The Role of Striatal-Enriched Protein Tyrosine Phosphatase (STEP) in Cognition

Striatal-enriched protein tyrosine phosphatase (STEP) has recently been implicated in several neuropsychiatric disorders with significant cognitive impairments, including Alzheimer’s disease, schizophrenia, and fragile X syndrome. A model has emerged by which STEP normally opposes the development of synaptic strengthening and that disruption in STEP activity leads to aberrant synaptic function. We review the mechanisms by which STEP contributes to the etiology of these and other neuropsychiatric disorders. These findings suggest that disruptions in STEP activity may be a common mechanism for cognitive impairments in diverse illnesses.

[1]  M. Bear,et al.  Role for rapid dendritic protein synthesis in hippocampal mGluR-dependent long-term depression. , 2000, Science.

[2]  L. Lue,et al.  Soluble Amyloid β Peptide Concentration as a Predictor of Synaptic Change in Alzheimer’s Disease , 1999 .

[3]  D. Salmon,et al.  Physical basis of cognitive alterations in alzheimer's disease: Synapse loss is the major correlate of cognitive impairment , 1991, Annals of neurology.

[4]  Angus C Nairn,et al.  Regulation of a protein phosphatase cascade allows convergent dopamine and glutamate signals to activate ERK in the striatum. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[5]  C. Portera-Cailliau,et al.  Delayed Stabilization of Dendritic Spines in Fragile X Mice , 2010, The Journal of Neuroscience.

[6]  S B Dunnett,et al.  Abnormal Synaptic Plasticity and Impaired Spatial Cognition in Mice Transgenic for Exon 1 of the Human Huntington's Disease Mutation , 2000, The Journal of Neuroscience.

[7]  P. Lombroso,et al.  Striatal Enriched Phosphatase 61 Dephosphorylates Fyn at Phosphotyrosine 420* , 2002, The Journal of Biological Chemistry.

[8]  M. Shamloo,et al.  Persistent Phosphorylation of Synaptic Proteins following Middle Cerebral Artery Occlusion , 2002, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[9]  J. Penney,et al.  Differential loss of striatal projection neurons in Huntington disease. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[10]  M. Bear,et al.  LTP and LTD An Embarrassment of Riches , 2004, Neuron.

[11]  W. Klein,et al.  Abeta oligomer-induced aberrations in synapse composition, shape, and density provide a molecular basis for loss of connectivity in Alzheimer's disease. , 2007, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[12]  S. W. Davies,et al.  Altered brain neurotransmitter receptors in transgenic mice expressing a portion of an abnormal human huntington disease gene. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[13]  F. Crews,et al.  Chronic Ethanol Exposure Potentiates NMDA Excitotoxicity in Cerebral Cortical Neurons , 1993, Journal of neurochemistry.

[14]  W. Greenough,et al.  Dendritic spine structural anomalies in fragile-X mental retardation syndrome. , 2000, Cerebral cortex.

[15]  Karl J. Friston,et al.  Dopaminergic modulation of impaired cognitive activation in the anterior cingulate cortex in schizophrenia , 1995, Nature.

[16]  C A Ross,et al.  Expansion of polyglutamine repeat in huntingtin leads to abnormal protein interactions involving calmodulin. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[17]  M. Shamloo,et al.  Expression and function of striatal enriched protein tyrosine phosphatase is profoundly altered in cerebral ischemia , 2008, The European journal of neuroscience.

[18]  R. Carroll,et al.  Metabotropic Glutamate Receptor Activation Regulates Fragile X Mental Retardation Protein and Fmr1 mRNA Localization Differentially in Dendrites and at Synapses , 2004, The Journal of Neuroscience.

[19]  P. Randall,et al.  Acute ethanol affects phosphorylation state of the NMDA receptor complex: implication of tyrosine phosphatases and protein kinase A. , 2003, Brain research. Molecular brain research.

[20]  R. A. Crowther,et al.  Multiple isoforms of human microtubule-associated protein tau: sequences and localization in neurofibrillary tangles of Alzheimer's disease , 1989, Neuron.

[21]  R. Radcliffe,et al.  Alcohol inhibition of the NMDA receptor function, long-term potentiation, and fear learning requires striatal-enriched protein tyrosine phosphatase , 2011, Proceedings of the National Academy of Sciences.

[22]  Alejandra del C. Alonso,et al.  Alzheimer's disease hyperphosphorylated tau sequesters normal tau into tangles of filaments and disassembles microtubules , 1996, Nature Medicine.

