Phenotypic differences in hiPSC NPCs derived from patients with schizophrenia.
paper
Cited
Public
- Authors
- Brennand, K; Savas, J N; Kim, Y; Tran, N; Simone, A; Hashimoto-Torii, K; Beaumont, K G; Kim, H J; Topol, A; Ladran, I; Abdelrahim, M; Matikainen-Ankney, B; Chao, S-h; Mrksich, M; Rakic, P; Fang, G; Zhang, B; Yates, J R; Gage, F H
- Year
- 2015
- Journal
- Molecular psychiatry
- PMID
- 24686136
- DOI
- 10.1038/mp.2014.22
- PMCID
- PMC4182344
Consistent with recent reports indicating that neurons differentiated in vitro from human-induced pluripotent stem cells (hiPSCs) are immature relative to those in the human brain, gene expression comparisons of our hiPSC-derived neurons to the Allen BrainSpan Atlas indicate that they most resemble fetal brain tissue. This finding suggests that, rather than modeling the late features of schizophrenia (SZ), hiPSC-based models may be better suited for the study of disease predisposition. We now report that a significant fraction of the gene signature of SZ hiPSC-derived neurons is conserved in SZ hiPSC neural progenitor cells (NPCs). We used two independent discovery-based approaches-microarray gene expression and stable isotope labeling by amino acids in cell culture (SILAC) quantitative proteomic mass spectrometry analyses-to identify cellular phenotypes in SZ hiPSC NPCs from four SZ patients. From our findings that SZ hiPSC NPCs show abnormal gene expression and protein levels related to cytoskeletal remodeling and oxidative stress, we predicted, and subsequently observed, aberrant migration and increased oxidative stress in SZ hiPSC NPCs. These reproducible NPC phenotypes were identified through scalable assays that can be applied to expanded cohorts of SZ patients, making them a potentially valuable tool with which to study the developmental mechanisms contributing to SZ.
Figure 1
Gene expression of control and schizophrenia (SZ) human-induced pluripotent stem cell (hiPSC) neural progenitor cells (NPCs) and 6-week-old neurons most resembles human first trimester forebrain tissue. (a) Heatmaps produced by Wilcoxon's rank-sum comparisons of control and SZ hiPSC forebrain NPC and 6-week-old neuron microarray gene expression relative to the Allen BrainSpan Atlas. (b) WGCNA (weighted gene co-expression network analysis) of the SZ NPC gene signature identified five modules. (c) Quantitative PCR validation of the altered expression of the adhesion genes NCAM1, NLGN1, NRXN1 and NRXN3 in hiPSC forebrain NPCs from six controls and four SZ patients. Error bars are s.e.m., ***P<0.001. See also Supplementary Figures 1–6.
Figure 2
Aberrant expression of cytoskeletal and oxidative stress proteins in four independent pairwise SILAC (stable isotope labeling by amino acids in cell culture) quantitative proteomic mass spectrometry comparisons of control and schizophrenia (SZ) human induced pluripotent stem cell (hiPSC) forebrain neural progenitor cells (NPCs). (a) Volcano plots of −log10 analysis of variance P-value versus log2 SZ/control protein levels for pairwise analyses of NPCs from patient 1 (left) and patient 3 (right) compared with gender-matched controls 1, 3 or 6, respectively. Key cytoskeletal remodeling proteins (cofilins and profilins) and oxidative stress proteins (thioredoxin and related proteins) are highlighted. From left to right, N=7072, 7226, 5215 and 6357 proteins. (b) Bar graphs showing decreased NLGN3 in P1 SILAC comparisons and increased PFN1, CFL1 and TXN protein levels in four independent SILAC comparisons. Error bars are s.e.m., *P<0.05, **P<0.01, ***P<0.001. See also Supplementary Figure 5.
