Behavioral and neurochemical phenotyping of Homer1 mutant mice: possible relevance to schizophrenia

Szumlinski, K. K.; Lominac, K. D.; Kleschen, M. J.; Oleson, E. B.; Dehoff, M. H.; Schwartz, M. K.; Seeberg, P. H.; Worley, P. F.; Kalivas, P. W.

doi:10.1111/j.1601-183x.2005.00120.x

Cited by 189Schizophrenia research and treatmentNeurotransmitter Receptor Influence on BehaviorNeuroscience and Neuropharmacology Research

Behavioral and neurochemical phenotyping of Homer1 mutant mice: possible relevance to schizophrenia

Szumlinski, K. K., Lominac, K. D., Kleschen, M. J., Oleson, E. B., Dehoff, M. H., Schwartz, M. K., Seeberg, P. H., Worley, P. F. +1 more·2005·Genes, Brain and Behavior

DOI 10.1111/j.1601-183x.2005.00120.x

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Abstract

Homer proteins are involved in the functional assembly of postsynaptic density proteins at glutamatergic synapses and are implicated in learning, memory and drug addiction. Here, we report that Homer1-knockout (Homer1-KO) mice exhibit behavioral and neurochemical abnormalities that are consistent with the animal models of schizophrenia. Relative to wild-type mice, Homer1-KO mice exhibited deficits in radial arm maze performance, impaired prepulse inhibition, enhanced 'behavioral despair', increased anxiety in a novel objects test, enhanced reactivity to novel environments, decreased instrumental responding for sucrose and enhanced MK-801- and methamphetamine-stimulated motor behavior. No-net-flux in vivo microdialysis revealed a decrease in extracellular glutamate content in the nucleus accumbens and an increase in the prefrontal cortex. Moreover, in Homer1-KO mice, cocaine did not stimulate a rise in frontal cortex extracellular glutamate levels, suggesting hypofrontality. These behavioral and neurochemical data derived from Homer1 mutant mice are consistent with the recent association of schizophrenia with a single-nucleotide polymorphism in the Homer1 gene and suggest that the regulation of extracellular levels of glutamate within limbo-corticostriatal structures by Homer1 gene products may be involved in the pathogenesis of this neuropsychiatric disorder.

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Mouse models have shown that a number of proteins associated with glutamate receptors, some of which are directly linked with schizophrenia susceptibility genes, have been suggested to show modifications in patients, which in turn cause schizophrenia-like phenotypes.
“Interestingly, mouse models have shown that a number of proteins associated with glutamate receptors, some of which are directly linked with schizophrenia susceptibility genes, have been suggested to show modifications in patients, which in turn cause schizophrenia-like phenotypes.86,87”
From Glutamate in Schizophrenia: A Focused Review and Meta-Analysis of 1H-MRS Studies (2013) · cites this paper as [86]

