Altered proliferation and networks in neural cells derived from idiopathic autistic individuals
Autism spectrum disorders (ASD) are common, complex and heterogeneous neurodevelopmental disorders. Cellular and molecular mechanisms responsible for ASD pathogenesis have been proposed based on genetic studies, brain pathology and imaging, but a major impediment to testing ASD hypotheses is the lac...
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| Published in | Molecular psychiatry Vol. 22; no. 6; pp. 820 - 835 |
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| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
London
Nature Publishing Group UK
01.06.2017
Nature Publishing Group |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Autism spectrum disorders (ASD) are common, complex and heterogeneous neurodevelopmental disorders. Cellular and molecular mechanisms responsible for ASD pathogenesis have been proposed based on genetic studies, brain pathology and imaging, but a major impediment to testing ASD hypotheses is the lack of human cell models. Here, we reprogrammed fibroblasts to generate induced pluripotent stem cells, neural progenitor cells (NPCs) and neurons from ASD individuals with early brain overgrowth and non-ASD controls with normal brain size. ASD-derived NPCs display increased cell proliferation because of dysregulation of a β-catenin/BRN2 transcriptional cascade. ASD-derived neurons display abnormal neurogenesis and reduced synaptogenesis leading to functional defects in neuronal networks. Interestingly, defects in neuronal networks could be rescued by insulin growth factor 1 (IGF-1), a drug that is currently in clinical trials for ASD. This work demonstrates that selection of ASD subjects based on endophenotypes unraveled biologically relevant pathway disruption and revealed a potential cellular mechanism for the therapeutic effect of IGF-1. |
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| AbstractList | Autism spectrum disorders (ASD) are common, complex and heterogeneous neurodevelopmental disorders. Cellular and molecular mechanisms responsible for ASD pathogenesis have been proposed based on genetic studies, brain pathology and imaging, but a major impediment to testing ASD hypotheses is the lack of human cell models. Here, we reprogrammed fibroblasts to generate induced pluripotent stem cells, neural progenitor cells (NPCs) and neurons from ASD individuals with early brain overgrowth and non-ASD controls with normal brain size. ASD-derived NPCs display increased cell proliferation because of dysregulation of a [beta]-catenin/BRN2 transcriptional cascade. ASD-derived neurons display abnormal neurogenesis and reduced synaptogenesis leading to functional defects in neuronal networks. Interestingly, defects in neuronal networks could be rescued by insulin growth factor 1 (IGF-1), a drug that is currently in clinical trials for ASD. This work demonstrates that selection of ASD subjects based on endophenotypes unraveled biologically relevant pathway disruption and revealed a potential cellular mechanism for the therapeutic effect of IGF-1. Autism spectrum disorders (ASD) are common, complex and heterogeneous neurodevelopmental disorders. Cellular and molecular mechanisms responsible for ASD pathogenesis have been proposed based on genetic studies, brain pathology and imaging, but a major impediment to testing ASD hypotheses is the lack of human cell models. Here, we reprogrammed fibroblasts to generate induced pluripotent stem cells, neural progenitor cells (NPCs) and neurons from ASD individuals with early brain overgrowth and non-ASD controls with normal brain size. ASD-derived NPCs display increased cell proliferation because of dysregulation of a β-catenin/BRN2 transcriptional cascade. ASD-derived neurons display abnormal neurogenesis and reduced synaptogenesis leading to functional defects in neuronal networks. Interestingly, defects in neuronal networks could be rescued by insulin growth factor 1 (IGF-1), a drug that is currently in clinical trials for ASD. This work demonstrates that selection of ASD subjects based on endophenotypes unraveled biologically relevant pathway disruption and revealed a