Dysregulated protocadherin-pathway activity as an intrinsic defect in induced pluripotent stem cell–derived cortical interneurons from subjects with schizophrenia
We generated cortical interneurons (cINs) from induced pluripotent stem cells derived from 14 healthy controls and 14 subjects with schizophrenia. Both healthy control cINs and schizophrenia cINs were authentic, fired spontaneously, received functional excitatory inputs from host neurons, and induce...
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| Published in | Nature neuroscience Vol. 22; no. 2; pp. 229 - 242 |
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| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
New York
Nature Publishing Group US
01.02.2019
Nature Publishing Group |
| Subjects | |
| Online Access | Get full text |
| ISSN | 1097-6256 1546-1726 1546-1726 |
| DOI | 10.1038/s41593-018-0313-z |
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| Abstract | We generated cortical interneurons (cINs) from induced pluripotent stem cells derived from 14 healthy controls and 14 subjects with schizophrenia. Both healthy control cINs and schizophrenia cINs were authentic, fired spontaneously, received functional excitatory inputs from host neurons, and induced GABA-mediated inhibition in host neurons in vivo. However, schizophrenia cINs had dysregulated expression of protocadherin genes, which lie within documented schizophrenia loci. Mice lacking protocadherin-α showed defective arborization and synaptic density of prefrontal cortex cINs and behavioral abnormalities. Schizophrenia cINs similarly showed defects in synaptic density and arborization that were reversed by inhibitors of protein kinase C, a downstream kinase in the protocadherin pathway. These findings reveal an intrinsic abnormality in schizophrenia cINs in the absence of any circuit-driven pathology. They also demonstrate the utility of homogenous and functional populations of a relevant neuronal subtype for probing pathogenesis mechanisms during development.
Shao et al. report that interneurons derived from iPSCs from schizophrenia patients have altered protocadherin expression and synaptic and arborization deficits. A PKC inhibitor, acting downstream of protocadherin, reversed the arborization deficit. |
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| AbstractList | We generated cortical interneurons (cINs) from induced pluripotent stem cells derived from 14 healthy controls and 14 subjects with schizophrenia. Both healthy control cINs and schizophrenia cINs were authentic, fired spontaneously, received functional excitatory inputs from host neurons, and induced GABA-mediated inhibition in host neurons in vivo. However, schizophrenia cINs had dysregulated expression of protocadherin genes, which lie within documented schizophrenia loci. Mice lacking protocadherin-α showed defective arborization and synaptic density of prefrontal cortex cINs and behavioral abnormalities. Schizophrenia cINs similarly showed defects in synaptic density and arborization that were reversed by inhibitors of protein kinase C, a downstream kinase in the protocadherin pathway. These findings reveal an intrinsic abnormality in schizophrenia cINs in the absence of any circuit-driven pathology. They also demonstrate the utility of homogenous and functional populations of a relevant neuronal subtype for probing pathogenesis mechanisms during development. We generated cortical interneurons (cINs) from induced pluripotent stem cells derived from 14 healthy controls and 14 subjects with schizophrenia. Both healthy control cINs and schizophrenia cINs were authentic, fired spontaneously, received functional excitatory inputs from host neurons, and induced GABA-mediated inhibition in host neurons in vivo. However, schizophrenia cINs had dysregulated expression of protocadherin genes, which lie within documented schizophrenia loci. Mice lacking protocadherin-[alpha] showed defective arborization and synaptic density of prefrontal cortex cINs and behavioral abnormalities. Schizophrenia cINs similarly showed defects in synaptic density and arborization that were reversed by inhibitors of protein kinase C, a downstream kinase in the protocadherin pathway. These findings reveal an intrinsic abnormality in schizophrenia cINs in the absence of any circuit-driven pathology. They also demonstrate the utility of homogenous and functional populations of a relevant neuronal subtype for probing pathogenesis mechanisms during development. We generated cortical interneurons (cINs) from induced pluripotent stem cells derived from 14 healthy controls and 14 subjects with schizophrenia. Both healthy control cINs and schizophrenia cINs were authentic, fired spontaneously, received functional