The impact of sex on gene expression in the brain of schizophrenic patients: a systematic review and meta-analysis of transcriptomic studies.

Schizophrenia / genetics Humans Sex Characteristics Brain / metabolism Transcriptome Female Male Prefrontal Cortex / metabolism
Hippocampus Meta-analysis Prefrontal cortex RNA-sequencing Schizophrenia Sex-based differences Systematic review

Journal

Biology of sex differences
ISSN: 2042-6410
Titre abrégé: Biol Sex Differ
Pays: England
ID NLM: 101548963

Informations de publication

Date de publication:
27 Jul 2024
Historique:
received: 30 06 2023
accepted: 08 07 2024
medline: 28 7 2024
pubmed: 28 7 2024
entrez: 27 7 2024
Statut: epublish

Résumé

Schizophrenia is a severe neuropsychiatric disorder characterized by altered perception, mood, and behavior that profoundly impacts patients and society despite its relatively low prevalence. Sex-based differences have been described in schizophrenia epidemiology, symptomatology and outcomes. Different studies explored the impact of schizophrenia in the brain transcriptome, however we lack a consensus transcriptomic profile that considers sex and differentiates specific cerebral regions. We performed a systematic review on bulk RNA-sequencing studies of post-mortem brain samples. Then, we fulfilled differential expression analysis on each study and summarized their results with regions-specific meta-analyses (prefrontal cortex and hippocampus) and a global all-studies meta-analysis. Finally, we used the consensus transcriptomic profiles to functionally characterize the impact of schizophrenia in males and females by protein-protein interaction networks, enriched biological processes and dysregulated transcription factors. We discovered the sex-based dysregulation of 265 genes in the prefrontal cortex, 1.414 genes in the hippocampus and 66 genes in the all-studies meta-analyses. The functional characterization of these gene sets unveiled increased processes related to immune response functions in the prefrontal cortex in male and the hippocampus in female schizophrenia patients and the overexpression of genes related to neurotransmission and synapses in the prefrontal cortex of female schizophrenia patients. Considering a meta-analysis of all brain regions available, we encountered the relative overexpression of genes related to synaptic plasticity and transmission in females and the overexpression of genes involved in organizing genetic information and protein folding in male schizophrenia patients. The protein-protein interaction networks and transcription factors activity analyses supported these sex-based profiles. Our results report multiple sex-based transcriptomic alterations in specific brain regions of schizophrenia patients, which provides new insight into the role of sex in schizophrenia. Moreover, we unveil a partial overlapping of inflammatory processes in the prefrontal cortex of males and the hippocampus of females. Schizophrenia is a serious illness characterised by changes in perception, mood and behaviour that profoundly affect patients and society. The frequency, symptoms and progression of schizophrenia are different in women and men, but the biological reason for this is not understood. The identification of disease mechanisms specific in men and women, is relevant because it would allow a better understanding of this pathology, as well as improving the personalisation of diagnoses and treatments for patients. To achieve this goal, in this work we reviewed all available RNA sequencing studies of post-mortem brain samples from women and men affected by schizophrenia. Then, we compared gene expression in each study by sex, and integrated all study results in different brain regions: prefrontal cortex, hippocampus and all-studies. We discovered significant changes between men and women: 265 genes differentially expressed in the prefrontal cortex, 1414 genes in the hippocampus and 66 genes in meta-analyses of all-studies. The study of these genes revealed increased immune response functions in the prefrontal cortex of men and in the hippocampus of women with schizophrenia, as well as increased neurotransmission and synapses in the prefrontal cortex of women with schizophrenia. Our results report multiple gene expression changes in specific brain regions of patients with schizophrenia, providing new insights into the role of sex in schizophrenia.

