Molecular signature of extracellular matrix pathology in schizophrenia
Growing evidence points to a critical involvement of the extracellular matrix (ECM) in the pathophysiology of schizophrenia (SZ). Decreases of perineuronal nets (PNNs) and altered expression of chondroitin sulphate proteoglycans (CSPGs) in glial cells have been identified in several brain regions. G...
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| Published in | The European journal of neuroscience Vol. 53; no. 12; pp. 3960 - 3987 |
|---|---|
| Main Authors | , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
France
Wiley Subscription Services, Inc
01.06.2021
John Wiley and Sons Inc |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Growing evidence points to a critical involvement of the extracellular matrix (ECM) in the pathophysiology of schizophrenia (SZ). Decreases of perineuronal nets (PNNs) and altered expression of chondroitin sulphate proteoglycans (CSPGs) in glial cells have been identified in several brain regions. GWAS data have identified several SZ vulnerability variants of genes encoding for ECM molecules. Given the potential relevance of ECM functions to the pathophysiology of this disorder, it is necessary to understand the extent of ECM changes across brain regions, their region‐ and sex‐specificity and which ECM components contribute to these changes. We tested the hypothesis that the expression of genes encoding for ECM molecules may be broadly disrupted in SZ across several cortical and subcortical brain regions and include key ECM components as well as factors such as ECM posttranslational modifications and regulator factors. Gene expression profiling of 14 neocortical brain regions, caudate, putamen and hippocampus from control subjects (n = 14/region) and subjects with SZ (n = 16/region) was conducted using Affymetrix microarray analysis. Analysis across brain regions revealed widespread dysregulation of ECM gene expression in cortical and subcortical brain regions in SZ, impacting several ECM functional key components. SRGN, CD44, ADAMTS1, ADAM10, BCAN, NCAN and SEMA4G showed some of the most robust changes. Region‐, sex‐ and age‐specific gene expression patterns and correlation with cognitive scores were also detected. Taken together, these findings contribute to emerging evidence for large‐scale ECM dysregulation in SZ and point to molecular pathways involved in PNN decreases, glial cell dysfunction and cognitive impairment in SZ.
Growing evidence points to a critical involvement of the extracellular matrix (ECM) in the pathophysiology of schizophrenia (SZ). We tested the hypothesis that the expression of genes encoding for ECM molecules may be broadly disrupted in SZ across several cortical and subcortical brain regions. Gene expression profiling of 14 neocortical brain regions, caudate, putamen and hippocampus from control subjects and donors with SZ was conducted using Affymetrix microarray analysis. Analysis across brain regions revealed widespread dysregulation of ECM gene expression in cortical and subcortical brain regions in SZ. In (a) proportion of ECM‐related differentially expressed genes (DEG) in SZ by the brain regions. The superior temporal cortex (BA22) showed the highest number of DEGs. In (b) ECM‐related DEGs in SZ compared to UC across all of the analysed regions (blue‐downregulated; red‐upregulated). DEG's t‐score (Y axis) values plotted against fold change (X axis). |
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| AbstractList | Growing evidence points to a critical involvement of the extracellular matrix (ECM) in the pathophysiology of schizophrenia (SZ). Decreases of perineuronal nets (PNNs) and altered expression of chondroitin sulphate proteoglycans (CSPGs) in glial cells have been identified in several brain regions. GWAS data have identified several SZ vulnerability variants of genes encoding for ECM molecules. Given the potential relevance of ECM functions to the pathophysiology of this disorder, it is necessary to understand the extent of ECM changes across brain regions, their region‐ and sex‐specificity and which ECM components contribute to these changes. We tested the hypothesis that the expression of genes encoding for ECM molecules may be broadly disrupted in SZ across several cortical and subcortical brain regions and include key ECM components as well as factors such as ECM posttranslational modifications and regulator factors. Gene expression profiling of 14 neocortical brain regions, caudate, putamen and hippocampus from control subjects (
n
= 14/region) and subjects with SZ (
n
= 16/region) was conducted using Affymetrix microarray analysis. Analysis across brain regions revealed widespread dysregulation of ECM gene expression in cortical and subcortical brain regions in SZ, impacting several ECM functional key components. SRGN, CD44, ADAMTS1, ADAM10, BCAN, NCAN and SEMA4G showed some of the most robust changes. Region‐, sex‐ and age‐specific gene expression patterns and correlation with cognitive scores were also detected. Taken together, these findings contribute to emerging evidence for large‐scale ECM dysregulation in SZ and point to molecular pathways involved in PNN decreases, glial cell dysfunction and cognitive impairment in SZ.