[23]  J. Becker,et al.  Cognitive deficits and clinical diagnosis of Alzheimer's disease , 1987, Neurology.

[24]  G. Kaplan,et al.  Antipsychotics regulate cyclic AMP-dependent protein kinase and phosphorylated cyclic AMP response element-binding protein in striatal and cortical brain regions in mice , 2004, Neuroscience Letters.

[25]  D. Javitt,et al.  Efficacy of high-dose glycine in the treatment of enduring negative symptoms of schizophrenia. , 1999, Archives of general psychiatry.

[26]  P. Calabresi,et al.  Dopaminergic control of synaptic plasticity in the dorsal striatum , 2001, The European journal of neuroscience.

[27]  J. Lucas,et al.  Striatal-Enriched Protein Tyrosine Phosphatase Expression and Activity in Huntington's Disease: A STEP in the Resistance to Excitotoxicity , 2011, The Journal of Neuroscience.

[28]  K. Davies,et al.  Phospho-regulation of synaptic and extrasynaptic N-methyl-d-aspartate receptors in adult hippocampal slices , 2009, Neuroscience.

[29]  P. S. St George-Hyslop,et al.  Amyloid beta protein gene: cDNA, mRNA distribution, and genetic linkage near the Alzheimer locus. , 1987, Science.

[30]  S. Hirsch,et al.  NMDA receptor mRNA correlation with antemortem cognitive impairment in schizophrenia. , 1996, Neuroreport.

[31]  I. Weiler,et al.  Abnormal dendritic spines in fragile X knockout mice: maturation and pruning deficits. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[32]  D. Arciniegas,et al.  Cognitive sequelae of hypoxic-ischemic brain injury: a review. , 2010, NeuroRehabilitation.

[33]  Alcino J. Silva,et al.  Molecular and cellular cognitive studies of the role of synaptic plasticity in memory. , 2003, Journal of neurobiology.

[34]  Peter K. Todd,et al.  The fragile X mental retardation protein is required for type-I metabotropic glutamate receptor-dependent translation of PSD-95 , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[35]  J. Lucas,et al.  Reduced calcineurin protein levels and activity in exon-1 mouse models of Huntington's disease: Role in excitotoxicity , 2009, Neurobiology of Disease.

[36]  I. Weiler,et al.  Synaptic synthesis of the Fragile X protein: possible involvement in synapse maturation and elimination. , 1999, American journal of medical genetics.

[37]  Stephen T Warren,et al.  Fragile X Syndrome: An Update and Review for the Primary Pediatrician , 2005, Clinical pediatrics.

[38]  W. Klein,et al.  Aβ Oligomer-Induced Aberrations in Synapse Composition, Shape, and Density Provide a Molecular Basis for Loss of Connectivity in Alzheimer's Disease , 2007, The Journal of Neuroscience.

[39]  K. Nikolich,et al.  Regulation of NMDA receptor trafficking and function by striatal‐enriched tyrosine phosphatase (STEP) , 2006, The European journal of neuroscience.

[40]  S. Younkin,et al.  Release of excess amyloid beta protein from a mutant amyloid beta protein precursor. , 1993, Science.

[41]  R. Pulido,et al.  Differential interaction of the tyrosine phosphatases PTP-SL, STEP and HePTP with the mitogen-activated protein kinases ERK1/2 and p38alpha is determined by a kinase specificity sequence and influenced by reducing agents. , 2003, The Biochemical journal.

[42]  D. Winder,et al.  NMDA and β1-Adrenergic Receptors Differentially Signal Phosphorylation of Glutamate Receptor Type 1 in Area CA1 of Hippocampus , 2003, The Journal of Neuroscience.

[43]  P. Lombroso,et al.  Identification of two alternatively spliced transcripts of STEP: a subfamily of brain-enriched protein tyrosine phosphatases. , 1995, Brain research. Molecular brain research.

[44]  D. Craufurd,et al.  Behavioral changes in Huntington Disease. , 2001, Neuropsychiatry, neuropsychology, and behavioral neurology.

[45]  T. H. Nguyen,et al.  Calcium‐Dependent Cleavage of Striatal Enriched Tyrosine Phosphatase (STEP) , 1999, Journal of neurochemistry.