potential cellular mechanism for the therapeutic effect of IGF-1. Autism spectrum disorders (ASD) are common, complex and heterogeneous neurodevelopmental disorders. Cellular and molecular mechanisms responsible for ASD pathogenesis have been proposed based on genetic studies, brain pathology and imaging, but a major impediment to testing ASD hypotheses is the lack of human cell models. Here, we reprogrammed fibroblasts to generate induced pluripotent stem cells, neural progenitor cells (NPCs) and neurons from ASD individuals with early brain overgrowth and non-ASD controls with normal brain size. ASD-derived NPCs display increased cell proliferation because of dysregulation of a [beta]-catenin/BRN2 transcriptional cascade. ASD-derived neurons display abnormal neurogenesis and reduced synaptogenesis leading to functional defects in neuronal networks. Interestingly, defects in neuronal networks could be rescued by insulin growth factor 1 (IGF-1), a drug that is currently in clinical trials for ASD. This work demonstrates that selection of ASD subjects based on endophenotypes unraveled biologically relevant pathway disruption and revealed a potential cellular mechanism for the therapeutic effect of IGF-1. Molecular Psychiatry (2017) 22, 820-835; doi: 10.1038/mp.2016.95; published online 5 July 2016 Autism spectrum disorders (ASD) are common, complex and heterogeneous neurodevelopmental disorders. Cellular and molecular mechanisms responsible for ASD pathogenesis have been proposed based on genetic studies, brain pathology and imaging, but a major impediment to testing ASD hypotheses is the lack of human cell models. Here, we reprogrammed fibroblasts to generate induced pluripotent stem cells, neural progenitor cells (NPCs) and neurons from ASD individuals with early brain overgrowth and non-ASD controls with normal brain size. ASD-derived NPCs display increased cell proliferation because of dysregulation of a β-catenin/BRN2 transcriptional cascade. ASD-derived neurons display abnormal neurogenesis and reduced synaptogenesis leading to functional defects in neuronal networks. Interestingly, defects in neuronal networks could be rescued by insulin growth factor 1 (IGF-1), a drug that is currently in clinical trials for ASD. This work demonstrates that selection of ASD subjects based on endophenotypes unraveled biologically relevant pathway disruption and revealed a potential cellular mechanism for the therapeutic effect of IGF-1.Autism spectrum disorders (ASD) are common, complex and heterogeneous neurodevelopmental disorders. Cellular and molecular mechanisms responsible for ASD pathogenesis have been proposed based on genetic studies, brain pathology and imaging, but a major impediment to testing ASD hypotheses is the lack of human cell models. Here, we reprogrammed fibroblasts to generate induced pluripotent stem cells, neural progenitor cells (NPCs) and neurons from ASD individuals with early brain overgrowth and non-ASD controls with normal brain size. ASD-derived NPCs display increased cell proliferation because of dysregulation of a β-catenin/BRN2 transcriptional cascade. ASD-derived neurons display abnormal neurogenesis and reduced synaptogenesis leading to functional defects in neuronal networks. Interestingly, defects in neuronal networks could be rescued by insulin growth factor 1 (IGF-1), a drug that is currently in clinical trials for ASD. This work demonstrates that selection of ASD subjects based on endophenotypes unraveled biologically relevant pathway disruption and revealed a potential cellular mechanism for the therapeutic effect of IGF-1. Autism spectrum disorders (ASD) are common, complex and heterogeneous neurodevelopmental disorders. Cellular and molecular mechanisms responsible for ASD pathogenesis have been proposed based on genetic studies, brain pathology, and imaging, but a major impediment to testing ASD hypotheses is the lack of human cell models. Here, we reprogrammed fibroblasts to generate induced pluripotent stem cells (iPSCs), neural progenitor cells (NPCs) and neurons from ASD individuals with early brain overgrowth and non-ASD controls with normal brain size. ASD-derived NPCs display increased cell proliferation due to dysregulation of a β-catenin/BRN2 transcriptional cascade. ASD-derived neurons display abnormal neurogenesis and reduced synaptogenesis leading to functional defects in neuronal networks. Interestingly, defects in neuronal networks could be rescued by IGF-1, a drug that is currently in clinical trials for ASD. This work demonstrates that selection of ASD subjects based on endophenotypes unraveled biologically relevant pathway disruption and revealed a potential cellular mechanism for the therapeutic effect of IGF-1. |