excitatory inputs from host neurons, and induced GABA-mediated inhibition in host neurons in vivo. However, schizophrenia cINs had dysregulated expression of protocadherin genes, which lie within documented schizophrenia loci. Mice lacking protocadherin-α showed defective arborization and synaptic density of prefrontal cortex cINs and behavioral abnormalities. Schizophrenia cINs similarly showed defects in synaptic density and arborization that were reversed by inhibitors of protein kinase C, a downstream kinase in the protocadherin pathway. These findings reveal an intrinsic abnormality in schizophrenia cINs in the absence of any circuit-driven pathology. They also demonstrate the utility of homogenous and functional populations of a relevant neuronal subtype for probing pathogenesis mechanisms during development.We generated cortical interneurons (cINs) from induced pluripotent stem cells derived from 14 healthy controls and 14 subjects with schizophrenia. Both healthy control cINs and schizophrenia cINs were authentic, fired spontaneously, received functional excitatory inputs from host neurons, and induced GABA-mediated inhibition in host neurons in vivo. However, schizophrenia cINs had dysregulated expression of protocadherin genes, which lie within documented schizophrenia loci. Mice lacking protocadherin-α showed defective arborization and synaptic density of prefrontal cortex cINs and behavioral abnormalities. Schizophrenia cINs similarly showed defects in synaptic density and arborization that were reversed by inhibitors of protein kinase C, a downstream kinase in the protocadherin pathway. These findings reveal an intrinsic abnormality in schizophrenia cINs in the absence of any circuit-driven pathology. They also demonstrate the utility of homogenous and functional populations of a relevant neuronal subtype for probing pathogenesis mechanisms during development. We generated cortical interneurons (cINs) from induced pluripotent stem cells derived from 14 healthy controls and 14 subjects with schizophrenia. Both healthy control cINs and schizophrenia cINs were authentic, fired spontaneously, received functional excitatory inputs from host neurons, and induced GABA-mediated inhibition in host neurons in vivo. However, schizophrenia cINs had dysregulated expression of protocadherin genes, which lie within documented schizophrenia loci. Mice lacking protocadherin-[alpha] showed defective arborization and synaptic density of prefrontal cortex cINs and behavioral abnormalities. Schizophrenia cINs similarly showed defects in synaptic density and arborization that were reversed by inhibitors of protein kinase C, a downstream kinase in the protocadherin pathway. These findings reveal an intrinsic abnormality in schizophrenia cINs in the absence of any circuit-driven pathology. They also demonstrate the utility of homogenous and functional populations of a relevant neuronal subtype for probing pathogenesis mechanisms during development. Shao et al. report that interneurons derived from iPSCs from schizophrenia patients have altered protocadherin expression and synaptic and arborization deficits. A PKC inhibitor, acting downstream of protocadherin, reversed the arborization deficit. We generated cortical interneurons (cINs) from induced pluripotent stem cells derived from 14 healthy controls and 14 subjects with schizophrenia. Both healthy control cINs and schizophrenia cINs were authentic, fired spontaneously, received functional excitatory inputs from host neurons, and induced GABA-mediated inhibition in host neurons in vivo. However, schizophrenia cINs had dysregulated expression of protocadherin genes, which lie within documented schizophrenia loci. Mice lacking protocadherin-α showed defective arborization and synaptic density of prefrontal cortex cINs and behavioral abnormalities. Schizophrenia cINs similarly showed defects in synaptic density and arborization that were reversed by inhibitors of protein kinase C, a downstream kinase in the protocadherin pathway. These findings reveal an intrinsic abnormality in schizophrenia cINs in the absence of any circuit-driven pathology. They also demonstrate the utility of homogenous and functional populations of a relevant neuronal subtype for probing pathogenesis mechanisms during development.Shao et al. report that interneurons derived from iPSCs from schizophrenia patients have altered protocadherin expression and synaptic and arborization deficits. A PKC inhibitor, acting downstream of protocadherin, reversed the arborization deficit. We generated cortical interneurons (cINs) from induced pluripotent stem cells derived from 14 healthy controls and 14 subjects with schizophrenia. Both healthy control cINs and schizophrenia cINs were