[46]  C. B. Smith,et al.  Postadolescent Changes in Regional Cerebral Protein Synthesis: An In Vivo Study in the Fmr1 Null Mouse , 2005, The Journal of Neuroscience.

[47]  A L Reiss,et al.  Cognitive profiles associated with the fra(X) syndrome in males and females. , 1991, American journal of medical genetics.

[48]  M. Ticku,et al.  Chronic ethanol treatment upregulates the NMDA receptor function and binding in mammalian cortical neurons. , 1995, Brain research. Molecular brain research.

[49]  P. Bartolomeo,et al.  Retest effects and cognitive decline in longitudinal follow-up of patients with early HD , 2001, Neurology.

[50]  P. Greengard,et al.  Severe deficiencies in dopamine signaling in presymptomatic Huntington's disease mice. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[51]  Hilla Peretz,et al.  Ju n 20 03 Schrödinger ’ s Cat : The rules of engagement , 2003 .

[52]  Jeffrey L. Cummings,et al.  The spectrum of behavioral changes in Alzheimer's disease , 1996, Neurology.

[53]  P. Greengard,et al.  Regulation of NMDA receptor trafficking by amyloid-beta. , 2005, Nature neuroscience.

[54]  P. Carlen,et al.  Reduced Cortical Synaptic Plasticity and GluR1 Expression Associated with Fragile X Mental Retardation Protein Deficiency , 2002, Molecular and Cellular Neuroscience.

[55]  J. Krystal,et al.  First in vivo evidence of an NMDA receptor deficit in medication-free schizophrenic patients , 2006, Molecular Psychiatry.

[56]  J. Nevins,et al.  Huntingtin Is Present in the Nucleus, Interacts with the Transcriptional Corepressor C-terminal Binding Protein, and Represses Transcription* , 2002, The Journal of Biological Chemistry.

[57]  J. Hardy,et al.  Alzheimer's disease: the amyloid cascade hypothesis. , 1992, Science.

[58]  J. Hell,et al.  Striatal-enriched Protein-tyrosine Phosphatase (STEP) , 2012 .

[59]  R. Roth,et al.  The Neuropsychopharmacology of Phencyclidine: From NMDA Receptor Hypofunction to the Dopamine Hypothesis of Schizophrenia , 1999, Neuropsychopharmacology.

[60]  宁北芳,et al.  疟原虫var基因转换速率变化导致抗原变异[英]/Paul H, Robert P, Christodoulou Z, et al//Proc Natl Acad Sci U S A , 2005 .

[61]  P. Lombroso,et al.  Molecular characterization of a protein-tyrosine-phosphatase enriched in striatum. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[62]  Mark F. Bear,et al.  Altered synaptic plasticity in a mouse model of fragile X mental retardation , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[63]  M. Picciotto,et al.  Striatal‐enriched protein tyrosine phosphatase (STEP) knockout mice have enhanced hippocampal memory , 2011, The European journal of neuroscience.

[64]  H. Benveniste The excitotoxin hypothesis in relation to cerebral ischemia. , 1991, Cerebrovascular and brain metabolism reviews.

[65]  V. Hachinski,et al.  A NEW DEFINITION OF ALZHEIMER'S DISEASE: A HIPPOCAMPAL DEMENTIA , 1985, The Lancet.

[66]  J. Bibb,et al.  Extrasynaptic NMDA Receptors Couple Preferentially to Excitotoxicity via Calpain-Mediated Cleavage of STEP , 2009, The Journal of Neuroscience.

[67]  J. Naegele,et al.  STEP61: A Member of a Family of Brain-Enriched PTPs Is Localized to the Endoplasmic Reticulum , 1996, The Journal of Neuroscience.

[68]  Mark F. Bear,et al.  Internalization of ionotropic glutamate receptors in response to mGluR activation , 2001, Nature Neuroscience.

[69]  Jun Wang,et al.  Ethanol Induces Long-Term Facilitation of NR2B-NMDA Receptor Activity in the Dorsal Striatum: Implications for Alcohol Drinking Behavior , 2007, The Journal of Neuroscience.

[70]  B. Christie,et al.  NMDA receptor hypofunction in the dentate gyrus and impaired context discrimination in adult Fmr1 knockout mice , 2012, Hippocampus.

[71]  D. Lowenstein,et al.  Mild experimental brain injury in the rat induces cognitive deficits associated with regional neuronal loss in the hippocampus. , 1993, Journal of neurotrauma.

