Network Effects of the 15q13.3 Microdeletion on the Transcriptome and Epigenome in Human-Induced Neurons
The 15q13.3 microdeletion is associated with several neuropsychiatric disorders, including autism and schizophrenia. Previous association and functional studies have investigated the potential role of several genes within the deletion in neuronal dysfunction, but the molecular effects of the deletio...
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| Published in | Biological psychiatry (1969) Vol. 89; no. 5; pp. 497 - 509 |
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| Main Authors | , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
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United States
Elsevier Inc
01.03.2021
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| Online Access | Get full text |
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| Abstract | The 15q13.3 microdeletion is associated with several neuropsychiatric disorders, including autism and schizophrenia. Previous association and functional studies have investigated the potential role of several genes within the deletion in neuronal dysfunction, but the molecular effects of the deletion as a whole remain largely unknown.
Induced pluripotent stem cells, from 3 patients with the 15q13.3 microdeletion and 3 control subjects, were generated and converted into induced neurons. We analyzed the effects of the 15q13.3 microdeletion on genome-wide gene expression, DNA methylation, chromatin accessibility, and sensitivity to cisplatin-induced DNA damage. Furthermore, we measured gene expression changes in induced neurons with CRISPR (clustered regularly interspaced short palindromic repeats) knockouts of individual 15q13.3 microdeletion genes.
In both induced pluripotent stem cells and induced neurons, gene copy number change within the 15q13.3 microdeletion was accompanied by significantly decreased gene expression and no compensatory changes in DNA methylation or chromatin accessibility, supporting the model that haploinsufficiency of genes within the deleted region drives the disorder. Furthermore, we observed global effects of the microdeletion on the transcriptome and epigenome, with disruptions in several neuropsychiatric disorder–associated pathways and gene families, including Wnt signaling, ribosome function, DNA binding, and clustered protocadherins. Individual gene knockouts mirrored many of the observed changes in an overlapping fashion between knockouts.
Our multiomics analysis of the 15q13.3 microdeletion revealed downstream effects in pathways previously associated with neuropsychiatric disorders and indications of interactions between genes within the deletion. This molecular systems analysis can be applied to other chromosomal aberrations to further our etiological understanding of neuropsychiatric disorders. |
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| AbstractList | The 15q13.3 microdeletion is associated with several neuropsychiatric disorders, including autism and schizophrenia. Previous association and functional studies have investigated the potential role of several genes within the deletion in neuronal dysfunction, but the molecular effects of the deletion as a whole remain largely unknown.
Induced pluripotent stem cells, from 3 patients with the 15q13.3 microdeletion and 3 control subjects, were generated and converted into induced neurons. We analyzed the effects of the 15q13.3 microdeletion on genome-wide gene expression, DNA methylation, chromatin accessibility, and sensitivity to cisplatin-induced DNA damage. Furthermore, we measured gene expression changes in induced neurons with CRISPR (clustered regularly interspaced short palindromic repeats) knockouts of individual 15q13.3 microdeletion genes.
In both induced pluripotent stem cells and induced neurons, gene copy number change within the 15q13.3 microdeletion was accompanied by significantly decreased gene expression and no compensatory changes in DNA methylation or chromatin accessibility, supporting the model that haploinsufficiency of genes within the deleted region drives the disorder. Furthermore, we observed global effects of the microdeletion on the transcriptome and epigenome, with disruptions in several neuropsychiatric disorder–associated pathways and gene families, including Wnt signaling, ribosome function, DNA binding, and clustered protocadherins. Individual gene knockouts mirrored many of the observed changes in an overlapping fashion between knockouts.