Growing evidence points to a critical involvement of the extracellular matrix (ECM) in the pathophysiology of schizophrenia (SZ). We tested the hypothesis that the expression of genes encoding for ECM molecules may be broadly disrupted in SZ across several cortical and subcortical brain regions. Gene expression profiling of 14 neocortical brain regions, caudate, putamen and hippocampus from control subjects and donors with SZ was conducted using Affymetrix microarray analysis. Analysis across brain regions revealed widespread dysregulation of ECM gene expression in cortical and subcortical brain regions in SZ. In (a) proportion of ECM‐related differentially expressed genes (DEG) in SZ by the brain regions. The superior temporal cortex (BA22) showed the highest number of DEGs. In (b) ECM‐related DEGs in SZ compared to UC across all of the analysed regions (blue‐downregulated; red‐upregulated). DEG's
t
‐score (
Y
axis) values plotted against fold change (
X
axis). Growing evidence points to a critical involvement of the extracellular matrix (ECM) in the pathophysiology of schizophrenia (SZ). Decreases of perineuronal nets (PNNs) and altered expression of chondroitin sulphate proteoglycans (CSPGs) in glial cells have been identified in several brain regions. GWAS data have identified several SZ vulnerability variants of genes encoding for ECM molecules. Given the potential relevance of ECM functions to the pathophysiology of this disorder, it is necessary to understand the extent of ECM changes across brain regions, their region‐ and sex‐specificity and which ECM components contribute to these changes. We tested the hypothesis that the expression of genes encoding for ECM molecules may be broadly disrupted in SZ across several cortical and subcortical brain regions and include key ECM components as well as factors such as ECM posttranslational modifications and regulator factors. Gene expression profiling of 14 neocortical brain regions, caudate, putamen and hippocampus from control subjects ( n = 14/region) and subjects with SZ ( n = 16/region) was conducted using Affymetrix microarray analysis. Analysis across brain regions revealed widespread dysregulation of ECM gene expression in cortical and subcortical brain regions in SZ, impacting several ECM functional key components. SRGN, CD44, ADAMTS1, ADAM10, BCAN, NCAN and SEMA4G showed some of the most robust changes. Region‐, sex‐ and age‐specific gene expression patterns and correlation with cognitive scores were also detected. Taken together, these findings contribute to emerging evidence for large‐scale ECM dysregulation in SZ and point to molecular pathways involved in PNN decreases, glial cell dysfunction and cognitive impairment in SZ. Growing evidence points to a critical involvement of the extracellular matrix (ECM) in the pathophysiology of schizophrenia (SZ). Decreases of perineuronal nets (PNNs) and altered expression of chondroitin sulphate proteoglycans (CSPGs) in glial cells have been identified in several brain regions. GWAS data have identified several SZ vulnerability variants of genes encoding for ECM molecules. Given the potential relevance of ECM functions to the pathophysiology of this disorder, it is necessary to understand the extent of ECM changes across brain regions, their region- and sex-specificity and which ECM components contribute to these changes. We tested the hypothesis that the expression of genes encoding for ECM molecules may be broadly disrupted in SZ across several cortical and subcortical brain regions and include key ECM components as well as factors such as ECM posttranslational modifications and regulator factors. Gene expression profiling of 14 neocortical brain regions, caudate, putamen and hippocampus from control subjects (n = 14/region) and subjects with SZ (n = 16/region) was conducted using Affymetrix microarray analysis. Analysis across brain regions revealed widespread dysregulation of ECM gene expression in cortical and subcortical brain regions in SZ, impacting several ECM functional key