Blood–brain barrier and intestinal epithelial barrier alterations in autism spectrum disorders
Autism spectrum disorders (ASD) are complex conditions whose pathogenesis may be attributed to gene-environment interactions. There are no definitive mechanisms explaining how environmental triggers can lead to ASD although the involvement of inflammation and immunity has been suggested. Inappropria...
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| Published in | Molecular autism Vol. 7; no. 1; p. 49 |
|---|---|
| Main Authors | , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
England
BioMed Central Ltd
29.11.2016
BioMed Central |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Autism spectrum disorders (ASD) are complex conditions whose pathogenesis may be attributed to gene-environment interactions. There are no definitive mechanisms explaining how environmental triggers can lead to ASD although the involvement of inflammation and immunity has been suggested. Inappropriate antigen trafficking through an impaired intestinal barrier, followed by passage of these antigens or immune-activated complexes through a permissive blood-brain barrier (BBB), can be part of the chain of events leading to these disorders. Our goal was to investigate whether an altered BBB and gut permeability is part of the pathophysiology of ASD.
cerebral cortex and cerebellum tissues from ASD, schizophrenia (SCZ), and healthy subjects (HC) and duodenal biopsies from ASD and HC were analyzed for gene and protein expression profiles. Tight junctions and other key molecules associated with the neurovascular unit integrity and function and neuroinflammation were investigated.
Claudin (
)-5 and -12 were increased in the ASD cortex and cerebellum.
,
, and
were higher in the ASD cortex.
,
, and
were downregulated in SCZ cortex;
was increased in the SCZ cerebellum. Differences between SCZ and ASD were observed for most of the genes analyzed in both brain areas. CLDN-5 protein was increased in ASD cortex and cerebellum, while CLDN-12 appeared reduced in both ASD and SCZ cortexes. In the intestine, 75% of the ASD samples analyzed had reduced expression of barrier-forming TJ components (
,
,
), whereas 66% had increased pore-forming CLDNs (
,
,
) compared to controls.
In the ASD brain, there is an altered expression of genes associated with BBB integrity coupled with increased neuroinflammation and possibly impaired gut barrier integrity. While these findings seem to be specific for ASD, the possibility of more distinct SCZ subgroups should be explored with additional studies. |
|---|---|
| AbstractList | Autism spectrum disorders (ASD) are complex conditions whose pathogenesis may be attributed to gene-environment interactions. There are no definitive mechanisms explaining how environmental triggers can lead to ASD although the involvement of inflammation and immunity has been suggested. Inappropriate antigen trafficking through an impaired intestinal barrier, followed by passage of these antigens or immune-activated complexes through a permissive blood-brain barrier (BBB), can be part of the chain of events leading to these disorders. Our goal was to investigate whether an altered BBB and gut permeability is part of the pathophysiology of ASD. Postmortem cerebral cortex and cerebellum tissues from ASD, schizophrenia (SCZ), and healthy subjects (HC) and duodenal biopsies from ASD and HC were analyzed for gene and protein expression profiles. Tight junctions and other key molecules associated with the neurovascular unit integrity and function and neuroinflammation were investigated. Claudin (CLDN)-5 and -12 were increased in the ASD cortex and cerebellum. CLDN-3, tricellulin, and MMP-9 were higher in the ASD cortex. IL-8, tPA, and IBA-1 were downregulated in SCZ cortex; IL-1b was increased in the SCZ cerebellum. Differences between SCZ and ASD were observed for most of the genes analyzed in both brain areas. CLDN-5 protein was increased in ASD cortex and cerebellum, while CLDN-12 appeared reduced in both ASD and SCZ cortexes. In the intestine, 75% of the ASD samples analyzed had reduced expression of barrier-forming TJ components (CLDN-1, OCLN, TRIC), whereas 66% had increased pore-forming CLDNs (CLDN-2, -10, -15) compared to controls. In the ASD brain, there is an altered expression of genes associated with BBB integrity coupled with increased neuroinflammation and possibly impaired gut barrier integrity. While these findings seem to be specific for ASD, the possibility of more distinct SCZ subgroups should be explored with additional studies. Background