Sections du résumé

BACKGROUND BACKGROUND
Schizophrenia is a severe neuropsychiatric disorder characterized by altered perception, mood, and behavior that profoundly impacts patients and society despite its relatively low prevalence. Sex-based differences have been described in schizophrenia epidemiology, symptomatology and outcomes. Different studies explored the impact of schizophrenia in the brain transcriptome, however we lack a consensus transcriptomic profile that considers sex and differentiates specific cerebral regions.
METHODS METHODS
We performed a systematic review on bulk RNA-sequencing studies of post-mortem brain samples. Then, we fulfilled differential expression analysis on each study and summarized their results with regions-specific meta-analyses (prefrontal cortex and hippocampus) and a global all-studies meta-analysis. Finally, we used the consensus transcriptomic profiles to functionally characterize the impact of schizophrenia in males and females by protein-protein interaction networks, enriched biological processes and dysregulated transcription factors.
RESULTS RESULTS
We discovered the sex-based dysregulation of 265 genes in the prefrontal cortex, 1.414 genes in the hippocampus and 66 genes in the all-studies meta-analyses. The functional characterization of these gene sets unveiled increased processes related to immune response functions in the prefrontal cortex in male and the hippocampus in female schizophrenia patients and the overexpression of genes related to neurotransmission and synapses in the prefrontal cortex of female schizophrenia patients. Considering a meta-analysis of all brain regions available, we encountered the relative overexpression of genes related to synaptic plasticity and transmission in females and the overexpression of genes involved in organizing genetic information and protein folding in male schizophrenia patients. The protein-protein interaction networks and transcription factors activity analyses supported these sex-based profiles.
CONCLUSIONS CONCLUSIONS
Our results report multiple sex-based transcriptomic alterations in specific brain regions of schizophrenia patients, which provides new insight into the role of sex in schizophrenia. Moreover, we unveil a partial overlapping of inflammatory processes in the prefrontal cortex of males and the hippocampus of females.
Schizophrenia is a serious illness characterised by changes in perception, mood and behaviour that profoundly affect patients and society. The frequency, symptoms and progression of schizophrenia are different in women and men, but the biological reason for this is not understood. The identification of disease mechanisms specific in men and women, is relevant because it would allow a better understanding of this pathology, as well as improving the personalisation of diagnoses and treatments for patients. To achieve this goal, in this work we reviewed all available RNA sequencing studies of post-mortem brain samples from women and men affected by schizophrenia. Then, we compared gene expression in each study by sex, and integrated all study results in different brain regions: prefrontal cortex, hippocampus and all-studies. We discovered significant changes between men and women: 265 genes differentially expressed in the prefrontal cortex, 1414 genes in the hippocampus and 66 genes in meta-analyses of all-studies. The study of these genes revealed increased immune response functions in the prefrontal cortex of men and in the hippocampus of women with schizophrenia, as well as increased neurotransmission and synapses in the prefrontal cortex of women with schizophrenia. Our results report multiple gene expression changes in specific brain regions of patients with schizophrenia, providing new insights into the role of sex in schizophrenia.

Autres résumés

Type: plain-language-summary (eng)
Schizophrenia is a serious illness characterised by changes in perception, mood and behaviour that profoundly affect patients and society. The frequency, symptoms and progression of schizophrenia are different in women and men, but the biological reason for this is not understood. The identification of disease mechanisms specific in men and women, is relevant because it would allow a better understanding of this pathology, as well as improving the personalisation of diagnoses and treatments for patients. To achieve this goal, in this work we reviewed all available RNA sequencing studies of post-mortem brain samples from women and men affected by schizophrenia. Then, we compared gene expression in each study by sex, and integrated all study results in different brain regions: prefrontal cortex, hippocampus and all-studies. We discovered significant changes between men and women: 265 genes differentially expressed in the prefrontal cortex, 1414 genes in the hippocampus and 66 genes in meta-analyses of all-studies. The study of these genes revealed increased immune response functions in the prefrontal cortex of men and in the hippocampus of women with schizophrenia, as well as increased neurotransmission and synapses in the prefrontal cortex of women with schizophrenia. Our results report multiple gene expression changes in specific brain regions of patients with schizophrenia, providing new insights into the role of sex in schizophrenia.

