Distinctive transcriptome alterations of prefrontal pyramidal neurons in schizophrenia and schizoaffective disorder

Arion, D; Corradi, J P; Tang, S; Datta, D; Boothe, F; He, A; Cacace, A M; Zaczek, R; Albright, C F; Tseng, G; Lewis, D A

doi:10.1038/mp.2014.171

Cited by 178Schizophrenia research and treatmentNeurotransmitter Receptor Influence on BehaviorMental Health and Psychiatry

Distinctive transcriptome alterations of prefrontal pyramidal neurons in schizophrenia and schizoaffective disorder

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Arion, D, Corradi, J P, Tang, S, Datta, D, Boothe, F, He, A, Cacace, A M, Zaczek, R +3 more·2015·Molecular Psychiatry

DOI 10.1038/mp.2014.171PMC PMC4492919

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Abstract

Schizophrenia is associated with alterations in working memory that reflect dysfunction of dorsolateral prefrontal cortex (DLPFC) circuitry. Working memory depends on the activity of excitatory pyramidal cells in DLPFC layer 3 and, to a lesser extent, in layer 5. Although many studies have profiled gene expression in DLPFC gray matter in schizophrenia, little is known about cell-type-specific transcript expression in these two populations of pyramidal cells. We hypothesized that interrogating gene expression, specifically in DLPFC layer 3 or 5 pyramidal cells, would reveal new and/or more robust schizophrenia-associated differences that would provide new insights into the nature of pyramidal cell dysfunction in the illness. We also sought to determine the impact of other variables, such as a diagnosis of schizoaffective disorder or medication use at the time of death, on the patterns of gene expression in pyramidal neurons. Individual pyramidal cells in DLPFC layers 3 or 5 were captured by laser microdissection from 36 subjects with schizophrenia or schizoaffective disorder and matched normal comparison subjects. The mRNA from cell collections was subjected to transcriptome profiling by microarray followed by quantitative PCR validation. Expression of genes involved in mitochondrial (MT) or ubiquitin-proteasome system (UPS) functions were markedly downregulated in the patient group (P-values for MT-related and UPS-related pathways were <10(-7) and <10(-5), respectively). MT-related gene alterations were more prominent in layer 3 pyramidal cells, whereas UPS-related gene alterations were more prominent in layer 5 pyramidal cells. Many of these alterations were not present, or found to a lesser degree, in samples of DLPFC gray matter from the same subjects, suggesting that they are pyramidal cell specific. Furthermore, these findings principally reflected alterations in the schizophrenia subjects were not present or present to a lesser degree in the schizoaffective disorder subjects (diagnosis of schizoaffective disorder was the most significant covariate, P<10(-6)) and were not attributable to factors frequently comorbid with schizophrenia. In summary, our findings reveal expression deficits in MT- and UPS-related genes specific to layer 3 and/or layer 5 pyramidal cells in the DLPFC of schizophrenia subjects. These cell type-specific transcriptome signatures are not characteristic of schizoaffective disorder, providing a potential molecular-cellular basis of differences in clinical phenotypes.

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Dorsolateral prefrontal cortex layer 3 pyramidal cells appear to receive fewer excitatory synaptic inputs, resulting in lower expression of gene products critical for energy production.
“Because DLPFC layer 3 PCs appear to receive fewer excitatory synaptic inputs (Glantz and Lewis, 2000) resulting in a lower expression of gene products critical for energy production (Arion et al, 2015)”
From Reduced Labeling of Parvalbumin Neurons and Perineuronal Nets in the Dorsolateral Prefrontal Cortex of Subjects with Schizophrenia (2016) · cites this paper as Arion et al, 2015

