Calcium signaling in the ER: its role in neuronal plasticity and neurodegenerative disorders

Endoplasmic reticulum (ER) is a multifaceted organelle that regulates protein synthesis and trafficking, cellular responses to stress, and intracellular Ca2+ levels. In neurons, it is distributed between the cellular compartments that regulate plasticity and survival, which include axons, dendrites, growth cones and synaptic terminals. Intriguing communication networks between ER, mitochondria and plasma membrane are being revealed that provide mechanisms for the precise regulation of temporal and spatial aspects of Ca2+ signaling. Alterations in Ca2+ homeostasis in ER contribute to neuronal apoptosis and excitotoxicity, and are being linked to the pathogenesis of several different neurodegenerative disorders, including Alzheimer's disease and stroke.

[1]  L. Jaffe The path of calcium in cytosolic calcium oscillations: a unifying hypothesis. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[2]  K. Mikoshiba,et al.  The calmodulin-binding domain in the mouse type 1 inositol 1,4,5-trisphosphate receptor. , 1995, The Biochemical journal.

[3]  P. Stanton,et al.  Induction of Hippocampal Long-Term Depression Requires Release of Ca2+ from Separate Presynaptic and Postsynaptic Intracellular Stores , 1996, The Journal of Neuroscience.

[4]  S. Snyder,et al.  FKBP12 Binds the Inositol 1,4,5-Trisphosphate Receptor at Leucine-Proline (1400–1401) and Anchors Calcineurin to this FK506-like Domain* , 1997, The Journal of Biological Chemistry.

[5]  M. Mattson,et al.  Increased vulnerability of hippocampal neurons from presenilin-1 mutant knock-in mice to amyloid beta-peptide toxicity: central roles of superoxide production and caspase activation. , 2008, Journal of neurochemistry.

[6]  I. Módy,et al.  NMDA receptor-dependent excitotoxicity: the role of intracellular Ca2+ release. , 1995, Trends in pharmacological sciences.

[7]  M. Mattson,et al.  Caspase and calpain substrates: Roles in synaptic plasticity and cell death , 1999, Journal of neuroscience research.

[8]  S. Snyder,et al.  Calcineurin associated with the inositol 1,4,5-trisphosphate receptor-FKBP12 complex modulates Ca2+ flux , 1995, Cell.

[9]  Miles W. Miller,et al.  Increased vulnerability of hippocampal neurons to excitotoxic necrosis in presenilin-1 mutant knock-in mice , 1999, Nature Medicine.

[10]  P. Carlen,et al.  Seizure-induced cell death produced by repeated tetanic stimulation in vitro: possible role of endoplasmic reticulum calcium stores. , 1999, Journal of neurophysiology.

[11]  G. Schellenberg,et al.  Presenilin‐1 mutation alters NGF‐induced neurite outgrowth, calcium homeostasis, and transcription factor (AP‐1) activation in PC12 cells , 1998, Journal of neuroscience research.

[12]  Role of calcium in the activation of erp72 and heme oxygenase-1 expression on depletion of endoplasmic reticulum calcium stores in rat neuronal cell culture , 1998, Neuroscience Letters.

[13]  Huafeng Wei,et al.  Dantrolene Is Cytoprotective in Two Models of Neuronal Cell Death , 1996, Journal of neurochemistry.

[14]  T. Crow,et al.  Loss of endoplasmic reticulum-associated enzymes in affected brain regions in Huntington's disease and Alzheimer-type dementia , 1985, Journal of the Neurological Sciences.

[15]  J. Nagy,et al.  Autoradiographic analysis of [3H]ryanodine binding sites in rat brain: Regional distribution and the effects of lesions on sites in the hippocampus , 1992, Journal of Chemical Neuroanatomy.

[16]  C. Cotman,et al.  Alzheimer's Presenilin-1 Mutation Potentiates Inositol 1,4,5-Trisphosphate-Mediated Calcium Signaling in Xenopus , 1999 .

[17]  S. B. Kater,et al.  ATP Released from Astrocytes Mediates Glial Calcium Waves , 1999, The Journal of Neuroscience.