components. SRGN, CD44, ADAMTS1, ADAM10, BCAN, NCAN and SEMA4G showed some of the most robust changes. Region-, sex- and age-specific gene expression patterns and correlation with cognitive scores were also detected. Taken together, these findings contribute to emerging evidence for large-scale ECM dysregulation in SZ and point to molecular pathways involved in PNN decreases, glial cell dysfunction and cognitive impairment in SZ. Growing evidence points to a critical involvement of the extracellular matrix (ECM) in the pathophysiology of schizophrenia (SZ). Decreases of perineuronal nets (PNNs) and altered expression of chondroitin sulphate proteoglycans (CSPGs) in glial cells have been identified in several brain regions. GWAS data have identified several SZ vulnerability variants of genes encoding for ECM molecules. Given the potential relevance of ECM functions to the pathophysiology of this disorder, it is necessary to understand the extent of ECM changes across brain regions, their region‐ and sex‐specificity and which ECM components contribute to these changes. We tested the hypothesis that the expression of genes encoding for ECM molecules may be broadly disrupted in SZ across several cortical and subcortical brain regions and include key ECM components as well as factors such as ECM posttranslational modifications and regulator factors. Gene expression profiling of 14 neocortical brain regions, caudate, putamen and hippocampus from control subjects (n = 14/region) and subjects with SZ (n = 16/region) was conducted using Affymetrix microarray analysis. Analysis across brain regions revealed widespread dysregulation of ECM gene expression in cortical and subcortical brain regions in SZ, impacting several ECM functional key components. SRGN, CD44, ADAMTS1, ADAM10, BCAN, NCAN and SEMA4G showed some of the most robust changes. Region‐, sex‐ and age‐specific gene expression patterns and correlation with cognitive scores were also detected. Taken together, these findings contribute to emerging evidence for large‐scale ECM dysregulation in SZ and point to molecular pathways involved in PNN decreases, glial cell dysfunction and cognitive impairment in SZ. Growing evidence points to a critical involvement of the extracellular matrix (ECM) in the pathophysiology of schizophrenia (SZ). We tested the hypothesis that the expression of genes encoding for ECM molecules may be broadly disrupted in SZ across several cortical and subcortical brain regions. Gene expression profiling of 14 neocortical brain regions, caudate, putamen and hippocampus from control subjects and donors with SZ was conducted using Affymetrix microarray analysis. Analysis across brain regions revealed widespread dysregulation of ECM gene expression in cortical and subcortical brain regions in SZ. In (a) proportion of ECM‐related differentially expressed genes (DEG) in SZ by the brain regions. The superior temporal cortex (BA22) showed the highest number of DEGs. In (b) ECM‐related DEGs in SZ compared to UC across all of the analysed regions (blue‐downregulated; red‐upregulated). DEG's t‐score (Y axis) values plotted against fold change (X axis). Growing evidence points to a critical involvement of the extracellular matrix (ECM) in the pathophysiology of schizophrenia (SZ). Decreases of perineuronal nets (PNNs) and altered expression of chondroitin sulphate proteoglycans (CSPGs) in glial cells have been identified in several brain regions. GWAS data have identified several SZ vulnerability variants of genes encoding for ECM molecules. Given the potential relevance of ECM functions to the pathophysiology of this disorder, it is necessary to understand the extent of ECM changes across brain regions, their region- and sex-specificity and which ECM components contribute to these changes. We tested the hypothesis that the expression of genes encoding for ECM molecules may be broadly disrupted in SZ across several cortical and subcortical brain regions and include key ECM components as well as factors such as ECM posttranslational modifications and