Our multiomics analysis of the 15q13.3 microdeletion revealed downstream effects in pathways previously associated with neuropsychiatric disorders and indications of interactions between genes within the deletion. This molecular systems analysis can be applied to other chromosomal aberrations to further our etiological understanding of neuropsychiatric disorders. The 15q13.3 microdeletion is associated with several neuropsychiatric disorders, including autism and schizophrenia. Previous association and functional studies have investigated the potential role of several genes within the deletion in neuronal dysfunction, but the molecular effects of the deletion as a whole remain largely unknown.BACKGROUNDThe 15q13.3 microdeletion is associated with several neuropsychiatric disorders, including autism and schizophrenia. Previous association and functional studies have investigated the potential role of several genes within the deletion in neuronal dysfunction, but the molecular effects of the deletion as a whole remain largely unknown.Induced pluripotent stem cells, from 3 patients with the 15q13.3 microdeletion and 3 control subjects, were generated and converted into induced neurons. We analyzed the effects of the 15q13.3 microdeletion on genome-wide gene expression, DNA methylation, chromatin accessibility, and sensitivity to cisplatin-induced DNA damage. Furthermore, we measured gene expression changes in induced neurons with CRISPR (clustered regularly interspaced short palindromic repeats) knockouts of individual 15q13.3 microdeletion genes.METHODSInduced pluripotent stem cells, from 3 patients with the 15q13.3 microdeletion and 3 control subjects, were generated and converted into induced neurons. We analyzed the effects of the 15q13.3 microdeletion on genome-wide gene expression, DNA methylation, chromatin accessibility, and sensitivity to cisplatin-induced DNA damage. Furthermore, we measured gene expression changes in induced neurons with CRISPR (clustered regularly interspaced short palindromic repeats) knockouts of individual 15q13.3 microdeletion genes.In both induced pluripotent stem cells and induced neurons, gene copy number change within the 15q13.3 microdeletion was accompanied by significantly decreased gene expression and no compensatory changes in DNA methylation or chromatin accessibility, supporting the model that haploinsufficiency of genes within the deleted region drives the disorder. Furthermore, we observed global effects of the microdeletion on the transcriptome and epigenome, with disruptions in several neuropsychiatric disorder-associated pathways and gene families, including Wnt signaling, ribosome function, DNA binding, and clustered protocadherins. Individual gene knockouts mirrored many of the observed changes in an overlapping fashion between knockouts.RESULTSIn both induced pluripotent stem cells and induced neurons, gene copy number change within the 15q13.3 microdeletion was accompanied by significantly decreased gene expression and no compensatory changes in DNA methylation or chromatin accessibility, supporting the model that haploinsufficiency of genes within the deleted region drives the disorder. Furthermore, we observed global effects of the microdeletion on the transcriptome and epigenome, with disruptions in several neuropsychiatric disorder-associated pathways and gene families, including Wnt signaling, ribosome function, DNA binding, and clustered protocadherins. Individual gene knockouts mirrored many of the observed changes in an overlapping fashion between knockouts.Our multiomics analysis of the 15q13.3 microdeletion revealed downstream effects in pathways previously associated with neuropsychiatric disorders and indications of interactions between genes within the deletion. This molecular systems analysis can be applied to other chromosomal aberrations to further our etiological understanding of neuropsychiatric disorders.CONCLUSIONSOur multiomics analysis of the 15q13.3 microdeletion revealed downstream effects in pathways previously associated with neuropsychiatric disorders and indications of interactions between genes within the deletion. This molecular systems analysis can be applied to other chromosomal aberrations to further our etiological understanding of neuropsychiatric disorders. AbstractBackgroundThe 15q13.3 microdeletion is associated with several neuropsychiatric disorders, including autism and schizophrenia. Previous association and functional studies have investigated the potential role of several genes within the deletion in neuronal dysfunction, but the molecular effects of the deletion as a whole remain largely unknown. MethodsInduced pluripotent stem cells, from 3 patients with the 15q13.3 microdeletion and 3 control subjects, were generated and converted into induced neurons. We analyzed the effects of the 15q13.3 microdeletion on genome-wide gene expression, DNA methylation, chromatin accessibility, and sensitivity to cisplatin-induced DNA damage. Furthermore, we measured gene expression changes in induced neurons with CRISPR (clustered regularly interspaced short palindromic repeats) knockouts of individual 15q13.3 microdeletion genes. ResultsIn both induced pluripotent stem cells and induced neurons, gene copy number change within the 15q13.3 microdeletion was accompanied by significantly decreased gene expression and no compensatory changes in DNA methylation or chromatin accessibility, supporting the model that haploinsufficiency of genes within the deleted region drives the disorder. Furthermore, we observed global effects of the microdeletion on the transcriptome and epigenome, with disruptions in several neuropsychiatric disorder–associated pathways and gene families, including Wnt signaling, ribosome function, DNA binding, and clustered protocadherins. Individual gene knockouts mirrored many of the observed changes in an overlapping fashion between knockouts. ConclusionsOur multiomics analysis of the 15q13.3 microdeletion revealed downstream effects in pathways previously associated with neuropsychiatric disorders and indications of interactions between genes within the deletion. This molecular systems analysis can be applied to other chromosomal aberrations to further our etiological understanding of neuropsychiatric disorders. |