authentic, fired spontaneously, received functional excitatory inputs from host neurons, and induced GABA-mediated inhibition in host neurons in vivo. However, schizophrenia cINs had dysregulated expression of protocadherin genes, which lie within documented schizophrenia loci. Mice lacking protocadherin-α showed defective arborization and synaptic density of prefrontal cortex cINs and behavioral abnormalities. Schizophrenia cINs similarly showed defects in synaptic density and arborization that were reversed by inhibitors of protein kinase C, a downstream kinase in the protocadherin pathway. These findings reveal an intrinsic abnormality in schizophrenia cINs in the absence of any circuit-driven pathology. They also demonstrate the utility of homogenous and functional populations of a relevant neuronal subtype for probing pathogenesis mechanisms during development. Shao et al. report that interneurons derived from iPSCs from schizophrenia patients have altered protocadherin expression and synaptic and arborization deficits. A PKC inhibitor, acting downstream of protocadherin, reversed the arborization deficit. |
| Audience | Academic |
| Author | Cote, Sarah E. Xi, Hualin Simon Perlis, Roy H. Eggan, Kevin C. Park, James M. McPhie, Donna L. Straub, Richard E. Stanton, Patric K. Yin, Changhong Coyle, Joseph T. Fukuda, Emi Cho, Jun-Hyeong Park, Joshua J. Huang, Weihua Eisenberg, Leonard M. Yagi, Takeshi Apud, Jose Cohen, Bruce M. Ghosh, Sulagna Zhao, Joyce Zheng, Kelvin Ni, Peiyan Moghadam, Alexander A. Noh, Haneul Ongur, Dost Kim, Hae-Young Berman, Karen F. Shao, Zhicheng Lanz, Thomas A. Chung, Sangmi Nguyen, Christine Rapoport, Judith L. Bin Kim, Woong Noyes, Elizabeth Weinberger, Daniel R. Parsons, Teagan Hirayama, Teruyoshi |
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Nguyen, Christine organization: Department of Psychiatry, McLean Hospital/Harvard Medical School – sequence: 6 givenname: Sarah E. surname: Cote fullname: Cote, Sarah E. organization: Department of Psychiatry, McLean Hospital/Harvard Medical School – sequence: 7 givenname: Elizabeth surname: Noyes fullname: Noyes, Elizabeth organization: Department of Psychiatry, McLean Hospital/Harvard Medical School – sequence: 8 givenname: Joyce surname: Zhao fullname: Zhao, Joyce organization: Department of Psychiatry, McLean Hospital/Harvard Medical School – sequence: 9 givenname: Teagan surname: Parsons fullname: Parsons, Teagan organization: Department of Psychiatry, McLean Hospital/Harvard Medical School – sequence: 10 givenname: James M. surname: Park fullname: Park, James M. organization: Department of Cell biology and Anatomy, New York Medical College – sequence: 11 givenname: Kelvin surname: Zheng fullname: Zheng, Kelvin organization: Department of Cell biology and Anatomy, New York Medical College – sequence: 12 givenname: Joshua J. surname: Park fullname: Park, Joshua J. organization: Department of Cell biology and Anatomy, New York Medical College – sequence: 13 givenname: Joseph T. orcidid: 0000-0002-0702-1395 surname: Coyle fullname: Coyle, Joseph T. organization: Department of Psychiatry, McLean Hospital/Harvard Medical School – sequence: 14 givenname: Daniel R. orcidid: 0000-0003-2409-2969 surname: Weinberger fullname: Weinberger, Daniel R. organization: Lieber Institute for Brain Development, Johns Hopkins University – sequence: 15 givenname: Richard E. surname: Straub fullname: Straub, Richard E. organization: Lieber Institute for Brain Development, Johns Hopkins University – sequence: 16 givenname: Karen F. surname: Berman fullname: Berman, Karen F. organization: Clinical and Translational Neuroscience Branch, National Institute of Mental Health, National Institutes of Health, Intramural Research Program – sequence: 17 givenname: Jose surname: Apud fullname: Apud, Jose organization: Clinical and Translational Neuroscience Branch, National Institute of Mental Health, National Institutes of Health, Intramural Research Program – sequence: 18 givenname: Dost surname: Ongur fullname: Ongur, Dost organization: Department of Psychiatry, McLean Hospital/Harvard Medical School – sequence: 19 givenname: Bruce M. surname: Cohen fullname: Cohen, Bruce M. organization: Department of Psychiatry, McLean Hospital/Harvard Medical School – sequence: 20 givenname: Donna L. surname: McPhie fullname: McPhie, Donna L. organization: Department of Psychiatry, McLean Hospital/Harvard Medical School – sequence: 21 givenname: Judith L. surname: Rapoport fullname: Rapoport, Judith L. organization: Child Psychiatry Branch, National Institute of Mental Health – sequence: 22 givenname: Roy H. surname: Perlis fullname: Perlis, Roy H. organization: Center for Quantitative Health, Massachusetts General Hospital – sequence: 23 givenname: Thomas