Autism spectrum disorders (ASD) are complex conditions whose pathogenesis may be attributed to gene-environment interactions. There are no definitive mechanisms explaining how environmental triggers can lead to ASD although the involvement of inflammation and immunity has been suggested. Inappropriate antigen trafficking through an impaired intestinal barrier, followed by passage of these antigens or immune-activated complexes through a permissive blood-brain barrier (BBB), can be part of the chain of events leading to these disorders. Our goal was to investigate whether an altered BBB and gut permeability is part of the pathophysiology of ASD. Methods Postmortem cerebral cortex and cerebellum tissues from ASD, schizophrenia (SCZ), and healthy subjects (HC) and duodenal biopsies from ASD and HC were analyzed for gene and protein expression profiles. Tight junctions and other key molecules associated with the neurovascular unit integrity and function and neuroinflammation were investigated. Results Claudin (CLDN)-5 and -12 were increased in the ASD cortex and cerebellum. CLDN-3, tricellulin, and MMP-9 were higher in the ASD cortex. IL-8, tPA, and IBA-1 were downregulated in SCZ cortex; IL-1b was increased in the SCZ cerebellum. Differences between SCZ and ASD were observed for most of the genes analyzed in both brain areas. CLDN-5 protein was increased in ASD cortex and cerebellum, while CLDN-12 appeared reduced in both ASD and SCZ cortexes. In the intestine, 75% of the ASD samples analyzed had reduced expression of barrier-forming TJ components (CLDN-1, OCLN, TRIC), whereas 66% had increased pore-forming CLDNs (CLDN-2, -10, -15) compared to controls. Conclusions In the ASD brain, there is an altered expression of genes associated with BBB integrity coupled with increased neuroinflammation and possibly impaired gut barrier integrity. While these findings seem to be specific for ASD, the possibility of more distinct SCZ subgroups should be explored with additional studies. Keywords: Blood-brain barrier, Autism spectrum disorders, Gut-brain axis, Gut permeability, Schizophrenia, Neuroinflammation, Postmortem brain, Duodenal biopsies Autism spectrum disorders (ASD) are complex conditions whose pathogenesis may be attributed to gene-environment interactions. There are no definitive mechanisms explaining how environmental triggers can lead to ASD although the involvement of inflammation and immunity has been suggested. Inappropriate antigen trafficking through an impaired intestinal barrier, followed by passage of these antigens or immune-activated complexes through a permissive blood-brain barrier (BBB), can be part of the chain of events leading to these disorders. Our goal was to investigate whether an altered BBB and gut permeability is part of the pathophysiology of ASD. cerebral cortex and cerebellum tissues from ASD, schizophrenia (SCZ), and healthy subjects (HC) and duodenal biopsies from ASD and HC were analyzed for gene and protein expression profiles. Tight junctions and other key molecules associated with the neurovascular unit integrity and function and neuroinflammation were investigated. Claudin ( )-5 and -12 were increased in the ASD cortex and cerebellum. , , and were higher in the ASD cortex. , , and were downregulated in SCZ cortex; was increased in the SCZ cerebellum. Differences between SCZ and ASD were observed for most of the genes analyzed in both brain areas. CLDN-5 protein was increased in ASD cortex and cerebellum, while CLDN-12 appeared reduced in both ASD and SCZ cortexes. In the intestine, 75% of the ASD samples analyzed had reduced expression of barrier-forming TJ components ( , , ), whereas 66% had increased pore-forming CLDNs ( , , ) compared to controls. In the ASD brain, there is an altered expression of genes associated with BBB integrity coupled with increased neuroinflammation and possibly impaired gut barrier integrity. While these findings seem to be specific for ASD, the possibility of more distinct SCZ subgroups should be explored with additional studies. Background Autism spectrum disorders (ASD) are complex conditions whose pathogenesis may be attributed to gene-environment interactions. There are no definitive mechanisms explaining how environmental triggers can lead to ASD although the involvement of inflammation and immunity has been suggested. Inappropriate antigen trafficking through an impaired intestinal barrier, followed by passage of these antigens or immune-activated complexes through a permissive blood-brain barrier (BBB), can be part of the chain of events leading to