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Functional Consequences of Mutations in Postsynaptic Scaffolding Proteins and Relevance to Psychiatric Disorders
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Differential Effects of Chronic Ethanol Consumption and Withdrawal on Homer/Glutamate Receptor Expression in Subregions of the Accumbens and Amygdala of P Rats
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Mice Lacking Homer 1 Exhibit a Skeletal Myopathy Characterized by Abnormal Transient Receptor Potential Channel Activity
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A Review of Biomarkers in Mood and Psychotic Disorders: A Dissection of Clinical vs. Preclinical Correlates
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Scaffolding Proteins of the Post-synaptic Density Contribute to Synaptic Plasticity by Regulating Receptor Localization and Distribution: Relevance for Neuropsychiatric Diseases
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Homer Isoforms Differentially Regulate Cocaine-Induced Neuroplasticity
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Evidence of Missense Mutations on the Neuregulin 1 Gene Affecting Function of Prepulse Inhibition
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Dynamic remodeling of scaffold interactions in dendritic spines controls synaptic excitability
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Complex, multimodal behavioral profile of the Homer1 knockout mouse
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Different effects of the NMDA receptor antagonists ketamine, MK-801, and memantine on postsynaptic density transcripts and their topography: role of Homer signaling, and implications for novel antipsychotic and pro-cognitive targets in psychosis
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Tonic Premarin dose-dependently enhances memory, affects neurotrophin protein levels and alters gene expression in middle-aged rats
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Treating the Synapse in Major Psychiatric Disorders: The Role of Postsynaptic Density Network in Dopamine-Glutamate Interplay and Psychopharmacologic Drugs Molecular Actions
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Fibroblast growth factor receptor signaling affects development and function of dopamine neurons – inhibition results in a schizophrenia‐like syndrome in transgenic mice
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Homer1/mGluR5 Activity Moderates Vulnerability to Chronic Social Stress
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Homer1 promotes dendritic spine growth through ankyrin-G and its loss reshapes the synaptic proteome
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A Homer 1 gene variant influences brain structure and function, lithium effects on white matter, and antidepressant response in bipolar disorder: a multimodal genetic imaging study
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Regional differences in the effects of withdrawal from repeated cocaine upon Homer and glutamate receptor expression: A two-species comparison
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Homer1 Mediates Acute Stress-Induced Cognitive Deficits in the Dorsal Hippocampus
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Genetic variability in scaffolding proteins and risk for schizophrenia and autism-spectrum disorders: a systematic review
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Requirement of the immediate early gene vesl-1S/homer-1a for fear memory formation
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Homer-1 polymorphisms are associated with psychopathology and response to treatment in schizophrenic patients
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Calcium-Dependent Networks in Dopamine–Glutamate Interaction: The Role of Postsynaptic Scaffolding Proteins
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The Importance of Cognitive Phenotypes in Experimental Modeling of Animal Anxiety and Depression
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Type 1 Equilibrative Nucleoside Transporter Regulates Ethanol Drinking Through Accumbal N-Methyl-D-Aspartate Receptor Signaling
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Contribution of early environmental stress to alcoholism vulnerability
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The Glutamatergic Aspects of Schizophrenia Molecular Pathophysiology: Role of the Postsynaptic Density, and Implications for Treatment
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Behavioral Tasks Evaluating Schizophrenia-like Symptoms in Animal Models: A Recent Update
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A Bi-Directional Competitive Interaction between CircHomer1 and Homer1b within the Orbitofrontal Cortex Regulates Reversal Learning
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Developmental roles for Homer: more than just a pretty scaffold
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Selective Disruption of Metabotropic Glutamate Receptor 5-Homer Interactions Mimics Phenotypes of Fragile X Syndrome in Mice
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Behavioral genetic contributions to the study of addiction-related amphetamine effects
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The Ampakine CX546 Restores the Prepulse Inhibition and Latent Inhibition Deficits in mGluR5-Deficient Mice
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Immediate-Early Genes Modulation by Antipsychotics: Translational Implications for a Putative Gateway to Drug-Induced Long-Term Brain Changes
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Cognitive Impairment in Schizophrenia: a Review of Developmental and Genetic Models, and Pro-cognitive Profile of the Optimised D3 > D2 Antagonist, S33138
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Imbalances in Prefrontal Cortex CC-Homer1 versus CC-Homer2 Expression Promote Cocaine Preference
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A Mutation in Hnrnph1 That Decreases Methamphetamine-Induced Reinforcement, Reward, and Dopamine Release and Increases Synaptosomal hnRNP H and Mitochondrial Proteins
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Pattern of acute induction of Homer1a gene is preserved after chronic treatment with first- and second-generation antipsychotics: effect of short-term drug discontinuation and comparison with Homer1a-interacting genes
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Biomarkers for Psychiatric Disorders
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Genomic analyses reveal distinct genetic architectures and selective pressures in buffaloes
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Rescue of synaptic plasticity and spatial learning deficits in the hippocampus of Homer1 knockout mice by recombinant Adeno-associated viral gene delivery of Homer1c
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Signaling pathways regulating Homer1a expression: implications for antidepressant therapy
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Strain Differences in the Gating-Disruptive Effects of Apomorphine: Relationship to Gene Expression in Nucleus Accumbens Signaling Pathways
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Differential expression of Homer 1 gene by acute and chronic administration of antipsychotics and dopamine transporter inhibitors in the rat forebrain
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Structural and Functional Modifications in Glutamateric Synapses Following Prolonged Ethanol Exposure
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The Homer1 family of proteins at the crossroad of dopamine-glutamate signaling: An emerging molecular “Lego” in the pathophysiology of psychiatric disorders. A systematic review and translational insight
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The dopamine D1 receptor agonist, but not the D2 receptor agonist, induces gene expression of Homer 1a in rat striatum and nucleus accumbens
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Anxiety‐related behavioral inhibition in rats: a model to examine mechanisms underlying the risk to develop stress‐related psychopathology
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Synaptic structural protein dysfunction leads to altered excitation inhibition ratios in models of autism spectrum disorder
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Phenotypes, mechanisms and therapeutics: insights from bipolar disorder GWAS findings
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DID it or DIDn't it? Exploration of a failure to replicate binge-like alcohol-drinking in C57BL/6J mice
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Homer 1a and mGluR5 phosphorylation in reward-sensitive metaplasticity: A hypothesis of neuronal selection and bidirectional synaptic plasticity
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Homer1a protein expression in schizophrenia, bipolar disorder, and major depression
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Candidate genes for panic disorder: insight from human and mouse genetic studies
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Targeting Homer genes using adeno-associated viral vector: lessons learned from behavioural and neurochemical studies
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Progressive recruitment of cortical and striatal regions by inducible postsynaptic density transcripts after increasing doses of antipsychotics with different receptor profiles: Insights for psychosis treatment
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Hybridizing behavioral models: A possible solution to some problems in neurophenotyping research?
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The intracellular domain of the human protocadherin hFat1 interacts with Homer signalling scaffolding proteins
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Protein expression of targets of the FMRP regulon is altered in brains of subjects with schizophrenia and mood disorders
Folsom, T. D., THURAS, P. D., & Fatemi, S. H. (2015) · Schizophrenia Research · doi:10.1016/j.schres.2015.04.012 · Cited by 29 · see citing works