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mGluR2 versus mGluR3 Metabotropic Glutamate Receptors in Primate Dorsolateral Prefrontal Cortex: Postsynaptic mGluR3 Strengthen Working Memory Networks
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Transcriptome-wide mega-analyses reveal joint dysregulation of immunologic genes and transcription regulators in brain and blood in schizophrenia
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Cognitive Dysfunction and Prefrontal Cortical Circuit Alterations in Schizophrenia: Developmental Trajectories
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Inference of cell type content from human brain transcriptomic datasets illuminates the effects of age, manner of death, dissection, and psychiatric diagnosis
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Parvalbumin interneuron deficits in schizophrenia
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Glutamate transporter splice variant expression in an enriched pyramidal cell population in schizophrenia
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Altered Gradients of Glutamate and Gamma-Aminobutyric Acid Transcripts in the Cortical Visuospatial Working Memory Network in Schizophrenia
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Altered Markers of Cortical γ-Aminobutyric Acid Neuronal Activity in Schizophrenia
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Targeting Prefrontal Cortical Systems for Drug Development: Potential Therapies for Cognitive Disorders
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Inhibition of STEP61 ameliorates deficits in mouse and hiPSC-based schizophrenia models
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Unusual Molecular Regulation of Dorsolateral Prefrontal Cortex Layer III Synapses Increases Vulnerability to Genetic and Environmental Insults in Schizophrenia
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Unique Molecular Regulation of Higher-Order Prefrontal Cortical Circuits: Insights into the Neurobiology of Schizophrenia
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Integration of Enhancer-Promoter Interactions with GWAS Summary Results Identifies Novel Schizophrenia-Associated Genes and Pathways
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Mitochondrial Proteostasis Requires Genes Encoded in a Neurodevelopmental Syndrome Locus
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Mapping Phosphodiesterase 4D (PDE4D) in Macaque Dorsolateral Prefrontal Cortex: Postsynaptic Compartmentalization in Layer III Pyramidal Cell Circuits
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Overexpression of neuregulin 1 in GABAergic interneurons results in reversible cortical disinhibition
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Transcriptome Alterations in Prefrontal Pyramidal Cells Distinguish Schizophrenia From Bipolar and Major Depressive Disorders
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Transcriptome alterations of prefrontal cortical parvalbumin neurons in schizophrenia
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PYRAMIDAL CELLS: ROLE IN PRIMATE PREFRONTAL CORTEX CIRCUITRY DURING POSTNATAL DEVELOPMENT AND SCHIZOPHRENIA
Datta, D. (2016) · D-Scholarship@Pitt (University of Pittsburgh)
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Transcriptional Profile of Pyramidal Neurons in Chronic Schizophrenia Reveals Lamina-Specific Dysfunction of Neuronal Immunity
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Authors: Arion, D., Corradi, J. P., Tang, S., Datta, D., Boothe, F., He, A., Cacace, A. M., Zaczek, R., Albright, C. F., Tseng, G., & Lewis, D. A.
Affiliations: University of Pittsburgh (US)
Bristol-Myers Squibb (United States) (US)
Corresponding author: Lewis, D A
ORCID: Corradi, J P
Cacace, A M
Tseng, G
Lewis, D A
Venue: Molecular Psychiatry
Publisher: Springer Science and Business Media LLC
Published: 2015-01-06
Volume: 20
Issue: 11
Pages: 1397-1405
ISSN: 1359-4184 (ISSN-L)
1476-5578
DOI: 10.1038/mp.2014.171
PMC: PMC4492919
OpenAlex: W1989747504
Cited by: 177
References: 63
Citations by year: 2026: 14 · 2025: 8 · 2024: 15 · 2023: 11 · 2022: 15 · 2021: 16 · 2020: 20 · 2019: 16 · 2018: 22 · 2017: 15 · 2016: 12 · 2015: 13
FWCI: 16.76
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: Molecular Psychiatry (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: Bristol-Myers Squibb
National Institutes of Health
National Institute of Mental Health (P50MH084053, MH084053, R01MH043784, P50MH103204, MH-103204, R37MH043784, MH043784)
Topics: Health Sciences › Medicine › Psychiatry and Mental health › Schizophrenia research and treatment
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Social Sciences › Arts and Humanities › Philosophy › Mental Health and Psychiatry
Keywords: schizophrenia, schizoaffective disorder, dorsolateral prefrontal cortex, pyramidal neurons, layer 5 pyramidal cells, cell type-specific gene expression, working memory, mitochondrial dysfunction, ubiquitin-proteasome system, postmortem brain, gene expression profiling, antipsychotic effects
MeSH terms: Adult, Analysis of Variance, Animals, Female, Gene Expression Regulation, Humans, Macaca fascicularis, Male, Middle Aged, Psychotic Disorders, RNA, Messenger, Schizophrenia, Antipsychotic Agents, Signal Transduction, Prefrontal Cortex, Pyramidal Cells, Oligonucleotide Array Sequence Analysis, Gene Expression Profiling, Mitochondrial Proteins, Ubiquitin, Transcriptome, Laser Capture Microdissection

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Distinctive transcriptome alterations of prefrontal pyramidal neurons in schizophrenia and schizoaffective disorder

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