these disorders. Our goal was to investigate whether an altered BBB and gut permeability is part of the pathophysiology of ASD. Methods Postmortem cerebral cortex and cerebellum tissues from ASD, schizophrenia (SCZ), and healthy subjects (HC) and duodenal biopsies from ASD and HC were analyzed for gene and protein expression profiles. Tight junctions and other key molecules associated with the neurovascular unit integrity and function and neuroinflammation were investigated. Results Claudin (CLDN)-5 and -12 were increased in the ASD cortex and cerebellum. CLDN-3, tricellulin, and MMP-9 were higher in the ASD cortex. IL-8, tPA, and IBA-1 were downregulated in SCZ cortex; IL-1b was increased in the SCZ cerebellum. Differences between SCZ and ASD were observed for most of the genes analyzed in both brain areas. CLDN-5 protein was increased in ASD cortex and cerebellum, while CLDN-12 appeared reduced in both ASD and SCZ cortexes. In the intestine, 75% of the ASD samples analyzed had reduced expression of barrier-forming TJ components (CLDN-1, OCLN, TRIC), whereas 66% had increased pore-forming CLDNs (CLDN-2, -10, -15) compared to controls. Conclusions In the ASD brain, there is an altered expression of genes associated with BBB integrity coupled with increased neuroinflammation and possibly impaired gut barrier integrity. While these findings seem to be specific for ASD, the possibility of more distinct SCZ subgroups should be explored with additional studies. |
| ArticleNumber | 49 |
| Audience | Academic |
| Author | Sapone, Anna Kadzielski, Sarah M. Senger, Stefania Kelly, Deanna L. Buie, Timothy M. Fiorentino, Maria Camhi, Stephanie S. Fasano, Alessio Cascella, Nicola |
| Author_xml | – sequence: 1 givenname: Maria orcidid: 0000-0001-5318-7313 surname: Fiorentino fullname: Fiorentino, Maria – sequence: 2 givenname: Anna surname: Sapone fullname: Sapone, Anna – sequence: 3 givenname: Stefania surname: Senger fullname: Senger, Stefania – sequence: 4 givenname: Stephanie S. surname: Camhi fullname: Camhi, Stephanie S. – sequence: 5 givenname: Sarah M. surname: Kadzielski fullname: Kadzielski, Sarah M. – sequence: 6 givenname: Timothy M. surname: Buie fullname: Buie, Timothy M. – sequence: 7 givenname: Deanna L. surname: Kelly fullname: Kelly, Deanna L. – sequence: 8 givenname: Nicola surname: Cascella fullname: Cascella, Nicola – sequence: 9 givenname: Alessio surname: Fasano fullname: Fasano, Alessio |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/27957319$$D View this record in MEDLINE/PubMed |
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| Snippet | Autism spectrum disorders (ASD) are complex conditions whose pathogenesis may be attributed to gene-environment interactions. There are no definitive... Background Autism spectrum disorders (ASD) are complex conditions whose pathogenesis may be attributed to gene-environment interactions. There are no... |
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| SubjectTerms | Adolescent Adult Analysis Antigens Autism Autism Spectrum Disorder - genetics Autism Spectrum Disorder - immunology Autism Spectrum Disorder - metabolism Autism Spectrum Disorder - pathology Biopsy Blood-brain barrier Blood-Brain Barrier - immunology Blood-Brain Barrier - metabolism Blood-Brain Barrier - pathology Care and treatment Case-Control Studies Cerebellum - immunology Cerebellum - metabolism Cerebellum - pathology Cerebral Cortex - immunology Cerebral Cortex - metabolism Cerebral Cortex - pathology Child Child, Preschool Claudin-3 - genetics Claudin-3 - immunology Claudin-5 - genetics Claudin-5 - immunology Claudins - genetics Claudins - immunology DNA-Binding Proteins - genetics DNA-Binding Proteins - immunology Duodenum - immunology Duodenum - metabolism Duodenum - pathology Female Gene Expression Health aspects Humans Inflammation Interleukin-1beta - genetics Interleukin-1beta - immunology Interleukin-8 - genetics Interleukin-8 - immunology Male MARVEL Domain Containing 2 Protein - genetics MARVEL Domain Containing 2 Protein - immunology Matrix Metalloproteinase 9 - genetics Matrix Metalloproteinase 9 - immunology Middle Aged Permeability Pervasive developmental disorders Risk factors Schizophrenia - genetics Schizophrenia - immunology Schizophrenia - metabolism Schizophrenia - pathology Tight Junctions - immunology Tight Junctions - metabolism Tight Junctions - pathology |
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| Title | Blood–brain barrier and intestinal epithelial barrier alterations in autism spectrum disorders |
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