Figure 3
Aberrant migration in schizophrenia (SZ) human-induced pluripotent stem cell (hiPSC) forebrain neural progenitor cells (NPCs). (a) Representative images of hiPSC forebrain NPC neurosphere outgrowth assay. The average distance between the radius of the inner neurosphere (dense aggregate of nuclei) and outer circumference of cells (white dashed line) was calculated. 4′,6-Diamidino-2-phenylindole (DAPI)-stained nuclei (blue). Scale bar, 100 μm. (b) Neurosphere outgrowth by control and SZ hiPSC forebrain NPCs. (c) Neurosphere outgrowth following coculture with control or SZ hiPSC NPC-conditioned media (CM). (d) Representative images of mixed control and SZ hiPSC NPCs, labeled with lentivirus-green fluorescent protein and lentivirus-red fluorescent protein. Green and red numbers indicate five furthest migrated lentiviral-green fluorescent protein and lentiviral-red fluorescent protein NPCs in reciprocal migration experiments. DAPI-stained nuclei (blue). Scale bar 100 μm. (e) Neurosphere outgrowth in neurospheres composed of mixed control and SZ hiPSC NPCs. (f) Representative images of hiPSC forebrain NPCs after 5 days in a microfluidic device. At time 0, all NPCs were below the microgrooves pictured—migration occurred up from chamber B into chamber A. Migrating neural cells stained with MAP2AB (red), βIII-tubulin (green); DAPI-stained nuclei (blue). Scale bar, 100 μm. (g) Schematic of the microfluidic chambers. At time 0, hiPSC NPCs were added to chamber B and allowed to begin migration toward chamber A via 15-μm grooves. (h) Cellular migration of control and SZ hiPSC NPCs in microfluidic devices at 48 h. (i) Representative images of hiPSC forebrain NPCs in micropatterned laminin spot migration assay. Laminin spot stained (green); migrating neural cells stained with βIII-tubulin (red); and DAPI-stained nuclei (blue). Scale bar, 100 μm. (j) Nearest-neighbor analysis of ‘chaining' between laminin spots by control and SZ hiPSC forebrain NPCs. Error bars are s.e.m., *P<0.05, **P<0.01, ***P<0.001. See also Supplementary Figures 6–8.
Figure 4
Mitochondrial damage and increased oxidative stress in schizophrenia (SZ) human-induced pluripotent stem cell (hiPSC) neural progenitor cells (NPCs). (a) Representative fluorescence-activated cell sorting (FACS) plots for JC-1 red/green fluorescence in control and SZ hiPSC NPCs. (b) FACS analysis for mitochondrial membrane potential (MMP) in control and SZ hiPSC NPCs indicated by median JC-1 red/green fluorescence. (c) OxyBlot western blot for oxidized proteins in SZ hiPSC NPCs. (d) Neurosphere outgrowth by control and SZ hiPSC forebrain NPCs with and without treatment by the anti-oxidant β-mercaptoethanol or valproic acid (VPA). (e) Graph shows fold change of GAPDH and HSP70 expression following H2O2 treatment compared with PBS exposure. There was significantly increased variability observed in SZ hiPSC NPCs as compared with the control (n>50), but no significant differences in the means in all sets of comparisons. Error bars are s.e.m., *P<0.05, ***P<0.001. See also Supplementary Figure 9.
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| Induced pluripotent stem cell reprogramming-associated methylation at the GABRA2 promoter and chr4p12 GABA<sub>A</sub> subunit gene expression in the context of alcohol use disorder. | Goetjen A et al. | — | 2020 | → |
| Integrating CRISPR Engineering and hiPSC-Derived 2D Disease Modeling Systems. | Rehbach K et al. | — | 2020 | → |
| Integration of CRISPR-engineering and hiPSC-based models of psychiatric genomics. | Matos MR et al. | — | 2020 | → |
| Investigation of de novo mutations in a schizophrenia case-parent trio by induced pluripotent stem cell-based in vitro disease modeling: convergence of schizophrenia- and autism-related cellular phenotypes. | Hathy E et al. | — | 2020 | → |
| Investigation of Schizophrenia with Human Induced Pluripotent Stem Cells. | Powell SK et al. | — | 2020 | → |
| iPSC-derived homogeneous populations of developing schizophrenia cortical interneurons have compromised mitochondrial function. | Ni P et al. | — | 2020 | → |
| Loss-of-function Mutations of CUL3, a High Confidence Gene for Psychiatric Disorders, Lead to Aberrant Neurodevelopment In Human Induced Pluripotent Stem Cells. | Fischer S et al. | — | 2020 | → |
