Personalized Human Astrocyte‐Derived Region‐Specific Forebrain Organoids Recapitulate Endogenous Pathological Features of Focal Cortical Dysplasia

Abstract Focal cortical dysplasia (FCD) is a highly heterogeneous neurodevelopmental malformation, the underlying mechanisms of which remain largely elusive. In this study, personalized dorsal and ventral forebrain organoids (DFOs/VFOs) are generated derived from brain astrocytes of patients with FC...

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Main Authors: Jinhong Xu, Yufei Kong, Nawen Wang, Huijuan Li, Yunteng Li, Zhuo Liu, Yuling Yang, Xiao Yu, Huihui Liu, Jing Ding, Yi Wang, Rui Zhao, Zhicheng Shao
Format: Article
Language:English
Published: Wiley 2025-02-01
Series:Advanced Science
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Online Access:https://doi.org/10.1002/advs.202409774
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author Jinhong Xu
Yufei Kong
Nawen Wang
Huijuan Li
Yunteng Li
Zhuo Liu
Yuling Yang
Xiao Yu
Huihui Liu
Jing Ding
Yi Wang
Rui Zhao
Zhicheng Shao
author_facet Jinhong Xu
Yufei Kong
Nawen Wang
Huijuan Li
Yunteng Li
Zhuo Liu
Yuling Yang
Xiao Yu
Huihui Liu
Jing Ding
Yi Wang
Rui Zhao
Zhicheng Shao
author_sort Jinhong Xu
collection DOAJ
description Abstract Focal cortical dysplasia (FCD) is a highly heterogeneous neurodevelopmental malformation, the underlying mechanisms of which remain largely elusive. In this study, personalized dorsal and ventral forebrain organoids (DFOs/VFOs) are generated derived from brain astrocytes of patients with FCD type II (FCD II). The pathological features of dysmorphic neurons, balloon cells, and astrogliosis are successfully replicated in patient‐derived DFOs, but not in VFOs. It is noteworthy that cardiomyocyte‐like cells correlated with dysmorphic neurons are generated through the high activation of BMP and WNT signaling in some of the FCD‐organoids and patient cortical tissues. Moreover, functional assessments demonstrated the occurrence of epileptiform burst firing and propagative self‐assembling neuronal hyperactivity in both FCD‐DFOs and VFOs. Additionally, the heterotopic cardiomyocyte‐organoids demonstrated the capacity for cardiomyocyte contraction and rhythmic firing. The presence of these cardiomyocytes contributes to the hyperactivity of neural networks in cardioids‐DFOs assembly. In conclusion, the personalized region‐specific forebrain organoids derived from FCD patient astrocytes effectively recapitulate heterogeneous pathological features, offering a valuable platform for the development of precise therapeutic strategies.
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spelling doaj-art-ccc8fbc52b4f4cda937c73b80ce6a5f62025-08-20T02:30:35ZengWileyAdvanced Science2198-38442025-02-01128n/an/a10.1002/advs.202409774Personalized Human Astrocyte‐Derived Region‐Specific Forebrain Organoids Recapitulate Endogenous Pathological Features of Focal Cortical DysplasiaJinhong Xu0Yufei Kong1Nawen Wang2Huijuan Li3Yunteng Li4Zhuo Liu5Yuling Yang6Xiao Yu7Huihui Liu8Jing Ding9Yi Wang10Rui Zhao11Zhicheng Shao12Institute for Translational Brain Research State Key Laboratory of Medical Neurobiology MOE Frontiers Center for Brain Science Institute of Pediatrics National Children's Medical Center Children's Hospital Fudan University Shanghai 200032 ChinaInstitute for Translational Brain Research State Key Laboratory of Medical Neurobiology MOE Frontiers Center for Brain Science Institute of Pediatrics National Children's Medical Center Children's Hospital Fudan University Shanghai 200032 ChinaInstitute for Translational Brain Research State Key Laboratory of Medical Neurobiology MOE Frontiers Center for Brain Science Institute of Pediatrics National Children's Medical Center Children's Hospital Fudan University Shanghai 200032 ChinaInstitute for Translational Brain Research State Key Laboratory of Medical Neurobiology MOE Frontiers Center for Brain Science Institute of Pediatrics National Children's Medical Center Children's Hospital Fudan University Shanghai 200032 ChinaInstitute for Translational Brain Research State Key Laboratory of Medical Neurobiology MOE Frontiers Center for Brain Science Institute of Pediatrics National Children's Medical Center Children's Hospital Fudan University Shanghai 200032 ChinaInstitute for Translational Brain Research State Key