[18]  M. Mattson,et al.  Altered Calcium Homeostasis and Mitochondrial Dysfunction in Cortical Synaptic Compartments of Presenilin‐1 Mutant Mice , 1999, Journal of neurochemistry.

[19]  L Manzo,et al.  Neuronal cell death: a demise with different shapes. , 1999, Trends in pharmacological sciences.

[20]  Arthur Konnerth,et al.  A new class of synaptic response involving calcium release in dendritic spines , 1998, Nature.

[21]  M. Mattson,et al.  Par-4 is a mediator of neuronal degeneration associated with the pathogenesis of Alzheimer disease , 1998, Nature Medicine.

[22]  J Rinzel,et al.  Ca2+ excitability of the ER membrane: an explanation for IP3-induced Ca2+ oscillations. , 1995, The American journal of physiology.

[23]  M. Mattson Neurotransmitters in the regulation of neuronal cytoarchitecture , 1988, Brain Research Reviews.

[24]  R. Leapman,et al.  Activity-Dependent Calcium Sequestration in Dendrites of Hippocampal Neurons in Brain Slices , 1997, The Journal of Neuroscience.

[25]  E. Rojas,et al.  Endoplasmic Reticulum as a Source of Ca2+ in Neurotransmitter Secretion , 1991, Annals of the New York Academy of Sciences.

[26]  J. Nagy,et al.  [3H]Ryanodine binding sites in rat brain demonstrated by membrane binding and autoradiography , 1991, Brain Research.

[27]  M. Mattson,et al.  Calbindin D28k blocks the proapoptotic actions of mutant presenilin 1: reduced oxidative stress and preserved mitochondrial function. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[28]  T. Deerinck,et al.  Differential distribution and subcellular localization of ryanodine receptor isoforms in the chicken cerebellum during development , 1997, Brain Research.

[29]  D. Langley,et al.  Specialized distributions of mitochondria and endoplasmic reticulum proteins define Ca2+ wave amplification sites in cultured astrocytes , 1998, Journal of neuroscience research.

[30]  M. Mattson,et al.  Alzheimer's PS‐1 mutation perturbs calcium homeostasis and sensitizes PC12 cells to death induced by amyloid β‐peptide , 1996, Neuroreport.

[31]  C. Armstrong,et al.  Induction of long-term depression and rebound potentiation by inositol trisphosphate in cerebellar Purkinje neurons. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[32]  J. Bockaert,et al.  Functional coupling between ryanodine receptors and L-type calcium channels in neurons , 1996, Nature.

[33]  E. Clementi,et al.  Caffeine-induced transmitter release is mediated via ryanodine-sensitive channel , 1994, Neuroscience Letters.

[34]  Robert E. Davis,et al.  Altered Calcium Homeostasis in Cells Transformed by Mitochondria from Individuals with Parkinson's Disease , 1997, Journal of neurochemistry.

[35]  George J. Augustine,et al.  Local calcium signalling by inositol-1,4,5-trisphosphate in Purkinje cell dendrites , 1998, Nature.

[36]  M. Mattson,et al.  Neurotrophic factor mediated protection from excitotoxicity and disturbances in calcium and free radical metabolism , 1993 .

[37]  K. Kohno,et al.  Conformational changes of the smooth endoplasmic reticulum are facilitated by L‐glutamate and its receptors in rat Purkinje cells , 1998, The Journal of comparative neurology.

[38]  Y. Tashiro,et al.  Rough surfaced smooth endoplasmic reticulum in rat and mouse cerebellar Purkinje cells visualized by quick-freezing techniques. , 1998, Cell structure and function.

[39]  M. Mattson,et al.  Alzheimer’s Presenilin Mutation Sensitizes Neural Cells to Apoptosis Induced by Trophic Factor Withdrawal and Amyloid β-Peptide: Involvement of Calcium and Oxyradicals , 1997, The Journal of Neuroscience.

[40]  Lawrence M. Lifshitz,et al.  Close contacts with the endoplasmic reticulum as determinants of mitochondrial Ca2+ responses. , 1998, Science.