| Mechanisms Underlying the Hyperexcitability of CA3 and Dentate Gyrus Hippocampal Neurons Derived From Patients With Bipolar Disorder. | Stern S et al. | — | 2020 | → |
| Mental health dished up-the use of iPSC models in neuropsychiatric research. | McNeill RV et al. | — | 2020 | → |
| Mitochondrial Dysfunction in Schizophrenia. | Ni P et al. | — | 2020 | → |
| Mitochondrial function parameters as a tool for tailored drug treatment of an individual with psychosis: a proof of concept study. | Bar-Yosef T et al. | — | 2020 | → |
| Modeling neuropsychiatric disorders using human induced pluripotent stem cells. | Wang M et al. | — | 2020 | → |
| Modeling Psychiatric Disorder Biology with Stem Cells. | Das D et al. | — | 2020 | → |
| Modeling the complex genetic architectures of brain disease. | Fernando MB et al. | — | 2020 | → |
| Molecular Correlates of Topiramate and GRIK1 rs2832407 Genotype in Pluripotent Stem Cell-Derived Neural Cultures. | Lieberman R et al. | — | 2020 | → |
| Motor Neuron Generation from iPSCs from Identical Twins Discordant for Amyotrophic Lateral Sclerosis. | Seminary ER et al. | — | 2020 | → |
| Neuronal Differentiation of Induced Pluripotent Stem Cells from Schizophrenia Patients in Two-Dimensional and in Three-Dimensional Cultures Reveals Increased Expression of the Kv4.2 Subunit DPP6 That Contributes to Decreased Neuronal Activity. | Naujock M et al. | — | 2020 | → |
| New gene discoveries highlight functional convergence in autism and related neurodevelopmental disorders. | Moyses-Oliveira M et al. | — | 2020 | → |
| Patient hiPSCs Identify Vascular Smooth Muscle Arylacetamide Deacetylase as Protective against Atherosclerosis. | Toyohara T et al. | — | 2020 | → |
| Stem Cells for Improving the Treatment of Neurodevelopmental Disorders. | Donegan JJ et al. | — | 2020 | → |
| The abiding relevance of mouse models of rare mutations to psychiatric neuroscience and therapeutics. | Gogos JA et al. | — | 2020 | → |
| The Evolution of Stem Cells, Disease Modeling, and Drug Discovery for Neurological Disorders. | Pernia C et al. | — | 2020 | → |
| The evolution of the human brain and disease susceptibility. | Pattabiraman K et al. | — | 2020 | → |
| TSC patient-derived isogenic neural progenitor cells reveal altered early neurodevelopmental phenotypes and rapamycin-induced MNK-eIF4E signaling. | Martin P et al. | — | 2020 | → |
| Unraveling Mechanisms of Patient-Specific NRXN1 Mutations in Neuropsychiatric Diseases Using Human Induced Pluripotent Stem Cells. | De Los Angeles A et al. | — | 2020 | → |
| Variation of Human Neural Stem Cells Generating Organizer States In Vitro before Committing to Cortical Excitatory or Inhibitory Neuronal Fates. | Micali N et al. | — | 2020 | → |
| Alcohol-responsive genes identified in human iPSC-derived neural cultures. | Jensen KP et al. | — | 2019 | → |
| Application of Human-Induced Pluripotent Stem Cells (hiPSCs) to Study Synaptopathy of Neurodevelopmental Disorders. | Shen X et al. | — | 2019 | → |
| Are we listening to everything the PARK genes are telling us? | Benson DL et al. | — | 2019 | → |
| Chromatin profiling of cortical neurons identifies individual epigenetic signatures in schizophrenia. | Gusev FE et al. | — | 2019 | → |
| Comparison of CRISPR Genomic Tagging for Affinity Purification and Endogenous Immunoprecipitation Coupled with Quantitative Mass Spectrometry To Identify the Dynamic AMPKα2 Interactome. | Stein BD et al. | — | 2019 | → |
| Contribution of induced pluripotent stem cell technologies to the understanding of cellular phenotypes in schizophrenia. | Balan S et al. | — | 2019 | → |
| Critical period plasticity-related transcriptional aberrations in schizophrenia and bipolar disorder. | Smith MR et al. | — | 2019 | → |
| Differential activity of transcribed enhancers in the prefrontal cortex of 537 cases with schizophrenia and controls. | Hauberg ME et al. | — | 2019 | → |
| Drug discovery in psychopharmacology: from 2D models to cerebral organoids . | Rossetti AC et al. | — | 2019 | → |
| Enhancing the Utility of Preclinical Research in Neuropsychiatry Drug Development. | Kaffman A et al. | — | 2019 | → |
| Human Cerebral Organoids and Fetal Brain Tissue Share Proteomic Similarities. | Nascimento JM et al. | — | 2019 | → |
| Human SPG11 cerebral organoids reveal cortical neurogenesis impairment. | Pérez-Brangulí F et al. | — | 2019 | → |