Laboratory of Medical Neurobiology MOE Frontiers Center for Brain Science Institute of Pediatrics National Children's Medical Center Children's Hospital Fudan University Shanghai 200032 ChinaDepartment of Neurology Zhongshan Hospital Fudan University Shanghai 200032 ChinaInstitute for Translational Brain Research State Key Laboratory of Medical Neurobiology MOE Frontiers Center for Brain Science Institute of Pediatrics National Children's Medical Center Children's Hospital Fudan University Shanghai 200032 ChinaInstitute for Translational Brain Research State Key Laboratory of Medical Neurobiology MOE Frontiers Center for Brain Science Institute of Pediatrics National Children's Medical Center Children's Hospital Fudan University Shanghai 200032 ChinaDepartment of Neurology Zhongshan Hospital Fudan University Shanghai 200032 ChinaNational Children's Medical Center Children's Hospital of Fudan University Shanghai 201102 ChinaShanghai Children' Hospital School of medicine Shanghai Jiao Tong University Shanghai 200062 ChinaInstitute for Translational Brain Research State Key Laboratory of Medical Neurobiology MOE Frontiers Center for Brain Science Institute of Pediatrics National Children's Medical Center Children's Hospital Fudan University Shanghai 200032 ChinaAbstract Focal cortical dysplasia (FCD) is a highly heterogeneous neurodevelopmental malformation, the underlying mechanisms of which remain largely elusive. In this study, personalized dorsal and ventral forebrain organoids (DFOs/VFOs) are generated derived from brain astrocytes of patients with FCD type II (FCD II). The pathological features of dysmorphic neurons, balloon cells, and astrogliosis are successfully replicated in patient‐derived DFOs, but not in VFOs. It is noteworthy that cardiomyocyte‐like cells correlated with dysmorphic neurons are generated through the high activation of BMP and WNT signaling in some of the FCD‐organoids and patient cortical tissues. Moreover, functional assessments demonstrated the occurrence of epileptiform burst firing and propagative self‐assembling neuronal hyperactivity in both FCD‐DFOs and VFOs. Additionally, the heterotopic cardiomyocyte‐organoids demonstrated the capacity for cardiomyocyte contraction and rhythmic firing. The presence of these cardiomyocytes contributes to the hyperactivity of neural networks in cardioids‐DFOs assembly. In conclusion, the personalized region‐specific forebrain organoids derived from FCD patient astrocytes effectively recapitulate heterogeneous pathological features, offering a valuable platform for the development of precise therapeutic strategies.https://doi.org/10.1002/advs.202409774disease modelingfocal cortical dysplasiaforebrain organoidshuman astrocyteinduced pluripotent stem cells
spellingShingle Jinhong Xu
Yufei Kong
Nawen Wang
Huijuan Li
Yunteng Li
Zhuo Liu
Yuling Yang
Xiao Yu
Huihui Liu
Jing Ding
Yi Wang
Rui Zhao
Zhicheng Shao
Personalized Human Astrocyte‐Derived Region‐Specific Forebrain Organoids Recapitulate Endogenous Pathological Features of Focal Cortical Dysplasia
Advanced Science
disease modeling
focal cortical dysplasia
forebrain organoids
human astrocyte
induced pluripotent stem cells
title Personalized Human Astrocyte‐Derived Region‐Specific Forebrain Organoids Recapitulate Endogenous Pathological Features of Focal Cortical Dysplasia
title_full Personalized Human Astrocyte‐Derived Region‐Specific Forebrain Organoids Recapitulate Endogenous Pathological Features of Focal Cortical Dysplasia
title_fullStr Personalized Human Astrocyte‐Derived Region‐Specific Forebrain Organoids Recapitulate Endogenous Pathological Features of Focal Cortical Dysplasia
title_full_unstemmed Personalized Human Astrocyte‐Derived Region‐Specific Forebrain Organoids Recapitulate Endogenous Pathological Features of Focal Cortical Dysplasia
title_short Personalized Human Astrocyte‐Derived Region‐Specific Forebrain Organoids Recapitulate Endogenous Pathological Features of Focal Cortical Dysplasia
title_sort personalized human astrocyte derived region specific forebrain organoids recapitulate endogenous pathological features of focal cortical dysplasia
topic disease modeling
focal cortical dysplasia
forebrain organoids
human astrocyte
induced pluripotent stem cells
url https://doi.org/10.1002/advs.202409774
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