[41]  S. Snyder,et al.  Differential immunohistochemical localization of inositol 1,4,5- trisphosphate- and ryanodine-sensitive Ca2+ release channels in rat brain , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[42]  K. Mikoshiba,et al.  Ca2+ release from Ca2+ stores, particularly from ryanodine-sensitive Ca2+ stores, is required for the induction of LTD in cultured cerebellar Purkinje cells. , 1995, Journal of neurophysiology.

[43]  J. B. Hutchins,et al.  Bcl‐2 Protects Isolated Plasma and Mitochondrial Membranes Against Lipid Peroxidation Induced by Hydrogen Peroxide and Amyloid β‐Peptide , 1998, Journal of neurochemistry.

[44]  G. Banker,et al.  An electron microscopic analysis of hippocampal neurons developing in culture: early stages in the emergence of polarity , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[45]  Steven G. Clarke,et al.  Role of ERAB/l-3-Hydroxyacyl-coenzyme A Dehydrogenase Type II Activity in Aβ-induced Cytotoxicity* , 1999, The Journal of Biological Chemistry.

[46]  M. Mattson,et al.  Evidence for the involvement of TNF and NF‐κB in hippocampal synaptic plasticity , 2000, Synapse.

[47]  J. Nagy,et al.  Subcellular localization of ryanodine receptors in rat brain. , 1996, European journal of pharmacology.

[48]  S A Kuznetsov,et al.  Transport of ER vesicles on actin filaments in neurons by myosin V. , 1998, Journal of cell science.

[49]  D. Bredesen,et al.  Bcl‐2 Protects Against Apoptosis in Neuronal Cell Line Caused by Thapsigargin‐Induced Depletion of Intracellular Calcium Stores , 1998, Journal of neurochemistry.

[50]  V. Pickel,et al.  Ultrastructural localization of sorcin, a 22 kDa calcium binding protein, in the rat caudate‐putamen nucleus: Association with ryanodine receptors and intracellular calcium release , 1997, The Journal of comparative neurology.

[51]  M. Mattson,et al.  ■ REVIEW : The Presenilins , 1999 .

[52]  T. Reese,et al.  Polarized compartmentalization of organelles in growth cones from developing optic tectum , 1985, The Journal of cell biology.

[53]  P. Fossier,et al.  Involvement of Ca2+ uptake by a reticulum-like store in the control of transmitter release , 1992, Neuroscience.

[54]  M. Mattson Acetylcholine potentiates glutamate-induced neurodegeneration in cultured hippocampal neurons , 1989, Brain Research.

[55]  G Raisman,et al.  Expression of type 1 inositol 1,4,5-trisphosphate receptor during axogenesis and synaptic contact in the central and peripheral nervous system of developing rat. , 1996, Development.

[56]  M. Mattson,et al.  Presenilins, the Endoplasmic Reticulum, and Neuronal Apoptosis in Alzheimer's Disease , 1998, Journal of neurochemistry.

[57]  M. Mattson,et al.  Astrocytic Gap Junctional Communication Decreases Neuronal Vulnerability to Oxidative Stress‐Induced Disruption of Ca2+ Homeostasis and Cell Death , 1998, Journal of neurochemistry.

[58]  A. Martínez-Serrano,et al.  Caffeine-sensitive calcium stores in presynaptic nerve endings: a physiological role? , 1989, Biochemical and biophysical research communications.

[59]  Huiling He,et al.  Maintenance of Calcium Homeostasis in the Endoplasmic Reticulum by Bcl-2 , 1997, The Journal of cell biology.

[60]  E. Salmon,et al.  Endoplasmic reticulum membrane tubules are distributed by microtubules in living cells using three distinct mechanisms , 1998, Current Biology.

[61]  F. LaFerla,et al.  Presenilin-2 Mutations Modulate Amplitude and Kinetics of Inositol 1,4,5-Trisphosphate-mediated Calcium Signals* , 1999, The Journal of Biological Chemistry.

