PTEN deficiency reprogrammes human neural stem cells towards a glioblastoma stem cell-like phenotype

Abstract PTEN is a tumour suppressor frequently mutated in many types of cancers. Here we show that targeted disruption of PTEN leads to neoplastic transformation of human neural stem cells (NSCs), but not mesenchymal stem cells. PTEN-deficient NSCs display neoplasm-associated metabolic and gene exp...

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Main Authors: Shunlei Duan, Guohong Yuan, Xiaomeng Liu, Ruotong Ren, Jingyi Li, Weizhou Zhang, Jun Wu, Xiuling Xu, Lina Fu, Ying Li, Jiping Yang, Weiqi Zhang, Ruijun Bai, Fei Yi, Keiichiro Suzuki, Hua Gao, Concepcion Rodriguez Esteban, Chuanbao Zhang, Juan Carlos Izpisua Belmonte, Zhiguo Chen, Xiaomin Wang, Tao Jiang, Jing Qu, Fuchou Tang, Guang-Hui Liu
Format: Article
Language:English
Published: Nature Portfolio 2015-12-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/ncomms10068
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author Shunlei Duan
Guohong Yuan
Xiaomeng Liu
Ruotong Ren
Jingyi Li
Weizhou Zhang
Jun Wu
Xiuling Xu
Lina Fu
Ying Li
Jiping Yang
Weiqi Zhang
Ruijun Bai
Fei Yi
Keiichiro Suzuki
Hua Gao
Concepcion Rodriguez Esteban
Chuanbao Zhang
Juan Carlos Izpisua Belmonte
Zhiguo Chen
Xiaomin Wang
Tao Jiang
Jing Qu
Fuchou Tang
Guang-Hui Liu
author_facet Shunlei Duan
Guohong Yuan
Xiaomeng Liu
Ruotong Ren
Jingyi Li
Weizhou Zhang
Jun Wu
Xiuling Xu
Lina Fu
Ying Li
Jiping Yang
Weiqi Zhang
Ruijun Bai
Fei Yi
Keiichiro Suzuki
Hua Gao
Concepcion Rodriguez Esteban
Chuanbao Zhang
Juan Carlos Izpisua Belmonte
Zhiguo Chen
Xiaomin Wang
Tao Jiang
Jing Qu
Fuchou Tang
Guang-Hui Liu
author_sort Shunlei Duan
collection DOAJ
description Abstract PTEN is a tumour suppressor frequently mutated in many types of cancers. Here we show that targeted disruption of PTEN leads to neoplastic transformation of human neural stem cells (NSCs), but not mesenchymal stem cells. PTEN-deficient NSCs display neoplasm-associated metabolic and gene expression profiles and generate intracranial tumours in immunodeficient mice. PTEN is localized to the nucleus in NSCs, binds to the PAX7 promoter through association with cAMP responsive element binding protein 1 (CREB)/CREB binding protein (CBP) and inhibits PAX7 transcription. PTEN deficiency leads to the upregulation of PAX7, which in turn promotes oncogenic transformation of NSCs and instates ‘aggressiveness’ in human glioblastoma stem cells. In a large clinical database, we find increased PAX7 levels in PTEN-deficient glioblastoma. Furthermore, we identify that mitomycin C selectively triggers apoptosis in NSCs with PTEN deficiency. Together, we uncover a potential mechanism of how PTEN safeguards NSCs, and establish a cellular platform to identify factors involved in NSC transformation, potentially permitting personalized treatment of glioblastoma.