| Audience | Academic |
| Author | Vadodaria, K C Brennand, K J Fu, C Eichenfield, L Pierce, K Beltrao-Braga, P C Pramparo, T Geschwind, D H Nunez, Y Eyler, L T Barnes, C C Ou, J Padmanabhan, K Wynshaw-Boris, A Gage, F H Tian, Y Muotri, A R Freitas, B C Trujillo, C A Mendes, A P D Marchetto, M C Wright, R Belinson, H Courchesne, E Ghosh, H |
| AuthorAffiliation | 1 The Salk Institute, Laboratory of Genetics, La Jolla, CA 92037, USA 3 University of California Los Angeles, Program in Neurogenetics, Department of Neurology, Center for Autism Research and Treatment, Semel Institute, David Geffen School of Medicine, Los Angeles, CA 90402, USA 2 University of California San Francisco, Department of Pediatrics, Institute for Human Genetics, CA 94143, USA 4 University of California San Diego, Department of Pediatrics/Rady Children’s Hospital San Diego, Department of Cellular & Molecular Medicine, Stem Cell Program, La Jolla, CA 92093-0695, USA 9 University of California San Diego, Department of Neurosciences, La Jolla, CA 92093, USA 5 Case Western Reserve University, Department of Genetics and Genome Sciences, Cleveland, OH 44106, USA 7 University of Rochester School of Medicine and Dentistry, Department of Neuroscience, 601 Elmwood Avenue, Box 603 Rochester, NY 14642 6 University of São Paulo, Department of Obstetrics, Department of Surgery, Center for Cellu |
| AuthorAffiliation_xml | – name: 6 University of São Paulo, Department of Obstetrics, Department of Surgery, Center for Cellular and Molecular Therapy, São Paulo, Brazil – name: 4 University of California San Diego, Department of Pediatrics/Rady Children’s Hospital San Diego, Department of Cellular & Molecular Medicine, Stem Cell Program, La Jolla, CA 92093-0695, USA – name: 1 The Salk Institute, Laboratory of Genetics, La Jolla, CA 92037, USA – name: 3 University of California Los Angeles, Program in Neurogenetics, Department of Neurology, Center for Autism Research and Treatment, Semel Institute, David Geffen School of Medicine, Los Angeles, CA 90402, USA – name: 8 Department of Psychiatry, Icahn School of Medicine at Mount Sinai, 1425 Madison Avenue, New York, NY 10029, USA – name: 9 University of California San Diego, Department of Neurosciences, La Jolla, CA 92093, USA – name: 7 University of Rochester School of Medicine and Dentistry, Department of Neuroscience, 601 Elmwood Avenue, Box 603 Rochester, NY 14642 – name: 5 Case Western Reserve University, Department of Genetics and Genome Sciences, Cleveland, OH 44106, USA – name: 2 University of California San Francisco, Department of Pediatrics, Institute for Human Genetics, CA 94143, USA |
| Author_xml | – sequence: 1 givenname: M C surname: Marchetto fullname: Marchetto, M C organization: Laboratory of Genetics, The Salk Institute – sequence: 2 givenname: H surname: Belinson fullname: Belinson, H organization: Department of Pediatrics, Institute for Human Genetics, University of California – sequence: 3 givenname: Y surname: Tian fullname: Tian, Y organization: Department of Neurology, Program in Neurogenetics, Center for Autism Research and Treatment, Semel Institute, David Geffen School of Medicine, University of California – sequence: 4 givenname: B C surname: Freitas fullname: Freitas, B C organization: Department of Pediatrics/Rady Children's Hospital San Diego, Department of Cellular and Molecular Medicine, Stem Cell Program, University of California, San Diego – sequence: 5 givenname: C surname: Fu fullname: Fu, C organization: Department of Genetics and Genome Sciences, Case Western Reserve University – sequence: 6 givenname: K C surname: Vadodaria fullname: Vadodaria, K C organization: Laboratory of Genetics, The