A. orcidid: 0000-0003-2483-3122 surname: Lanz fullname: Lanz, Thomas A. organization: Internal Medicine Research Unit, Pfizer Inc – sequence: 24 givenname: Hualin Simon surname: Xi fullname: Xi, Hualin Simon organization: Computational Sciences, Pfizer Inc – sequence: 25 givenname: Changhong surname: Yin fullname: Yin, Changhong organization: Department of Pathology, New York Medical College – sequence: 26 givenname: Weihua surname: Huang fullname: Huang, Weihua organization: Department of Pathology, New York Medical College – sequence: 27 givenname: Teruyoshi surname: Hirayama fullname: Hirayama, Teruyoshi organization: KOKORO-Biology Group, Laboratories for Integrated Biology, Graduate School of Frontier Biosciences, Osaka University, Department of Anatomy and Developmental Neurobiology, Tokushima University Graduate School of Medical Science – sequence: 28 givenname: Emi surname: Fukuda fullname: Fukuda, Emi organization: KOKORO-Biology Group, Laboratories for Integrated Biology, Graduate School of Frontier Biosciences, Osaka University – sequence: 29 givenname: Takeshi surname: Yagi fullname: Yagi, Takeshi organization: KOKORO-Biology Group, Laboratories for Integrated Biology, Graduate School of Frontier Biosciences, Osaka University – sequence: 30 givenname: Sulagna surname: Ghosh fullname: Ghosh, Sulagna organization: Department of Stem Cell and Regenerative Biology, Harvard Stem Cell Institute, Harvard University – sequence: 31 givenname: Kevin C. orcidid: 0000-0003-4436-8467 surname: Eggan fullname: Eggan, Kevin C. organization: Department of Stem Cell and Regenerative Biology, Harvard Stem Cell Institute, Harvard University – sequence: 32 givenname: Hae-Young surname: Kim fullname: Kim, Hae-Young organization: Department of Public Health, New York Medical College – sequence: 33 givenname: Leonard M. surname: Eisenberg fullname: Eisenberg, Leonard M. organization: New York Medical College/Westchester Medical Center Stem Cell Laboratory, Departments of Physiology and Medicine, New York Medical College – sequence: 34 givenname: Alexander A. surname: Moghadam fullname: Moghadam, Alexander A. organization: Department of Cell biology and Anatomy, New York Medical College – sequence: 35 givenname: Patric K. surname: Stanton fullname: Stanton, Patric K. organization: Department of Cell biology and Anatomy, New York Medical College – sequence: 36 givenname: Jun-Hyeong orcidid: 0000-0002-6844-3583 surname: Cho fullname: Cho, Jun-Hyeong email: juncho@ucr.edu organization: Department of Molecular, Cell and Systems Biology, University of California, Riverside – sequence: 37 givenname: Sangmi orcidid: 0000-0002-8737-9978 surname: Chung fullname: Chung, Sangmi email: schung8@nymc.edu organization: Department of Psychiatry, McLean Hospital/Harvard Medical School, Department of Cell biology and Anatomy, New York Medical College |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/30664768$$D View this record in MEDLINE/PubMed |
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| Copyright | The Author(s), under exclusive licence to Springer Nature America, Inc. 2019 COPYRIGHT 2019 Nature Publishing Group 2019© The Author(s), under exclusive licence to Springer Nature America, Inc. 2019 |
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| DOI | 10.1038/s41593-018-0313-z |
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| Snippet | We generated cortical interneurons (cINs) from induced pluripotent stem cells derived from 14 healthy controls and 14 subjects with schizophrenia. Both healthy... |
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| SubjectTerms | 13/100 13/51 631/136 631/378 692/699 Abnormalities Analysis Animal Genetics and Genomics Animals Behavioral Sciences Biological Techniques Biomedical and Life Sciences Biomedicine Brain Cadherins - genetics Cadherins - metabolism Care and treatment Density Female GABA Gene expression Genes Genome-wide association studies Humans Induced Pluripotent Stem Cells Interneurons Interneurons - metabolism Interneurons - pathology Kinases Male Mental disorders Mice Mice, Knockout Neurobiology Neurons Neurophysiology Neurosciences Pathogenesis Pluripotency Prefrontal cortex Prefrontal Cortex - metabolism Prefrontal Cortex - pathology Protein kinase C Protein kinases Proteins Protocadherin Risk factors Schizophrenia Schizophrenia - metabolism Schizophrenia - pathology Signal Transduction - physiology Stem cell transplantation Stem cells Synapses - genetics Synapses - metabolism Synaptic density γ-Aminobutyric acid |
| Title | Dysregulated protocadherin-pathway activity as an intrinsic defect in induced pluripotent stem cell–derived cortical interneurons from subjects with schizophrenia |
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