[72]  Paolo Calabresi,et al.  Dopamine-mediated regulation of corticostriatal synaptic plasticity , 2007, Trends in Neurosciences.

[73]  S. Warren,et al.  The fragile X mental retardation protein inhibits translation via interacting with mRNA. , 2001, Nucleic acids research.

[74]  Manish S. Shah,et al.  A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington's disease chromosomes , 1993, Cell.

[75]  S. Warren,et al.  Transcription, translation and fragile X syndrome. , 2006, Current opinion in genetics & development.

[76]  Bernardo L Sabatini,et al.  Natural Oligomers of the Alzheimer Amyloid-β Protein Induce Reversible Synapse Loss by Modulating an NMDA-Type Glutamate Receptor-Dependent Signaling Pathway , 2007, The Journal of Neuroscience.

[77]  L. Lue,et al.  Soluble amyloid beta peptide concentration as a predictor of synaptic change in Alzheimer's disease. , 1999, The American journal of pathology.

[78]  M. Kaste,et al.  Clinical determinants of poststroke dementia. , 1998, Stroke.

[79]  Joshua T Dudman,et al.  Mechanism of Positive Allosteric Modulators Acting on AMPA Receptors , 2005, The Journal of Neuroscience.

[80]  D. Ron Signaling Cascades Regulating NMDA Receptor Sensitivity to Ethanol , 2004, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[81]  S. Snyder,et al.  Dopamine receptor binding predicts clinical and pharmacological potencies of antischizophrenic drugs. , 1976, Science.

[82]  J. Mandel,et al.  Instability of a 550-base pair DNA segment and abnormal methylation in fragile X syndrome , 1991, Science.

[83]  J. C. Stoof,et al.  Opposing roles for D-1 and D-2 dopamine receptors in efflux of cyclic AMP from rat neostriatum , 1981, Nature.

[84]  K. Roche Regulation of NMDA receptor trafficking , 2010, Neuroscience Research.

[85]  Jun Wang,et al.  Author manuscript, published in "Journal of Neuroscience 2010;30(30):10187-98" DOI: 10.1523/JNEUROSCI.2268-10.2010 Long-Lasting Adaptations of the NR2B-containing NMDA Receptors in the Dorsomedial Striatum Play a Crucial Role in Alcohol Consumption and Re , 2012 .

[86]  D. Lovinger,et al.  Ethanol reverses the direction of long‐term synaptic plasticity in the dorsomedial striatum , 2007, The European journal of neuroscience.

[87]  A. Sidhu,et al.  Dopamine promotes striatal neuronal apoptotic death via ERK signaling cascades , 2009, The European journal of neuroscience.

[88]  G. Halliday,et al.  Patients with vascular dementia due to microvascular pathology have significant hippocampal neuronal loss , 2002, Journal of neurology, neurosurgery, and psychiatry.

[89]  A. Ostareck-Lederer,et al.  Evidence that fragile X mental retardation protein is a negative regulator of translation. , 2001, Human molecular genetics.

[90]  O. Hansson,et al.  Transgenic mice expressing a Huntington's disease mutation are resistant to quinolinic acid-induced striatal excitotoxicity. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[91]  Stephen T Warren,et al.  Fragile X mental retardation protein deficiency leads to excessive mGluR5-dependent internalization of AMPA receptors , 2007, Proceedings of the National Academy of Sciences.

[92]  Shaomin Li,et al.  Amyloid-β protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory , 2008, Nature Medicine.

[93]  R. Myers,et al.  Impaired synaptic plasticity in mice carrying the Huntington's disease mutation. , 1999, Human molecular genetics.

[94]  A. Malhotra,et al.  Schizophrenia is associated with elevated amphetamine-induced synaptic dopamine concentrations: evidence from a novel positron emission tomography method. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[95]  Tadashi Yamamoto,et al.  Tyrosine Dephosphorylation and Ethanol Inhibition of N-Methyl-d-aspartate Receptor Function* , 2003, The Journal of Biological Chemistry.

[96]  J. Kew,et al.  Allosteric modulators of NR2B‐containing NMDA receptors: molecular mechanisms and therapeutic potential , 2009, British journal of pharmacology.

[97]  Daniel C. Javitt,et al.  High dose D-serine in the treatment of schizophrenia , 2010, Schizophrenia Research.

[98]  P. Greengard,et al.  Genetic reduction of striatal-enriched tyrosine phosphatase (STEP) reverses cognitive and cellular deficits in an Alzheimer’s disease mouse model , 2010, Proceedings of the National Academy of Sciences.