Distinct Roles for Different Homer1 Isoforms in Behaviors and Associated Prefrontal Cortex Function
Lominac, K. D., Oleson, E. B., Pava, M. J., Klugmann, M., Schwarz, M. K., Seeburg, P. H., During, M. J., Worley, P. F., Kalivas, P. W., & Szumlinski, K. K. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.3764-05.2005 · Cited by 118 · see citing works
Self-citation
Homer 1a Gene Expression Modulation by Antipsychotic Drugs: Involvement of the
(2002)
Homer proteins: implications for neuropsychiatric disorders
Szumlinski, K. K., Kalivas, P. W., & Worley, P. F. (2006) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2006.05.002 · Cited by 174 · see citing works
Self-citation
Mice lacking the AMPA GluR1 receptor exhibit striatal hypodopaminergia and 'schizophrenia−related' behaviors
Wiedholz, L. M., Owens, W. A., Horton, R., Feyder, M., Karlsson, R.-M., Hefner, K., Sprengel, R., Celikel, T., Daws, L. C., & Holmes, A. (2007) · Max Planck Institute for Plasma Physics
Mice lacking the AMPA GluR1 receptor exhibit striatal hyperdopaminergia and ‘schizophrenia-related’ behaviors
Wiedholz, L. M., Owens, W. A., Horton, R. E., Feyder, M. J., Karlsson, R.-M., Hefner, K. R., Sprengel, R., Celikel, T., Daws, L. C., & Holmes, A. (2007) · Molecular Psychiatry · doi:10.1038/sj.mp.4002056 · Cited by 180 · see citing works

Authors: Szumlinski, K. K., Lominac, K. D., Kleschen, M. J., Oleson, E. B., Dehoff, M. H., Schwartz, M. K., Seeberg, P. H., Worley, P. F., & Kalivas, P. W.
Affiliations: Medical University of South Carolina (US)
Johns Hopkins University (US)
Max Planck Institute for Medical Research (DE)
Corresponding author: Szumlinski, K. K.
ORCID: Szumlinski, K. K.
Lominac, K. D.
Oleson, E. B.
Worley, P. F.
Kalivas, P. W.
Venue: Genes, Brain and Behavior
Publisher: Wiley
Published: 2005-02-08
Volume: 4
Issue: 5
Pages: 273-288
ISSN: 1601-183X (ISSN-L)
1601-1848
DOI: 10.1111/j.1601-183x.2005.00120.x
OpenAlex: W2069755036
Cited by: 181
References: 57
Citations by year: 2025: 5 · 2024: 8 · 2023: 5 · 2022: 4 · 2021: 3 · 2020: 8 · 2019: 4 · 2018: 6 · 2017: 10 · 2016: 6 · 2015: 9 · 2014: 8 · 2013: 16 · 2012: 9
FWCI: 8.02
Type: journal article
Language: en
Open access: closed
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations: Genes Brain & Behavior (publishedVersion)
PubMed (publishedVersion)
Max Planck Institute for Plasma Physics (submittedVersion)
Max Planck Digital Library (submittedVersion)
MPG.PuRe (Max Planck Society) (submittedVersion)
Funders: National Institute of Mental Health (R01MH040817, MH-40817)
National Institute on Drug Abuse (DA14185, DA 11742, R21DA014185, R01DA011742)
Topics: Health Sciences › Medicine › Psychiatry and Mental health › Schizophrenia research and treatment
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords: Homer1, schizophrenia, postsynaptic density, glutamatergic synapses, prepulse inhibition, anxiety, behavioral despair, sucrose preference, glutamate, nucleus accumbens, prefrontal cortex, hypofrontality, single nucleotide polymorphisms, animal models of schizophrenia
MeSH terms: Homer Scaffolding Proteins, Animals, Behavior, Animal, Carrier Proteins, Conditioning, Operant, Exploratory Behavior, Female, Frontal Lobe, Humans, Male, Mice, Inbred C57BL, Neural Inhibition, Nucleus Accumbens, Phenotype, Schizophrenia, Gene Deletion, Mice, Knockout, Glutamic Acid, Maze Learning, Polymorphism, Single Nucleotide, Mice

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Behavioral and neurochemical phenotyping of Homer1 mutant mice: possible relevance to schizophrenia

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