regulator factors. Gene expression profiling of 14 neocortical brain regions, caudate, putamen and hippocampus from control subjects (n = 14/region) and subjects with SZ (n = 16/region) was conducted using Affymetrix microarray analysis. Analysis across brain regions revealed widespread dysregulation of ECM gene expression in cortical and subcortical brain regions in SZ, impacting several ECM functional key components. SRGN, CD44, ADAMTS1, ADAM10, BCAN, NCAN and SEMA4G showed some of the most robust changes. Region-, sex- and age-specific gene expression patterns and correlation with cognitive scores were also detected. Taken together, these findings contribute to emerging evidence for large-scale ECM dysregulation in SZ and point to molecular pathways involved in PNN decreases, glial cell dysfunction and cognitive impairment in SZ.Growing evidence points to a critical involvement of the extracellular matrix (ECM) in the pathophysiology of schizophrenia (SZ). Decreases of perineuronal nets (PNNs) and altered expression of chondroitin sulphate proteoglycans (CSPGs) in glial cells have been identified in several brain regions. GWAS data have identified several SZ vulnerability variants of genes encoding for ECM molecules. Given the potential relevance of ECM functions to the pathophysiology of this disorder, it is necessary to understand the extent of ECM changes across brain regions, their region- and sex-specificity and which ECM components contribute to these changes. We tested the hypothesis that the expression of genes encoding for ECM molecules may be broadly disrupted in SZ across several cortical and subcortical brain regions and include key ECM components as well as factors such as ECM posttranslational modifications and regulator factors. Gene expression profiling of 14 neocortical brain regions, caudate, putamen and hippocampus from control subjects (n = 14/region) and subjects with SZ (n = 16/region) was conducted using Affymetrix microarray analysis. Analysis across brain regions revealed widespread dysregulation of ECM gene expression in cortical and subcortical brain regions in SZ, impacting several ECM functional key components. SRGN, CD44, ADAMTS1, ADAM10, BCAN, NCAN and SEMA4G showed some of the most robust changes. Region-, sex- and age-specific gene expression patterns and correlation with cognitive scores were also detected. Taken together, these findings contribute to emerging evidence for large-scale ECM dysregulation in SZ and point to molecular pathways involved in PNN decreases, glial cell dysfunction and cognitive impairment in SZ. Growing evidence points to a critical involvement of the extracellular matrix (ECM) in the pathophysiology of schizophrenia (SZ). Decreases of perineuronal nets (PNNs) and altered expression of chondroitin sulphate proteoglycans (CSPGs) in glial cells have been identified in several brain regions. GWAS data have identified several SZ vulnerability variants of genes encoding for ECM molecules. Given the potential relevance of ECM functions to the pathophysiology of this disorder, it is necessary to understand the extent of ECM changes across brain regions, their region‐ and sex‐specificity and which ECM components contribute to these changes. We tested the hypothesis that the expression of genes encoding for ECM molecules may be broadly disrupted in SZ across several cortical and subcortical brain regions and include key ECM components as well as factors such as ECM posttranslational modifications and regulator factors. Gene expression profiling of 14 neocortical brain regions, caudate, putamen and hippocampus from control subjects (n = 14/region) and subjects with SZ (n = 16/region) was conducted using Affymetrix microarray analysis. Analysis across brain regions revealed widespread dysregulation of ECM gene expression in cortical and subcortical brain regions in SZ, impacting several ECM functional key components. SRGN, CD44, ADAMTS1, ADAM10, BCAN, NCAN and SEMA4G showed some of the most robust changes. Region‐, sex‐ and age‐specific gene expression patterns and correlation with cognitive scores were also detected. Taken together, these findings contribute to emerging evidence for large‐scale ECM dysregulation in SZ and point to molecular pathways involved in PNN decreases, glial cell dysfunction and cognitive impairment in SZ. |