| Imaging Flow Cytometry Quantifies Neural Genome Dynamics. | Michel N et al. | — | 2019 | → |
| Induced pluripotent stem cells for neural drug discovery. | Farkhondeh A et al. | — | 2019 | → |
| Mitochondrial deficits in human iPSC-derived neurons from patients with 22q11.2 deletion syndrome and schizophrenia. | Li J et al. | — | 2019 | → |
| Modelling mitochondrial dysfunction in Alzheimer's disease using human induced pluripotent stem cells. | Hawkins KE et al. | — | 2019 | → |
| Neuronal impact of patient-specific aberrant NRXN1α splicing. | Flaherty E et al. | — | 2019 | → |
| New considerations for hiPSC-based models of neuropsychiatric disorders. | Hoffman GE et al. | — | 2019 | → |
| New insights on synaptic dysfunction in neuropsychiatric disorders. | Lima Caldeira G et al. | — | 2019 | → |
| Primary Cilia-An Underexplored Topic in Major Mental Illness. | Pruski M et al. | — | 2019 | → |
| Progress in iPSC-Based Modeling of Psychiatric Disorders. | Hoffmann A et al. | — | 2019 | → |
| Proteomic analyses reveal misregulation of LIN28 expression and delayed timing of glial differentiation in human iPS cells with MECP2 loss-of-function. | Kim JJ et al. | — | 2019 | → |
| Role of Microglia in Ataxias. | Ferro A et al. | — | 2019 | → |
| Sodium valproate rescues expression of TRANK1 in iPSC-derived neural cells that carry a genetic variant associated with serious mental illness. | Jiang X et al. | — | 2019 | → |
| Species-specific maturation profiles of human, chimpanzee and bonobo neural cells. | Marchetto MC et al. | — | 2019 | → |
| Stem Cells in Psychiatry. | Kucharska-Mazur J et al. | — | 2019 | → |
| Studying Human Neurological Disorders Using Induced Pluripotent Stem Cells: From 2D Monolayer to 3D Organoid and Blood Brain Barrier Models. | Logan S et al. | — | 2019 | → |
| A Perspective of the Cross-Tissue Interplay of Genetics, Epigenetics, and Transcriptomics, and Their Relation to Brain Based Phenotypes in Schizophrenia. | Liu J et al. | — | 2018 | → |
| Childhood-Onset Schizophrenia: Insights from Induced Pluripotent Stem Cells. | Hoffmann A et al. | — | 2018 | → |
| Combining NGN2 Programming with Developmental Patterning Generates Human Excitatory Neurons with NMDAR-Mediated Synaptic Transmission. | Nehme R et al. | — | 2018 | → |
| Convergent Pathways in Idiopathic Autism Revealed by Time Course Transcriptomic Analysis of Patient-Derived Neurons. | DeRosa BA et al. | — | 2018 | → |
| Dynamic Changes of the Mitochondria in Psychiatric Illnesses: New Mechanistic Insights From Human Neuronal Models. | Srivastava R et al. | — | 2018 | → |
| Effect of leukocyte inhibitory factor on neuron differentiation from human induced pluripotent stem cell-derived neural precursor cells. | Xu L et al. | — | 2018 | → |
| Efficient Generation of CA3 Neurons from Human Pluripotent Stem Cells Enables Modeling of Hippocampal Connectivity In Vitro. | Sarkar A et al. | — | 2018 | → |
| Examining the effects of alcohol on GABA<sub>A</sub> receptor mRNA expression and function in neural cultures generated from control and alcohol dependent donor induced pluripotent stem cells. | Lieberman R et al. | — | 2018 | → |
| Expression-based drug screening of neural progenitor cells from individuals with schizophrenia. | Readhead B et al. | — | 2018 | → |
| Genetics of Alcohol Use Disorder: A Role for Induced Pluripotent Stem Cells? | Prytkova I et al. | — | 2018 | → |
| HippoCA3mpal Stem Cell Models Expose Dysfunctional Circuits in Schizophrenia. | Johnstone M et al. | — | 2018 | → |
| hiPSC-derived neural stem cells from patients with schizophrenia induce an impaired angiogenesis. | Casas BS et al. | — | 2018 | → |
| Induced Pluripotent Stem Cells Reveal Common Neurodevelopmental Genome Deprograming in Schizophrenia. | Narla ST et al. | — | 2018 | → |
| Inhibition of STEP<sub>61</sub> ameliorates deficits in mouse and hiPSC-based schizophrenia models. | Xu J et al. | — | 2018 | → |
| Investigating pediatric disorders with induced pluripotent stem cells. | Durbin MD et al. | — | 2018 | → |
| Isolated Mitochondria Transfer Improves Neuronal Differentiation of Schizophrenia-Derived Induced Pluripotent Stem Cells and Rescues Deficits in a Rat Model of the Disorder. | Robicsek O et al. | — | 2018 | → |
| Modeling Neuropsychiatric and Neurodegenerative Diseases With Induced Pluripotent Stem Cells. | LaMarca EA et al. | — | 2018 | → |