[99]  Angus C. Nairn,et al.  The Dopamine/D1 Receptor Mediates the Phosphorylation and Inactivation of the Protein Tyrosine Phosphatase STEP via a PKA-Dependent Pathway , 2000, The Journal of Neuroscience.

[100]  L. Raymond,et al.  N-Methyl-d-aspartate (NMDA) receptor function and excitotoxicity in Huntington's disease , 2007, Progress in Neurobiology.

[101]  M. Hayden,et al.  Cognitive Dysfunction Precedes Neuropathology and Motor Abnormalities in the YAC128 Mouse Model of Huntington's Disease , 2005, The Journal of Neuroscience.

[102]  Marc G Caron,et al.  Mice with Reduced NMDA Receptor Expression Display Behaviors Related to Schizophrenia , 1999, Cell.

[103]  T. Kirino,et al.  Selective vulnerability in the gerbil hippocampus following transient ischemia , 2004, Acta Neuropathologica.

[104]  M. Solimena,et al.  STEP: a family of brain-enriched PTPs. Alternative splicing produces transmembrane, cytosolic and truncated isoforms. , 1997, European journal of cell biology.

[105]  Y. Uchiyama,et al.  Delayed neuronal death in the CA1 pyramidal cell layer of the gerbil hippocampus following transient ischemia is apoptosis , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[106]  C. Iadecola Bright and dark sides of nitric oxide in ischemic brain injury , 1997, Trends in Neurosciences.

[107]  E. Seeberg,et al.  Mutant Huntingtin Impairs Axonal Trafficking in Mammalian Neurons In Vivo and In Vitro , 2004, Molecular and Cellular Biology.

[108]  Philip D. Harvey,et al.  Cognitive deficits in schizophrenia. , 1993, The Psychiatric clinics of North America.

[109]  S. Nelson,et al.  Homeostatic plasticity in the developing nervous system , 2004, Nature Reviews Neuroscience.

[110]  David M. Bannerman,et al.  Effects of cytotoxic hippocampal lesions in mice on a cognitive test battery , 2002, Behavioural Brain Research.

[111]  M. Lerner,et al.  A protein tyrosine phosphatase expressed within dopaminoceptive neurons of the basal ganglia and related structures , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[112]  Katalin Illes,et al.  Mutant huntingtin alters MAPK signaling pathways in PC12 and striatal cells: ERK1/2 protects against mutant huntingtin-associated toxicity. , 2006, Human molecular genetics.

[113]  S. Wonnacott,et al.  Nicotinic acetylcholine receptors and the regulation of neuronal signalling. , 2004, Trends in pharmacological sciences.

[114]  T. Bliss,et al.  A synaptic model of memory: long-term potentiation in the hippocampus , 1993, Nature.

[115]  K. Nozaki,et al.  Mitogen-activated protein kinases and cerebral ischemia , 2001, Molecular Neurobiology.

[116]  E. Mandelkow,et al.  Clogging of axons by tau, inhibition of axonal traffic and starvation of synapses , 2003, Neurobiology of Aging.

[117]  W. K. Cullen,et al.  Naturally secreted oligomers of amyloid β protein potently inhibit hippocampal long-term potentiation in vivo , 2002, Nature.

[118]  G. Bernardi,et al.  Resistance to NMDA toxicity correlates with appearance of nuclear inclusions, behavioural deficits and changes in calcium homeostasis in mice transgenic for exon 1 of the huntington gene , 2001, The European journal of neuroscience.

[119]  S. Younkin,et al.  An increased percentage of long amyloid beta protein secreted by familial amyloid beta protein precursor (beta APP717) mutants. , 1994, Science.

[120]  Paul Greengard,et al.  Aβ-Mediated NMDA Receptor Endocytosis in Alzheimer's Disease Involves Ubiquitination of the Tyrosine Phosphatase STEP61 , 2010, The Journal of Neuroscience.

[121]  W. K. Cullen,et al.  β‐Amyloid produces a delayed NMDA receptor‐ dependent reduction in synaptic transmission in rat hippocampus , 1996, Neuroreport.

[122]  P. Wahle,et al.  Cellular and molecular characterization of a brain-enriched protein tyrosine phosphatase , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[123]  M. Bear,et al.  Chemical induction of mGluR5- and protein synthesis--dependent long-term depression in hippocampal area CA1. , 2001, Journal of neurophysiology.