| Author | Chelini, Gabriele Pantazopoulos, Harry Berretta, Sabina Haroutunian, Vahram Klengel, Torsten Katsel, Pavel |
| AuthorAffiliation | 1 Department of Neurobiology and Anatomical Sciences University of Mississippi Medical Center Jackson MS USA 4 Mental Illness Research Education Clinical Centers of Excellence (MIRECC) JJ Peters VA Medical Center Bronx NY USA 6 Department of Psychiatry Harvard Medical School Boston MA USA 9 Program in Neuroscience Harvard Medical School Boston MA USA 2 Department of Psychiatry The Icahn School of Medicine at Mount Sinai New York NY USA 5 Translational Neuroscience Laboratory Mclean Hospital Belmont MA USA 8 Department of Psychiatry University Medical Center Göttingen Göttingen Germany 7 Translational Molecular Genomics Laboratory Mclean Hospital Belmont MA USA 3 Department of Neuroscience The Icahn School of Medicine at Mount Sinai New York NY USA |
| AuthorAffiliation_xml | – name: 2 Department of Psychiatry The Icahn School of Medicine at Mount Sinai New York NY USA – name: 7 Translational Molecular Genomics Laboratory Mclean Hospital Belmont MA USA – name: 9 Program in Neuroscience Harvard Medical School Boston MA USA – name: 1 Department of Neurobiology and Anatomical Sciences University of Mississippi Medical Center Jackson MS USA – name: 6 Department of Psychiatry Harvard Medical School Boston MA USA – name: 5 Translational Neuroscience Laboratory Mclean Hospital Belmont MA USA – name: 4 Mental Illness Research Education Clinical Centers of Excellence (MIRECC) JJ Peters VA Medical Center Bronx NY USA – name: 8 Department of Psychiatry University Medical Center Göttingen Göttingen Germany – name: 3 Department of Neuroscience The Icahn School of Medicine at Mount Sinai New York NY USA |
| Author_xml | – sequence: 1 givenname: Harry surname: Pantazopoulos fullname: Pantazopoulos, Harry organization: University of Mississippi Medical Center – sequence: 2 givenname: Pavel surname: Katsel fullname: Katsel, Pavel organization: JJ Peters VA Medical Center – sequence: 3 givenname: Vahram surname: Haroutunian fullname: Haroutunian, Vahram organization: JJ Peters VA Medical Center – sequence: 4 givenname: Gabriele surname: Chelini fullname: Chelini, Gabriele organization: Harvard Medical School – sequence: 5 givenname: Torsten surname: Klengel fullname: Klengel, Torsten organization: University Medical Center Göttingen – sequence: 6 givenname: Sabina orcidid: 0000-0002-4057-7766 surname: Berretta fullname: Berretta, Sabina email: s.berretta@mclean.harvard.edu organization: Harvard Medical School |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/33070392$$D View this record in MEDLINE/PubMed |
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| Keywords | glial cells microarray neurodevelopment schizophrenia synaptic plasticity extracellular matrix interneurons perineuronal nets |
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| Snippet | Growing evidence points to a critical involvement of the extracellular matrix (ECM) in the pathophysiology of schizophrenia (SZ). Decreases of perineuronal... |
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| SubjectTerms | ADAMTS-1 protein Brain Brain - metabolism CD44 antigen Chondroitin Sulfate Proteoglycans - genetics Chondroitin Sulfate Proteoglycans - metabolism Cognitive ability DNA microarrays Extracellular matrix Extracellular Matrix - metabolism Gene expression Glial cells Humans interneurons Mental disorders microarray neurodevelopment Neuroglia - metabolism Pathophysiology Perineuronal nets Proteoglycans Putamen Schizophrenia Schizophrenia - genetics Special Issue synaptic plasticity |
| Title | Molecular signature of extracellular matrix pathology in schizophrenia |
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