| Modeling Parkinson's Disease Using Patient-specific Induced Pluripotent Stem Cells. | Li H et al. | — | 2018 | → |
| Neural Stem Cell Dysfunction in Human Brain Disorders. | Liszewska E et al. | — | 2018 | → |
| Neuron-specific signatures in the chromosomal connectome associated with schizophrenia risk. | Rajarajan P et al. | — | 2018 | → |
| Pluripotent Stem Cells for Uncovering the Role of Mitochondria in Human Brain Function and Dysfunction. | Zink A et al. | — | 2018 | → |
| Psychiatry in a Dish: Stem Cells and Brain Organoids Modeling Autism Spectrum Disorders. | Ilieva M et al. | — | 2018 | → |
| Rapid Detection of Neurodevelopmental Phenotypes in Human Neural Precursor Cells (NPCs). | Williams M et al. | — | 2018 | → |
| Roles of mitochondria in neuronal development. | Son G et al. | — | 2018 | → |
| Single-cell analysis of diversity in human stem cell-derived neurons. | Harbom LJ et al. | — | 2018 | → |
| Single-cell trajectory analysis of human homogenous neurons carrying a rare RELN variant. | Arioka Y et al. | — | 2018 | → |
| Stem cell models of human synapse development and degeneration. | Wilson ES et al. | — | 2018 | → |
| Synaptic dysfunction in neurodegenerative and neurodevelopmental diseases: an overview of induced pluripotent stem-cell-based disease models. | Taoufik E et al. | — | 2018 | → |
| THC exposure of human iPSC neurons impacts genes associated with neuropsychiatric disorders. | Guennewig B et al. | — | 2018 | → |
| The Role of the Eukaryotic Translation Initiation Factor 4E (eIF4E) in Neuropsychiatric Disorders. | Amorim IS et al. | — | 2018 | → |
| The Use of Stem Cell-Derived Neurons for Understanding Development and Disease of the Cerebellum. | Nayler SP et al. | — | 2018 | → |
| Tracing Early Neurodevelopment in Schizophrenia with Induced Pluripotent Stem Cells. | Ahmad R et al. | — | 2018 | → |
| α-Synuclein oligomers induce early axonal dysfunction in human iPSC-based models of synucleinopathies. | Prots I et al. | — | 2018 | → |
| An Efficient Platform for Astrocyte Differentiation from Human Induced Pluripotent Stem Cells. | Tcw J et al. | — | 2017 | → |
| An update on stem cell biology and engineering for brain development. | Parr CJC et al. | — | 2017 | → |
| Application of induced pluripotent stem cells to understand neurobiological basis of bipolar disorder and schizophrenia. | Liu YN et al. | — | 2017 | → |
| Application of olfactory tissue and its neural progenitors to schizophrenia and psychiatric research. | Lavoie J et al. | — | 2017 | → |
| Are reprogrammed cells a useful tool for studying dopamine dysfunction in psychotic disorders? A review of the current evidence. | Sauerzopf U et al. | — | 2017 | → |
| Brain imaging genetics in ADHD and beyond - Mapping pathways from gene to disorder at different levels of complexity. | Klein M et al. | — | 2017 | → |
| Cell migration in schizophrenia: Patient-derived cells do not regulate motility in response to extracellular matrix. | Tee JY et al. | — | 2017 | → |
| Cellular models to study schizophrenia: A systematic review. | Seshadri M et al. | — | 2017 | → |
| Cerebral organoids reveal early cortical maldevelopment in schizophrenia-computational anatomy and genomics, role of FGFR1. | Stachowiak EK et al. | — | 2017 | → |
| Characterization of macrophages from schizophrenia patients. | Ormel PR et al. | — | 2017 | → |
| Common developmental genome deprogramming in schizophrenia - Role of Integrative Nuclear FGFR1 Signaling (INFS). | Narla ST et al. | — | 2017 | → |
| Complement System in Neural Synapse Elimination in Development and Disease. | Presumey J et al. | — | 2017 | → |
| Concise Review: Induced Pluripotent Stem Cell Models for Neuropsychiatric Diseases. | Adegbola A et al. | — | 2017 | → |
| Epigenomics of Major Depressive Disorders and Schizophrenia: Early Life Decides. | Hoffmann A et al. | — | 2017 | → |
| Evaluating Synthetic Activation and Repression of Neuropsychiatric-Related Genes in hiPSC-Derived NPCs, Neurons, and Astrocytes. | Ho SM et al. | — | 2017 | → |
| Examining FKBP5 mRNA expression in human iPSC-derived neural cells. | Lieberman R et al. | — | 2017 | → |
| Genetically-Informed Patient Selection for iPSC Studies of Complex Diseases May Aid in Reducing Cellular Heterogeneity. | Hoekstra SD et al. | — | 2017 | → |