| Author | Urban, Alexander E. Hallmayer, Joachim Wong, Wing Hung Zhang, Xianglong Davis, Kasey N. Bernstein, Jonathan A. Zhang, Siming Purmann, Carolin Shrestha, Anima Huang, Yiling Pattni, Reenal Ma, Shining Ho, Marcus |
| AuthorAffiliation | 4 School of Medicine, Stanford University, and Department of Statistics, School of Humanities and Sciences, Stanford University, Stanford, California 6 Department of Genetics, School of Humanities and Science, Stanford University, Stanford, California; Department of Psychiatry and Behavioral Sciences, School of Humanities and Science, Stanford University, Stanford, California 5 Department of Human Biology, School of Humanities and Science, Stanford University, Stanford, California 2 Department of Psychiatry and Behavioral Sciences, School of Humanities and Science, Stanford University, Stanford, California 1 Department of Genetics, School of Humanities and Science, Stanford University, Stanford, California 3 Department of Pediatrics, School of Humanities and Sciences, Stanford University, Stanford, California |
| AuthorAffiliation_xml | – name: 1 Department of Genetics, School of Humanities and Science, Stanford University, Stanford, California – name: 2 Department of Psychiatry and Behavioral Sciences, School of Humanities and Science, Stanford University, Stanford, California – name: 5 Department of Human Biology, School of Humanities and Science, Stanford University, Stanford, California – name: 6 Department of Genetics, School of Humanities and Science, Stanford University, Stanford, California; Department of Psychiatry and Behavioral Sciences, School of Humanities and Science, Stanford University, Stanford, California – name: 4 School of Medicine, Stanford University, and Department of Statistics, School of Humanities and Sciences, Stanford University, Stanford, California – name: 3 Department of Pediatrics, School of Humanities and Sciences, Stanford University, Stanford, California |
| Author_xml | – sequence: 1 givenname: Siming orcidid: 0000-0003-3008-8392 surname: Zhang fullname: Zhang, Siming organization: Department of Genetics, School of Humanities and Science, Stanford University, Stanford, California – sequence: 2 givenname: Xianglong surname: Zhang fullname: Zhang, Xianglong organization: Department of Psychiatry and Behavioral Sciences, School of Humanities and Science, Stanford University, Stanford, California – sequence: 3 givenname: Carolin surname: Purmann fullname: Purmann, Carolin organization: Department of Psychiatry and Behavioral Sciences, School of Humanities and Science, Stanford University, Stanford, California – sequence: 4 givenname: Shining surname: Ma fullname: Ma, Shining organization: and Department of Pediatrics, School of Humanities and Sciences, Stanford University, Stanford, California – sequence: 5 givenname: Anima surname: Shrestha fullname: Shrestha, Anima organization: School of Medicine, Stanford University, and Department of Statistics, School of Humanities and Sciences, Stanford University, Stanford, California – sequence: 6 givenname: Kasey N. orcidid: 0000-0003-1717-7040 surname: Davis fullname: Davis, Kasey N. organization: Department of Psychiatry and Behavioral Sciences, School of Humanities and Science, Stanford University, Stanford, California – sequence: 7 givenname: Marcus surname: Ho fullname: Ho, Marcus organization: Department of Psychiatry and Behavioral Sciences, School of Humanities and Science, Stanford University, Stanford, California – sequence: 8 givenname: Yiling surname: Huang fullname: Huang, Yiling organization: Department of Psychiatry and Behavioral Sciences, School of Humanities and Science, Stanford University, Stanford, California – sequence: 9 givenname: Reenal surname: Pattni fullname: Pattni, Reenal organization: Department of Psychiatry and Behavioral Sciences, School of Humanities and Science, Stanford University, Stanford, California – sequence: 10 givenname: Wing Hung surname: Wong fullname: Wong, Wing Hung organization: and Department of Pediatrics, School of Humanities and Sciences, Stanford University, Stanford, California – sequence: 11 givenname: Jonathan A. orcidid: 0000-0001-5369-346X surname: Bernstein fullname: Bernstein, Jonathan A. organization: and Department of Human Biology, School of Humanities and Science, Stanford University, Stanford, California – sequence: 12 givenname: Joachim surname: Hallmayer fullname: Hallmayer, Joachim organization: Department of Psychiatry and Behavioral Sciences, School of Humanities and Science, Stanford University, Stanford, California – sequence: 13 givenname: Alexander E. surname: Urban fullname: Urban, Alexander E. email: aeurban@stanford.edu organization: Department of Genetics, School of Humanities and Science, Stanford University, Stanford, California |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/32919612$$D View this record in MEDLINE/PubMed |
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| Copyright | 2020 Society of Biological Psychiatry Society of Biological Psychiatry Copyright © 2020 Society of Biological Psychiatry. Published by Elsevier Inc. All rights reserved. |
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| Keywords | 15q13.3 Induced pluripotent stem cells Neurons CRISPR–Cas9 Genomics Copy number variants |
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| Snippet | The 15q13.3 microdeletion is associated with several neuropsychiatric disorders, including autism and schizophrenia. Previous association and functional... AbstractBackgroundThe 15q13.3 microdeletion is associated with several neuropsychiatric disorders, including autism and schizophrenia. Previous association and... |
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| SubjectTerms | 15q13.3 Chromosome Deletion Chromosome Disorders - genetics Chromosomes, Human, Pair 15 - genetics Copy number variants CRISPR–Cas9 Epigenome Genomics Humans Induced pluripotent stem cells Intellectual Disability Neurons Psychiatric/Mental Health Seizures Transcriptome |
| Title | Network Effects of the 15q13.3 Microdeletion on the Transcriptome and Epigenome in Human-Induced Neurons |
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