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publishDate 2015-12-01
publisher Nature Portfolio
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spelling doaj-art-d32f7136da0d42e3becf0c27cf41f2bf2025-08-20T03:16:00ZengNature PortfolioNature Communications2041-17232015-12-016111410.1038/ncomms10068PTEN deficiency reprogrammes human neural stem cells towards a glioblastoma stem cell-like phenotypeShunlei Duan0Guohong Yuan1Xiaomeng Liu2Ruotong Ren3Jingyi Li4Weizhou Zhang5Jun Wu6Xiuling Xu7Lina Fu8Ying Li9Jiping Yang10Weiqi Zhang11Ruijun Bai12Fei Yi13Keiichiro Suzuki14Hua Gao15Concepcion Rodriguez Esteban16Chuanbao Zhang17Juan Carlos Izpisua Belmonte18Zhiguo Chen19Xiaomin Wang20Tao Jiang21Jing Qu22Fuchou Tang23Guang-Hui Liu24National Laboratory of Biomacromolecules, Institute of Biophysics, Chinese Academy of SciencesNational Laboratory of Biomacromolecules, Institute of Biophysics, Chinese Academy of SciencesBiodynamic Optical Imaging Center, College of Life Sciences, Peking UniversityNational Laboratory of Biomacromolecules, Institute of Biophysics, Chinese Academy of SciencesBiodynamic Optical Imaging Center, College of Life Sciences, Peking UniversityDepartment of Pathology, Carver College of Medicine, University of IowaGene Expression Laboratory, Salk Institute for Biological StudiesNational Laboratory of Biomacromolecules, Institute of Biophysics, Chinese Academy of SciencesNational Laboratory of Biomacromolecules, Institute of Biophysics, Chinese Academy of SciencesNational Laboratory of Biomacromolecules, Institute of Biophysics, Chinese Academy of SciencesNational Laboratory of Biomacromolecules, Institute of Biophysics, Chinese Academy of SciencesNational Laboratory of Biomacromolecules, Institute of Biophysics, Chinese Academy of SciencesFSU-CAS Innovation InstituteDepartment of Molecular and Cellular Physiology, Stanford University School of MedicineGene Expression Laboratory, Salk Institute for Biological StudiesResearch Center for Translational Medicine, Shanghai East Hospital, School of Life Sciences and Technology, Tongji UniversityGene Expression Laboratory, Salk Institute for Biological StudiesBeijing Institute for Brain DisordersGene Expression Laboratory, Salk Institute for Biological StudiesCell Therapy Center, Xuanwu Hospital Capital Medical UniversityBeijing Institute for Brain DisordersBeijing Institute for Brain DisordersState Key Laboratory of Stem Cell and Reproductive Biology, Institute of Zoology, Chinese Academy of SciencesBiodynamic Optical Imaging Center, College of Life Sciences, Peking UniversityNational Laboratory of Biomacromolecules, Institute of Biophysics, Chinese Academy of SciencesAbstract PTEN is a tumour suppressor frequently mutated in many types of cancers. Here we show that targeted disruption of PTEN leads to neoplastic transformation of human neural stem cells (NSCs), but not mesenchymal stem cells. PTEN-deficient NSCs display neoplasm-associated metabolic and gene expression profiles and generate intracranial tumours in immunodeficient mice. PTEN is localized to the nucleus in NSCs, binds to the PAX7 promoter through association with cAMP responsive element binding protein 1 (CREB)/CREB binding protein (CBP) and inhibits PAX7 transcription. PTEN deficiency leads to the upregulation of PAX7, which in turn promotes oncogenic transformation of NSCs and instates ‘aggressiveness’ in human glioblastoma stem cells. In a large clinical database, we find increased PAX7 levels in PTEN-deficient glioblastoma. Furthermore, we identify that mitomycin C selectively triggers apoptosis in NSCs with PTEN deficiency. Together, we uncover a potential mechanism of how PTEN safeguards NSCs, and establish a cellular platform to identify factors involved in NSC transformation, potentially permitting personalized treatment of glioblastoma.https://doi.org/10.1038/ncomms10068
spellingShingle Shunlei Duan
Guohong Yuan
Xiaomeng Liu
Ruotong Ren
Jingyi Li
Weizhou Zhang
Jun Wu
Xiuling Xu
Lina Fu
Ying Li
Jiping Yang
Weiqi Zhang
Ruijun Bai
Fei Yi
Keiichiro Suzuki
Hua Gao
Concepcion Rodriguez Esteban
Chuanbao Zhang
Juan Carlos Izpisua Belmonte
Zhiguo Chen
Xiaomin Wang
Tao Jiang
Jing Qu
Fuchou Tang
Guang-Hui Liu
PTEN deficiency reprogrammes human neural stem cells towards a glioblastoma stem cell-like phenotype
Nature Communications
title PTEN deficiency reprogrammes human neural stem cells towards a glioblastoma stem cell-like phenotype
title_full PTEN deficiency reprogrammes human neural stem cells towards a glioblastoma stem cell-like phenotype
title_fullStr PTEN deficiency reprogrammes human neural stem cells towards a glioblastoma stem cell-like phenotype
title_full_unstemmed PTEN deficiency reprogrammes human neural stem cells towards a glioblastoma stem cell-like phenotype
title_short PTEN deficiency reprogrammes human neural stem cells towards a glioblastoma stem cell-like phenotype
title_sort pten deficiency reprogrammes human neural stem cells towards a glioblastoma stem cell like phenotype
url https://doi.org/10.1038/ncomms10068
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