| High-resolution copy number variation analysis of schizophrenia in Japan. | Kushima I et al. | — | 2017 | → |
| Human induced pluripotent stem cells for modelling neurodevelopmental disorders. | Ardhanareeswaran K et al. | — | 2017 | → |
| Human iPSC-Derived Cerebellar Neurons from a Patient with Ataxia-Telangiectasia Reveal Disrupted Gene Regulatory Networks. | Nayler SP et al. | — | 2017 | → |
| Induced pluripotent stem cells as a discovery tool for Alzheimer׳s disease. | Sullivan SE et al. | — | 2017 | → |
| Induced pluripotent stem cell technology: a decade of progress. | Shi Y et al. | — | 2017 | → |
| Left-Right Asymmetry of Maturation Rates in Human Embryonic Neural Development. | de Kovel CGF et al. | — | 2017 | → |
| Mitochondrial metabolism in early neural fate and its relevance for neuronal disease modeling. | Lorenz C et al. | — | 2017 | → |
| Modeling neurodevelopmental and psychiatric diseases with human iPSCs. | Wen Z | — | 2017 | → |
| Modeling schizophrenia pathogenesis using patient-derived induced pluripotent stem cells (iPSCs). | Noh H et al. | — | 2017 | → |
| Molecular analyses of neurogenic defects in a human pluripotent stem cell model of fragile X syndrome. | Boland MJ et al. | — | 2017 | → |
| Neural organoids for disease phenotyping, drug screening and developmental biology studies. | Hartley BJ et al. | — | 2017 | → |
| Open Chromatin Profiling in hiPSC-Derived Neurons Prioritizes Functional Noncoding Psychiatric Risk Variants and Highlights Neurodevelopmental Loci. | Forrest MP et al. | — | 2017 | → |
| Patient-derived hiPSC neurons with heterozygous CNTNAP2 deletions display altered neuronal gene expression and network activity. | Flaherty E et al. | — | 2017 | → |
| Personalized medicine in a dish: the growing possibility of neuropsychiatric disease drug discovery tailored to patient genetic variants using stem cells. | Brennand KJ | — | 2017 | → |
| Phenotypic screening with primary neurons to identify drug targets for regeneration and degeneration. | Cooper DJ et al. | — | 2017 | → |
| Prospects for Modeling Abnormal Neuronal Function in Schizophrenia Using Human Induced Pluripotent Stem Cells. | Prytkova I et al. | — | 2017 | → |
| Psychosis Risk Candidate ZNF804A Localizes to Synapses and Regulates Neurite Formation and Dendritic Spine Structure. | Deans PJM et al. | — | 2017 | → |
| Revisiting Mitochondrial Function and Metabolism in Pluripotent Stem Cells: Where Do We Stand in Neurological Diseases? | Lopes C et al. | — | 2017 | → |
| Stem cell-derived neurons in the development of targeted treatment for schizophrenia and bipolar disorder. | Watmuff B et al. | — | 2017 | → |
| THC Treatment Alters Glutamate Receptor Gene Expression in Human Stem Cell-Derived Neurons. | Obiorah IV et al. | — | 2017 | → |
| The Importance of Non-neuronal Cell Types in hiPSC-Based Disease Modeling and Drug Screening. | Gonzalez DM et al. | — | 2017 | → |
| Transcriptional signatures of schizophrenia in hiPSC-derived NPCs and neurons are concordant with post-mortem adult brains. | Hoffman GE et al. | — | 2017 | → |
| Understanding neurodevelopmental disorders using human pluripotent stem cell-derived neurons. | Tamburini C et al. | — | 2017 | → |
| Using hiPSCs to model neuropsychiatric copy number variations (CNVs) has potential to reveal underlying disease mechanisms. | Flaherty EK et al. | — | 2017 | → |
| What if it was easier to prevent schizophrenia than to treat it? | J Brennand K | — | 2017 | → |
| Activity-Dependent Changes in Gene Expression in Schizophrenia Human-Induced Pluripotent Stem Cell Neurons. | Roussos P et al. | — | 2016 | → |
| A Dishful of a Troubled Mind: Induced Pluripotent Stem Cells in Psychiatric Research. | Kálmán S et al. | — | 2016 | → |
| Advancing drug discovery for neuropsychiatric disorders using patient-specific stem cell models. | Haggarty SJ et al. | — | 2016 | → |
| Analysis of induced pluripotent stem cells carrying 22q11.2 deletion. | Toyoshima M et al. | — | 2016 | → |
| A role for miR-19 in the migration of adult-born neurons and schizophrenia. | Han J et al. | — | 2016 | → |
| Common pitfalls of stem cell differentiation: a guide to improving protocols for neurodegenerative disease models and research. | Engel M et al. | — | 2016 | → |