[62]  D. Linden,et al.  Synaptic Transmission and Hippocampal Long-Term Potentiation in Transgenic Mice Expressing FAD-Linked Presenilin 1 , 1999, Neurobiology of Disease.

[63]  L. Bourguignon,et al.  Identification of the Ankyrin-binding Domain of the Mouse T-lymphoma Cell Inositol 1,4,5-Trisphosphate (IP3) Receptor and Its Role in the Regulation of IP3-mediated Internal Ca2+ Release (*) , 1995, The Journal of Biological Chemistry.

[64]  S. B. Kater,et al.  Calcium regulation of the neuronal growth cone , 1988, Trends in Neurosciences.

[65]  W. Abraham,et al.  Immediate early gene transcription and synaptic modulation , 1999, Journal of neuroscience research.

[66]  J. Buxbaum,et al.  Calsenilin: A calcium-binding protein that interacts with the presenilins and regulates the levels of a presenilin fragment , 1998, Nature Medicine.

[67]  M. F. Schneider,et al.  Caffeine‐induced [Ca2+] oscillations in neurones of frog sympathetic ganglia , 1999, The Journal of physiology.

[68]  A. Marks,et al.  Stabilization of calcium release channel (ryanodine receptor) function by FK506-binding protein , 1994, Cell.

[69]  Peter Lipp,et al.  Cooking with Calcium: The Recipes for Composing Global Signals from Elementary Events , 1997, Cell.

[70]  S. Waxman,et al.  Blocking Ca2+ mobilization with thapsigargin reduces neurite initiation in cultured adult rat DRG neurons. , 1995, Brain research. Developmental brain research.

[71]  A. Schousboe,et al.  Dantrolene Prevents Glutamate Cytotoxicity and Ca2+ Release from Intracellular Stores in Cultured Cerebral Cortical Neurons , 1991, Journal of neurochemistry.

[72]  T. Takadera,et al.  Apoptotic cell death and CPP32-like activation induced by thapsigargin and their prevention by nerve growth factor in PC12 cells. , 1998, Biochimica et biophysica acta.

[73]  B. Pettmann,et al.  Neuronal Cell Death , 1998, Neuron.

[74]  E. Korkotian,et al.  Elevation of Intracellular Glucosylceramide Levels Results in an Increase in Endoplasmic Reticulum Density and in Functional Calcium Stores in Cultured Neurons* , 1999, The Journal of Biological Chemistry.

[75]  M. Berridge Neuronal Calcium Signaling , 1998, Neuron.

[76]  C. Culmsee,et al.  Roles of Nuclear Factor κB in Neuronal Survival and Plasticity , 2000 .

[77]  M. Mattson,et al.  The Endoplasmic Reticulum Stress-Responsive Protein GRP78 Protects Neurons Against Excitotoxicity and Apoptosis: Suppression of Oxidative Stress and Stabilization of Calcium Homeostasis , 1999, Experimental Neurology.

[78]  M. Stein,et al.  High affinity [3H]ryanodine binding sites in postmortem human brain: regional distribution and effects of calcium, magnesium and caffeine , 1992, Brain Research.

[79]  G. Hajnóczky,et al.  Quasi‐synaptic calcium signal transmission between endoplasmic reticulum and mitochondria , 1999, The EMBO journal.

[80]  G. Schellenberg,et al.  Secreted amyloid β–protein similar to that in the senile plaques of Alzheimer's disease is increased in vivo by the presenilin 1 and 2 and APP mutations linked to familial Alzheimer's disease , 1996, Nature Medicine.

[81]  James D. Lechleiter,et al.  Differential Modulation of SERCA2 Isoforms by Calreticulin , 1998, The Journal of cell biology.

[82]  P. S. St George-Hyslop,et al.  Developmental Expression of Wild-Type and Mutant Presenilin-1 in Hippocampal Neurons from Transgenic Mice: Evidence for Novel Species-Specific Properties of Human Presenilin-1 , 1999, Molecular medicine.

[83]  M. Dailey,et al.  Dynamics of the endoplasmic reticulum and other membranous organelles in growth cones of cultured neurons , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.