Identifiants

DOI: 10.1186/s13293-024-00635-x PMID: 39068467
pubmed: 39068467
doi: 10.1186/s13293-024-00635-x
pii: 10.1186/s13293-024-00635-x
doi:

Types de publication

Journal Article Systematic Review Meta-Analysis

Langues

eng

Sous-ensembles de citation

IM

Pagination

59

Subventions

Organisme : Ministerio de Ciencia e Innovación
ID : PID2021- 124430OA-I00
Organisme : Ministerio de Ciencia e Innovación
ID : MS21-074
Organisme : Instituto de Salud Carlos III
ID : IMP/00019

Informations de copyright

© 2024. The Author(s).

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Auteurs

Hector Carceller (H)

Neurobiology Unit, Program in Neurosciences and Institute of Biotechnology and Biomedicine (BIOTECMED), Universitat de València, Burjassot, Spain.
Spanish National Network for Research in Mental Health, Centro de Investigación Biomédica en Red de Salud Mental (CIBERSAM), Madrid, Spain.
Joint unit in Biomedical Imaging FISABIO-CIPF, Head of Computational Biomedicine Laboratory, Foundation for the Promotion of Health and Biomedical Research of Valencia Region, Eduardo Primo Yúfera Street, 3, 46012, València, Spain.

Marta R Hidalgo (MR)

Joint unit in Biomedical Imaging FISABIO-CIPF, Head of Computational Biomedicine Laboratory, Foundation for the Promotion of Health and Biomedical Research of Valencia Region, Eduardo Primo Yúfera Street, 3, 46012, València, Spain.
Computational Biomedicine Laboratory, Principe Felipe Research Centre (CIPF), Eduardo Primo Yúfera Street, 3, Valencia, 46012, Spain.

María José Escartí (MJ)

Centro de Investigación Biomédica en Red de Salud Mental (CIBERSAM), ISC III, Avda. Blasco Ibáñez 15, Valencia, Spain.

Juan Nacher (J)

Neurobiology Unit, Program in Neurosciences and Institute of Biotechnology and Biomedicine (BIOTECMED), Universitat de València, Burjassot, Spain.
Spanish National Network for Research in Mental Health, Centro de Investigación Biomédica en Red de Salud Mental (CIBERSAM), Madrid, Spain.
Fundación Investigación Hospital Clínico de Valencia, INCLIVA, Valencia, Spain.

Maria de la Iglesia-Vayá (M)

Spanish National Network for Research in Mental Health, Centro de Investigación Biomédica en Red de Salud Mental (CIBERSAM), Madrid, Spain.
Joint unit in Biomedical Imaging FISABIO-CIPF, Head of Computational Biomedicine Laboratory, Foundation for the Promotion of Health and Biomedical Research of Valencia Region, Eduardo Primo Yúfera Street, 3, 46012, València, Spain.

Francisco García-García (F)

Joint unit in Biomedical Imaging FISABIO-CIPF, Head of Computational Biomedicine Laboratory, Foundation for the Promotion of Health and Biomedical Research of Valencia Region, Eduardo Primo Yúfera Street, 3, 46012, València, Spain. fgarcia@cipf.es.
Computational Biomedicine Laboratory, Principe Felipe Research Centre (CIPF), Eduardo Primo Yúfera Street, 3, Valencia, 46012, Spain. fgarcia@cipf.es.
ORCID: 0000-0001-8354-5636

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Classifications MeSH

questionsmedicales.fr › Troubles mentaux › Schizophrénie et troubles avec traits psychotiques › Schizophrénie › The impact of sex on gene expression in the...
questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Primates › Haplorhini › Catarrhini › Hominidae › Humains › The impact of sex on gene expression in the...
questionsmedicales.fr › Phénomènes physiologiques des appareils urinaire et reproducteur › Phénomènes physiologiques de la reproduction › Caractères sexuels › The impact of sex on gene expression in the...
questionsmedicales.fr › Système nerveux › Système nerveux central › Encéphale › The impact of sex on gene expression in the...
questionsmedicales.fr › Phénomènes génétiques › Structures génétiques › Transcriptome › The impact of sex on gene expression in the...
questionsmedicales.fr › Système nerveux › Système nerveux central › Encéphale › Prosencéphale › Télencéphale › Cerveau › Cortex cérébral › Lobe frontal › Cortex préfrontal › The impact of sex on gene expression in the...