| Concise Review: Progress and Challenges in Using Human Stem Cells for Biological and Therapeutics Discovery: Neuropsychiatric Disorders. | Panchision DM | — | 2016 | → |
| Decoding the non-coding genome: elucidating genetic risk outside the coding genome. | Barr CL et al. | — | 2016 | → |
| Disease signatures for schizophrenia and bipolar disorder using patient-derived induced pluripotent stem cells. | Watmuff B et al. | — | 2016 | → |
| Dysregulation of miRNA-9 in a Subset of Schizophrenia Patient-Derived Neural Progenitor Cells. | Topol A et al. | — | 2016 | → |
| Evaluating cell reprogramming, differentiation and conversion technologies in neuroscience. | Mertens J et al. | — | 2016 | → |
| Human Inducible Pluripotent Stem Cells and Autism Spectrum Disorder: Emerging Technologies. | Nestor MW et al. | — | 2016 | → |
| Implications for reactive oxygen species in schizophrenia pathogenesis. | Koga M et al. | — | 2016 | → |
| Induced Pluripotent Stem Cells as a Novel Tool in Psychiatric Research. | Kim S et al. | — | 2016 | → |
| In vivo modeling of neuronal function, axonal impairment and connectivity in neurodegenerative and neuropsychiatric disorders using induced pluripotent stem cells. | Korecka JA et al. | — | 2016 | → |
| Micropatterning Facilitates the Long-Term Growth and Analysis of iPSC-Derived Individual Human Neurons and Neuronal Networks. | Burbulla LF et al. | — | 2016 | → |
| Modeling developmental neuropsychiatric disorders with iPSC technology: challenges and opportunities. | Young-Pearse TL et al. | — | 2016 | → |
| Modeling psychiatric disorders: from genomic findings to cellular phenotypes. | Falk A et al. | — | 2016 | → |
| Molecular substrates of schizophrenia: homeostatic signaling to connectivity. | Landek-Salgado MA et al. | — | 2016 | → |
| Neurodevelopmental origins of bipolar disorder: iPSC models. | O'Shea KS et al. | — | 2016 | → |
| Proteomics and molecular tools for unveiling missing links in the biochemical understanding of schizophrenia. | Nascimento JM et al. | — | 2016 | → |
| Rapid Ngn2-induction of excitatory neurons from hiPSC-derived neural progenitor cells. | Ho SM et al. | — | 2016 | → |
| Recurrent copy number variations as risk factors for neurodevelopmental disorders: critical overview and analysis of clinical implications. | Torres F et al. | — | 2016 | → |
| Reduced CYFIP1 in Human Neural Progenitors Results in Dysregulation of Schizophrenia and Epilepsy Gene Networks. | Nebel RA et al. | — | 2016 | → |
| Schizophrenia patient-derived olfactory neurosphere-derived cells do not respond to extracellular reelin. | Tee JY et al. | — | 2016 | → |
| Serotonergic neurons derived from induced pluripotent stem cells (iPSCs): a new pathway for research on the biology and pharmacology of major depression. | Licinio J et al. | — | 2016 | → |
| The Future is The Past: Methylation QTLs in Schizophrenia. | Hoffmann A et al. | — | 2016 | → |
| The identification of novel genetic variants associated with antipsychotic treatment response outcomes in first-episode schizophrenia patients. | Drögemöller BI et al. | — | 2016 | → |
| The involvement of N-methyl-D-aspartate receptor (NMDAR) subunit NR1 in the pathophysiology of schizophrenia. | Ju P et al. | — | 2016 | → |
| The TLX-miR-219 cascade regulates neural stem cell proliferation in neurodevelopment and schizophrenia iPSC model. | Murai K et al. | — | 2016 | → |
| Transcriptomics analysis of iPSC-derived neurons and modeling of neuropsychiatric disorders. | Lin M et al. | — | 2016 | → |
| Using Induced Pluripotent Stem Cells to Investigate Complex Genetic Psychiatric Disorders. | Temme SJ et al. | — | 2016 | → |
| A dangerous method? The use of induced pluripotent stem cells as a model for schizophrenia. | Jacobs BM | — | 2015 | → |
| Addressing the Genetics of Human Mental Health Disorders in Model Organisms. | McCammon JM et al. | — | 2015 | → |
| Advances in microfluidic platforms for analyzing and regulating human pluripotent stem cells. | Qian T et al. | — | 2015 | → |
| A guide to generating and using hiPSC derived NPCs for the study of neurological diseases. | Topol A et al. | — | 2015 | → |
| Altered WNT Signaling in Human Induced Pluripotent Stem Cell Neural Progenitor Cells Derived from Four Schizophrenia Patients. | Topol A et al. | — | 2015 | → |
| Analysis of conditional heterozygous STXBP1 mutations in human neurons. | Patzke C et al. | — | 2015 | → |
