Modelling schizophrenia using human induced pluripotent stem cells.
paper
Cited
Public
- Authors
- Brennand, Kristen J; Simone, Anthony; Jou, Jessica; Gelboin-Burkhart, Chelsea; Tran, Ngoc; Sangar, Sarah; Li, Yan; Mu, Yangling; Chen, Gong; Yu, Diana; McCarthy, Shane; Sebat, Jonathan; Gage, Fred H
- Year
- 2011
- Journal
- Nature
- PMID
- 21490598
- DOI
- 10.1038/nature09915
- PMCID
- PMC3392969
Schizophrenia (SCZD) is a debilitating neurological disorder with a world-wide prevalence of 1%; there is a strong genetic component, with an estimated heritability of 80-85%. Although post-mortem studies have revealed reduced brain volume, cell size, spine density and abnormal neural distribution in the prefrontal cortex and hippocampus of SCZD brain tissue and neuropharmacological studies have implicated dopaminergic, glutamatergic and GABAergic activity in SCZD, the cell types affected in SCZD and the molecular mechanisms underlying the disease state remain unclear. To elucidate the cellular and molecular defects of SCZD, we directly reprogrammed fibroblasts from SCZD patients into human induced pluripotent stem cells (hiPSCs) and subsequently differentiated these disorder-specific hiPSCs into neurons (Supplementary Fig. 1). SCZD hiPSC neurons showed diminished neuronal connectivity in conjunction with decreased neurite number, PSD95-protein levels and glutamate receptor expression. Gene expression profiles of SCZD hiPSC neurons identified altered expression of many components of the cyclic AMP and WNT signalling pathways. Key cellular and molecular elements of the SCZD phenotype were ameliorated following treatment of SCZD hiPSC neurons with the antipsychotic loxapine. To date, hiPSC neuronal pathology has only been demonstrated in diseases characterized by both the loss of function of a single gene product and rapid disease progression in early childhood. We now report hiPSC neuronal phenotypes and gene expression changes associated with SCZD, a complex genetic psychiatric disorder.
Patient-specific hiPSCs, NPCs and neuronsLeft. hiPSCs express NANOG (green) and TRA-1-60 (red). DAPI (blue). Γ100, scale bar 100 Β΅m. Centre. hiPSC neural progenitor cells (NPCs) express NESTIN (green) and SOX2 (red). DAPI (blue). Γ600, scale bar 100 Β΅m. Right. hiPSC neurons express Ξ²III-tubulin (red) and the dendritic marker MAP2AB (green). DAPI (blue). Γ200, scale bar 100 Β΅m.
Decreased neuronal connectivity in SCZD hiPSC neuronsA. Representative images of control and SCZD hiPSC neurons cotransduced with LV-SYNP-HTG and Rabies-ENVAΞG-RFP, 10 days post rabies transduction. All images were captured using identical laser power and gain settings. Ξ²III-tubulin staining (purple) of the field is shown below each panel. Γ400, scale bar 80 Β΅m. B. Graph showing treatment of SCZD hiPSC neurons with Loxapine resulted in a statistically significant improvement in neuronal connectivity. Error bars are s.e., *P < 0.05.
Decreased neurites and synaptic protein levels but normal electrophysiological and spontaneous calcium transient activity in SCZD hiPSC neuronsA. Graph showing decreased neurites in SCZD hiPSC neurons. B. Graph showing decreased PSD95 protein relative to MAP2AB for SCZD hiPSC neurons. C. Graph showing a trend of decreased PSD95 synaptic density in SCZD hiPSC neurons. DβG. Electrophysiological characterization. hiPSC neurons cultured on astrocytes show normal sodium and potassium currents when voltage-clamped (D), normal induced action potentials when current-clamped (E), and spontaneous excitatory (F) and inhibitory (G) synaptic activity. HβK. Spontaneous calcium transient imaging. Representative spontaneous Fluo-4AM calcium traces of fluorescent intensity versus time generated from three-month-old hiPSC neurons (H). Graph showing no difference between the spike amplitude of spontaneous calcium transients of control and SCZD hiPSC neurons (I). Graph showing no difference between the total numbers of spontaneous calcium transients per total number of ROIs in cultures of control and SCZD hiPSC neurons (J). Graph showing no change in percentage synchronicity per calcium transient in control and SCZD hiPSC neurons (K). Error bars are SE. Asterisks used as follows: *** p<0.001.
