Harbor protocols.

[45]  J. Foskett,et al.  InsP3R channel gating altered by clustering? , 2011, Nature.

[46]  S. G. Dedos,et al.  Counting Functional Inositol 1,4,5-Trisphosphate Receptors into the Plasma Membrane* , 2008, Journal of Biological Chemistry.

[47]  Zhongming Ma,et al.  Redox-regulated heterogeneous thresholds for ligand recruitment among InsP3R Ca2+-release channels. , 2010, Biophysical journal.

[48]  M. Betzenhauser,et al.  Protein Kinase A Increases Type-2 Inositol 1,4,5-Trisphosphate Receptor Activity by Phosphorylation of Serine 937* , 2009, The Journal of Biological Chemistry.

[49]  J. Foskett,et al.  Regulation of IP(3)R Channel Gating by Ca(2+) and Ca(2+) Binding Proteins. , 2010, Current topics in membranes.

[50]  G. Tall,et al.  Functional Inositol 1,4,5-Trisphosphate Receptors Assembled from Concatenated Homo- and Heteromeric Subunits*♦ , 2013, The Journal of Biological Chemistry.

[51]  Don-On Daniel Mak,et al.  Inositol 1,4,5-tris-phosphate activation of inositol tris-phosphate receptor Ca2+ channel by ligand tuning of Ca2+ inhibition , 1998 .

[52]  Don-On Daniel Mak,et al.  Single-Channel Kinetics, Inactivation, and Spatial Distribution of Inositol Trisphosphate (IP3) Receptors in Xenopus Oocyte Nucleus , 1997, The Journal of general physiology.

[53]  K. Mikoshiba,et al.  ATP Modulation of Ca2+ Release by Type-2 and Type-3 Inositol (1, 4, 5)-Triphosphate Receptors , 2008, Journal of Biological Chemistry.

[54]  P. Lipp,et al.  A hierarchical concept of cellular and subcellular Ca(2+)-signalling. , 1996, Progress in biophysics and molecular biology.

[55]  Colin W. Taylor,et al.  Dynamic regulation of IP3 receptor clustering and activity by IP3 , 2009, Channels.

[56]  Don-On Daniel Mak,et al.  Single-Channel Properties in Endoplasmic Reticulum Membrane of Recombinant Type 3 Inositol Trisphosphate Receptor , 2000, The Journal of general physiology.

[57]  M. Betzenhauser,et al.  Linking structure to function: Recent lessons from inositol 1,4,5-trisphosphate receptor mutagenesis. , 2010, Cell calcium.

[58]  J. Foskett,et al.  Regulation by Ca2+ and Inositol 1,4,5-Trisphosphate (Insp3) of Single Recombinant Type 3 Insp3 Receptor Channels , 2001, The Journal of general physiology.

[59]  Suman Datta,et al.  Rapid ligand‐regulated gating kinetics of single inositol 1,4,5‐trisphosphate receptor Ca2+ release channels , 2007, EMBO reports.

[60]  E. Morris,et al.  Molecular Characterization of the Inositol 1,4,5-Trisphosphate Receptor Pore-forming Segment* , 2008, Journal of Biological Chemistry.

[61]  Martin Falcke,et al.  A kinetic model of the inositol trisphosphate receptor based on single-channel data. , 2009, Biophysical journal.

[62]  J. Kevin Foskett,et al.  Unitary Ca2+ current through recombinant type 3 InsP3 receptor channels under physiological ionic conditions , 2010, The Journal of general physiology.

[63]  B. Eisenberg,et al.  Calcium Ion Permeation through the Calcium Release Channel (Ryanodine Receptor) of Cardiac Muscle , 2003 .

[64]  Don-On Daniel Mak,et al.  Inositol trisphosphate receptor Ca2+ release channels. , 2007, Physiological reviews.

[65]  J. Pearson,et al.  Permeant calcium ion feed-through regulation of single inositol 1,4,5-trisphosphate receptor channel gating , 2012, The Journal of general physiology.

[66]  Larry E Wagner,et al.  Regulation of single inositol 1,4,5‐trisphosphate receptor channel activity by protein kinase A phosphorylation , 2008, The Journal of physiology.

[67]  C. Hidalgo,et al.  Contribution of Ca2+ release channels to hippocampal synaptic plasticity and spatial memory: potential redox modulation. , 2014, Antioxidants & redox signaling.

[68]  Ilya Bezprozvanny,et al.  Modulation of Type 1 Inositol (1,4,5)-Trisphosphate Receptor Function by Protein Kinase A and Protein Phosphatase 1α , 2003, The Journal of Neuroscience.

[69]  M Montal,et al.  Formation of bimolecular membranes from lipid monolayers and a study of their electrical properties. , 1972, Proceedings of the National Academy of Sciences of the United States of America.

[70]  M. Berridge,et al.  Elementary and global aspects of calcium signalling. , 1997, The Journal of experimental biology.

[71]  Colin W. Taylor,et al.  Ca2+ Entry Through Plasma Membrane IP3 Receptors , 2006, Science.

[72]  J. Foskett,et al.  Nuclear Patch Clamp Electrophysiology of Inositol Trisphosphate Receptor Ca2+ Release Channels , 2005 .

[73]  Ghanim Ullah,et al.  A data-driven model of a modal gated ion channel: The inositol 1,4,5-trisphosphate receptor in insect Sf9 cells , 2012, The Journal of general physiology.

[74]  G. Warnecke,et al.  Calcium domains around single and clustered IP3 receptors and their modulation by buffers. , 2010, Biophysical journal.

[75]  Edmund J Crampin,et al.  A kinetic model for type I and II IP3R accounting for mode changes. , 2012, Biophysical journal.

[76]  J. Foskett,et al.  Patch-clamp electrophysiology of intracellular Ca2+ channels. , 2013, Cold Spring Harbor protocols.

[77]  S. Joseph Role of thiols in the structure and function of inositol trisphosphate receptors. , 2010, Current topics in membranes.

[78]  M Fill,et al.  Isoform-specific function of single inositol 1,4,5-trisphosphate receptor channels. , 1998, Biophysical journal.

[79]  Ian Parker,et al.  Ca2+ Puffs Originate from Preestablished Stable Clusters of Inositol Trisphosphate Receptors , 2009, Science Signaling.

[80]  C Dingwall,et al.  The nuclear membrane. , 1992, Science.

[81]  I. Parker,et al.  Single-molecule tracking of inositol trisphosphate receptors reveals different motilities and distributions. , 2014, Biophysical journal.