| Challenges in understanding psychiatric disorders and developing therapeutics: a role for zebrafish. | McCammon JM et al. | — | 2015 | → |
| Characterization of molecular and cellular phenotypes associated with a heterozygous <i>CNTNAP2</i> deletion using patient-derived hiPSC neural cells. | Lee IS et al. | — | 2015 | → |
| Co-expression network of neural-differentiation genes shows specific pattern in schizophrenia. | Maschietto M et al. | — | 2015 | → |
| Connectivity and circuitry in a dish versus in a brain. | Chinchalongporn V et al. | — | 2015 | → |
| Converging models of schizophrenia--Network alterations of prefrontal cortex underlying cognitive impairments. | Sakurai T et al. | — | 2015 | → |
| Creating Patient-Specific Neural Cells for the In Vitro Study of Brain Disorders. | Brennand KJ et al. | — | 2015 | → |
| Differential responses to lithium in hyperexcitable neurons from patients with bipolar disorder. | Mertens J et al. | — | 2015 | → |
| Direct somatic lineage conversion. | Tanabe K et al. | — | 2015 | → |
| Epigenetic regulation of UBE3A and roles in human neurodevelopmental disorders. | LaSalle JM et al. | — | 2015 | → |
| Evidence of Mitochondrial Dysfunction within the Complex Genetic Etiology of Schizophrenia. | Hjelm BE et al. | — | 2015 | → |
| From "directed differentiation" to "neuronal induction": modeling neuropsychiatric disease. | Ho SM et al. | — | 2015 | → |
| GABRA2 Alcohol Dependence Risk Allele is Associated with Reduced Expression of Chromosome 4p12 GABAA Subunit Genes in Human Neural Cultures. | Lieberman R et al. | — | 2015 | → |
| Genomic DISC1 Disruption in hiPSCs Alters Wnt Signaling and Neural Cell Fate. | Srikanth P et al. | — | 2015 | → |
| Human Induced Pluripotent Stem Cells Re-Engineer the Study of Neurodevelopmental Disorders. | Kim ES et al. | — | 2015 | → |
| Impact of prenatal environmental stress on cortical development. | Ishii S et al. | — | 2015 | → |
| Importance of being Nernst: Synaptic activity and functional relevance in stem cell-derived neurons. | Bradford AB et al. | — | 2015 | → |
| Increased abundance of translation machinery in stem cell-derived neural progenitor cells from four schizophrenia patients. | Topol A et al. | — | 2015 | → |
| Low oxygen alters mitochondrial function and response to oxidative stress in human neural progenitor cells. | Lages YM et al. | — | 2015 | → |
| Modeling a model: Mouse genetics, 22q11.2 Deletion Syndrome, and disorders of cortical circuit development. | Meechan DW et al. | — | 2015 | → |
| Path from schizophrenia genomics to biology: gene regulation and perturbation in neurons derived from induced pluripotent stem cells and genome editing. | Duan J | — | 2015 | → |
| Probing disorders of the nervous system using reprogramming approaches. | Ichida JK et al. | — | 2015 | → |
| Reduced protein synthesis in schizophrenia patient-derived olfactory cells. | English JA et al. | — | 2015 | → |
| Transcriptomic Analysis of Induced Pluripotent Stem Cells Derived from Patients with Bipolar Disorder from an Old Order Amish Pedigree. | Kim KH et al. | — | 2015 | → |
| Translational potential of olfactory mucosa for the study of neuropsychiatric illness. | Borgmann-Winter K et al. | — | 2015 | → |
| Utilizing induced pluripotent stem cells (iPSCs) to understand the actions of estrogens in human neurons. | Shum C et al. | — | 2015 | → |
| A quantitative framework to evaluate modeling of cortical development by neural stem cells. | Stein JL et al. | — | 2014 | → |
| Evolving toward a human-cell based and multiscale approach to drug discovery for CNS disorders. | Schadt EE et al. | — | 2014 | → |
| Human-induced pluripotent stem cells: potential for neurodegenerative diseases. | Ross CA et al. | — | 2014 | → |
| Human iPSC neurons display activity-dependent neurotransmitter secretion: aberrant catecholamine levels in schizophrenia neurons. | Hook V et al. | — | 2014 | → |
| Is prophylactic psychiatry around the corner? combating adolescent oxidative stress for adult psychosis and schizophrenia. | Sawa A et al. | — | 2014 | → |
| Roles of heat shock factor 1 in neuronal response to fetal environmental risks and its relevance to brain disorders. | Hashimoto-Torii K et al. | — | 2014 | → |
| Synaptic dysregulation in a human iPS cell model of mental disorders. | Wen Z et al. | — | 2014 | → |