RNA expression analysis of control and SCZD hiPSC neuronsAβC. Heat maps showing microarray expression profiles of altered expression of glutamate receptors (A), cAMP signaling (B), and WNT signaling (C) genes in SCZD hiPSC neurons. Fold-change and p-values (diagnosis) provided to the right of each heat map. D. Heat maps showing perturbed expression (highlighted in yellow) of NRG1 and ANK3 in all four SCZD patients, as well as altered expression of ZNF804A, GABRB1, ERBB4, DISC1 and PDE4B in some but not all patients. Fold-change and p-values (diagnosis) provided to the right of each heat map. E. Altered expression of NRG1 is detected in SCZD hiPSC neurons but not in patient fibroblasts, hiPSCs or hiPSC NPCs. F. qPCR validation of altered expression of NRG1, GRIK1, ADCY8, PRKCA, WNT7A, TCF4 and DISC1, as well as response to three weeks of treatment with Loxapine (striped bars) in six-week-old hiPSC neurons. Asterisks used as follows: * p<0.05, ** p<0.01, *** p<0.001.
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| Application of iPSC to Modelling of Respiratory Diseases. | Calvert BA et al. | β | 2020 | β |
| Association of a Reproducible Epigenetic Risk Profile for Schizophrenia With Brain Methylation and Function. | Chen J et al. | β | 2020 | β |
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| Human iPSC modelling of a familial form of atrial fibrillation reveals a gain of function of If and ICaL in patient-derived cardiomyocytes. | Benzoni P et al. | β | 2020 | β |
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| Integrative Analysis Identifies Key Molecular Signatures Underlying Neurodevelopmental Deficits in Fragile X Syndrome. | Utami KH et al. | β | 2020 | β |
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| A Layer-by-Layer Single-Cell Coating Technique To Produce Injectable Beating Mini Heart Tissues via Microfluidics. | Guerzoni LPB et al. | β | 2019 | β |
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| Modelling heme-mediated brain injury associated with cerebral malaria in human brain cortical organoids. | Harbuzariu A et al. | β | 2019 | β |
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| Mutations in thyroid hormone receptor Ξ±1 cause premature neurogenesis and progenitor cell depletion in human cortical development. | Krieger TG et al. | β | 2019 | β |
| Nestin in immature embryonic neurons affects axon growth cone morphology and Semaphorin3a sensitivity. | Bott CJ et al. | β | 2019 | β |
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| Neurite Collapse and Altered ER Ca<sup>2+</sup> Control in Human Parkinson Disease Patient iPSC-Derived Neurons with LRRK2 G2019S Mutation. | Korecka JA et al. | β | 2019 | β |
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| Oligodendrocytes as A New Therapeutic Target in Schizophrenia: From Histopathological Findings to Neuron-Oligodendrocyte Interaction. | Raabe FJ et al. | β | 2019 | β |
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| The Astrocyte-Neuron Interface: An Overview on Molecular and Cellular Dynamics Controlling Formation and Maintenance of the Tripartite Synapse. | Hasan U et al. | β | 2019 | β |
| The effect of rho kinase inhibition on morphological and electrophysiological maturity in iPSC-derived neurons. | Harbom LJ et al. | β | 2019 | β |
| Transcriptomic immaturity inducible by neural hyperexcitation is shared by multiple neuropsychiatric disorders. | Murano T et al. | β | 2019 | β |
| Transient Deregulation of Canonical Wnt Signaling in Developing Pyramidal Neurons Leads to Dendritic Defects and Impaired Behavior. | Viale B et al. | β | 2019 | β |
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| <i>In Vivo</i> Imaging of CNS Injury and Disease. | Akassoglou K et al. | β | 2017 | β |
| Mapping and Analysis of the Connectome of Sympathetic Premotor Neurons in the Rostral Ventrolateral Medulla of the Rat Using a Volumetric Brain Atlas. | Dempsey B et al. | β | 2017 | β |
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| Use of Human Neurons Derived via Cellular Reprogramming Methods to Study Host-Parasite Interactions of Toxoplasma gondii in Neurons. | Halonen SK | β | 2017 | β |
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| Using Human iPSC-Derived Neurons to Uncover Activity-Dependent Non-Coding RNAs. | Bitar M et al. | β | 2017 | β |
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| Concordant but Varied Phenotypes among Duchenne Muscular Dystrophy Patient-Specific Myoblasts Derived using a Human iPSC-Based Model. | Choi IY et al. | β | 2016 | β |
| Cultivate Primary Nasal Epithelial Cells from Children and Reprogram into Induced Pluripotent Stem Cells. | Ulm A et al. | β | 2016 | β |
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| Development of a Scalable, High-Throughput-Compatible Assay to Detect Tau Aggregates Using iPSC-Derived Cortical Neurons Maintained in a Three-Dimensional Culture Format. | Medda X et al. | β | 2016 | β |
| Differentiation of human pluripotent stem cells into Medial Ganglionic Eminence vs. Caudal Ganglionic Eminence cells. | Ahn S et al. | β | 2016 | β |
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| Human iPS Cell-Derived Neurons Uncover the Impact of Increased Ras Signaling in Costello Syndrome. | Rooney GE et al. | β | 2016 | β |
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| Identification of small-molecule inhibitors of Zika virus infection and induced neural cell death via a drug repurposing screen. | Xu M et al. | β | 2016 | β |
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