[124]  Blair R. Leavitt,et al.  Loss of Huntingtin-Mediated BDNF Gene Transcription in Huntington's Disease , 2001, Science.

[125]  Mark F Bear,et al.  The mGluR theory of fragile X mental retardation , 2004, Trends in Neurosciences.

[126]  C. Bramham,et al.  BDNF function in adult synaptic plasticity: The synaptic consolidation hypothesis , 2005, Progress in Neurobiology.

[127]  P. Seeman,et al.  Brain receptors for antipsychotic drugs and dopamine: direct binding assays. , 1975, Proceedings of the National Academy of Sciences of the United States of America.

[128]  Brad E. Pfeiffer,et al.  Fragile X Mental Retardation Protein Induces Synapse Loss through Acute Postsynaptic Translational Regulation , 2007, The Journal of Neuroscience.

[129]  J. Ronesi,et al.  Metabotropic Glutamate Receptors and Fragile X Mental Retardation Protein: Partners in Translational Regulation at the Synapse , 2008, Science Signaling.

[130]  H. Wigström,et al.  Long‐term Depression in the Hippocampal CA1 Region is Associated with Equal Changes in AMPA and NMDA Receptor‐mediated Synaptic Potentials , 1994, The European journal of neuroscience.

[131]  L. Mucke,et al.  Fyn Kinase Induces Synaptic and Cognitive Impairments in a Transgenic Mouse Model of Alzheimer's Disease , 2005, The Journal of Neuroscience.

[132]  Angus C. Nairn,et al.  NMDA-mediated activation of the tyrosine phosphatase STEP regulates the duration of ERK signaling , 2003, Nature Neuroscience.

[133]  M. Bear,et al.  Chemical Induction of mGluR 5-and Protein Synthesis – Dependent Long-Term Depression in Hippocampal Area CA 1 , 2001 .

[134]  G. Collingridge,et al.  The Tyrosine Phosphatase STEP Mediates AMPA Receptor Endocytosis after Metabotropic Glutamate Receptor Stimulation , 2008, The Journal of Neuroscience.

[135]  K. M. Huber,et al.  Metabotropic receptor-dependent long-term depression persists in the absence of protein synthesis in the mouse model of fragile X syndrome. , 2006, Journal of neurophysiology.

[136]  R. Cappai,et al.  Amyloid beta. , 1999, The international journal of biochemistry & cell biology.

[137]  A. Chaudhuri,et al.  Neuroanatomical, molecular genetic, and behavioral correlates of fragile X syndrome , 2007, Brain Research Reviews.

[138]  P. Best,et al.  Ethanol, memory, and hippocampal function: A review of recent findings , 2000, Hippocampus.

[139]  S. Vannucci,et al.  Hypoxia‐Ischemia in Perinatal Rat Brain Induces the Formation of a Low Molecular Weight Isoform of Striatal Enriched Tyrosine Phosphatase (STEP) , 1999, Journal of neurochemistry.

[140]  J. J. Dougherty,et al.  β-Amyloid Regulation of Presynaptic Nicotinic Receptors in Rat Hippocampus and Neocortex , 2003, The Journal of Neuroscience.

[141]  S. Chattarji,et al.  Characterization and reversal of synaptic defects in the amygdala in a mouse model of fragile X syndrome , 2010, Proceedings of the National Academy of Sciences.

[142]  M. MacDonald,et al.  Specific progressive cAMP reduction implicates energy deficit in presymptomatic Huntington's disease knock-in mice. , 2003, Human molecular genetics.

[143]  M. Folstein,et al.  Cognitive impairment of Alzheimer disease. , 1983, Neurobehavioral toxicology and teratology.

[144]  J. Ule,et al.  RNA binding proteins and the regulation of neuronal synaptic plasticity , 2006, Current Opinion in Neurobiology.

[145]  Marian DiFiglia,et al.  Excitotoxic injury of the neostriatum: a model for Huntington's disease , 1990, Trends in Neurosciences.

[146]  Rand Askalan,et al.  Tyrosine Phosphatase STEP Is a Tonic Brake on Induction of Long-Term Potentiation , 2002, Neuron.

[147]  Stephen C Bowden,et al.  Neurocognitive impairment associated with alcohol use disorders: implications for treatment. , 2002, Experimental and clinical psychopharmacology.