Salk Institute – sequence: 7 givenname: P C surname: Beltrao-Braga fullname: Beltrao-Braga, P C organization: Department of Pediatrics/Rady Children's Hospital San Diego, Department of Cellular and Molecular Medicine, Stem Cell Program, University of California, San Diego, Department of Obstetrics and Surgery, Center for Cellular and Molecular Therapy, University of São Paulo – sequence: 8 givenname: C A surname: Trujillo fullname: Trujillo, C A organization: Department of Pediatrics/Rady Children's Hospital San Diego, Department of Cellular and Molecular Medicine, Stem Cell Program, University of California, San Diego – sequence: 9 givenname: A P D surname: Mendes fullname: Mendes, A P D organization: Laboratory of Genetics, The Salk Institute – sequence: 10 givenname: K surname: Padmanabhan fullname: Padmanabhan, K organization: Department of Neuroscience, University of Rochester School of Medicine and Dentistry – sequence: 11 givenname: Y surname: Nunez fullname: Nunez, Y organization: Laboratory of Genetics, The Salk Institute, Department of Pediatrics/Rady Children's Hospital San Diego, Department of Cellular and Molecular Medicine, Stem Cell Program, University of California, San Diego – sequence: 12 givenname: J surname: Ou fullname: Ou, J organization: Department of Neurology, Program in Neurogenetics, Center for Autism Research and Treatment, Semel Institute, David Geffen School of Medicine, University of California – sequence: 13 givenname: H surname: Ghosh fullname: Ghosh, H organization: Laboratory of Genetics, The Salk Institute – sequence: 14 givenname: R surname: Wright fullname: Wright, R organization: Laboratory of Genetics, The Salk Institute – sequence: 15 givenname: K J surname: Brennand fullname: Brennand, K J organization: Department of Psychiatry, Icahn School of Medicine at Mount Sinai – sequence: 16 givenname: K surname: Pierce fullname: Pierce, K organization: Department of Neurosciences, University of California, San Diego – sequence: 17 givenname: L surname: Eichenfield fullname: Eichenfield, L organization: Department of Neurosciences, University of California, San Diego – sequence: 18 givenname: T surname: Pramparo fullname: Pramparo, T organization: Department of Neurosciences, University of California, San Diego – sequence: 19 givenname: L T orcidid: 0000-0002-7783-8798 surname: Eyler fullname: Eyler, L T organization: Department of Neurosciences, University of California, San Diego – sequence: 20 givenname: C C surname: Barnes fullname: Barnes, C C organization: Department of Neurosciences, University of California, San Diego – sequence: 21 givenname: E surname: Courchesne fullname: Courchesne, E organization: Department of Neurosciences, University of California, San Diego – sequence: 22 givenname: D H surname: Geschwind fullname: Geschwind, D H organization: Department of Neurology, Program in Neurogenetics, Center for Autism Research and Treatment, Semel Institute, David Geffen School of Medicine, University of California – sequence: 23 givenname: F H surname: Gage fullname: Gage, F H organization: Laboratory of Genetics, The Salk Institute – sequence: 24 givenname: A surname: Wynshaw-Boris fullname: Wynshaw-Boris, A email: ajw168@case.edu organization: Department of Pediatrics, Institute for Human Genetics, University of California, Department of Genetics and Genome Sciences, Case Western Reserve University – sequence: 25 givenname: A R surname: Muotri fullname: Muotri, A R email: muotri@ucsd.edu organization: Department of Pediatrics/Rady Children's Hospital San Diego, Department of Cellular and Molecular Medicine, Stem Cell Program, University of California, San Diego |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/27378147$$D View this record in MEDLINE/PubMed |
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| Snippet | Autism spectrum disorders (ASD) are common, complex and heterogeneous neurodevelopmental disorders. Cellular and molecular mechanisms responsible for ASD... |
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| Title | Altered proliferation and networks in neural cells derived from idiopathic autistic individuals |
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