Tumor Spheroids of an Aggressive Form of Central Neurocytoma Have Transit-Amplifying Progenitor Characteristics with Enhanced EGFR and Tumor Stem Cell Signaling
Central neurocytoma (CN) has been known as a benign neuronal tumor. In rare cases, CN undergoes malignant transformation to glioblastomas (GBM). Here we examined its cellular origin by characterizing differentiation potential and gene expression of CN-spheroids. First, we demonstrate that both CN ti...
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| Published in | Experimental neurobiology Vol. 30; no. 2; pp. 120 - 143 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
Korea (South)
The Korean Society for Brain and Neural Sciences
30.04.2021
한국뇌신경과학회 |
| Subjects | |
| Online Access | Get full text |
| ISSN | 1226-2560 2093-8144 |
| DOI | 10.5607/en21004 |
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| Abstract | Central neurocytoma (CN) has been known as a benign neuronal tumor. In rare cases, CN undergoes malignant transformation to glioblastomas (GBM). Here we examined its cellular origin by characterizing differentiation potential and gene expression of CN-spheroids. First, we demonstrate that both CN tissue and cultured primary cells recapitulate the hierarchal cellular composition of subventricular zone (SVZ), which is comprised of neural stem cells (NSCs), transit amplifying progenitors (TAPs), and neuroblasts. We then derived spheroids from CN which displayed EGFR+/ MASH+ TAP and BLBP+ radial glial cell (RGC) characteristic, and mitotic neurogenesis and gliogenesis by single spheroids were observed with cycling multipotential cells. CN-spheroids expressed increased levels of pluripotency and tumor stem cell genes such as
and
, when compared to their differentiated cells and human NSCs. Importantly, Gene Set Enrichment Analysis showed that gene sets of GBM-Spheroids, EGFR Signaling, and Packaging of Telomere Ends are enriched in CN-spheroids in comparison with their differentiated cells. We speculate that CN tumor stem cells have TAP and RGC characteristics, and upregulation of EGFR signaling as well as downregulation of eph-ephrin signaling have critical roles in tumorigenesis of CN. And their ephemeral nature of TAPs destined to neuroblasts, might reflect benign nature of CN. |
|---|---|
| AbstractList | Central neurocytoma (CN) has been known as a benign neuronal tumor. In rare cases, CN undergoes malignant transformation to glioblastomas (GBM). Here we examined its cellular origin by characterizing differentiation potential and gene expression of CN-spheroids. First, we demonstrate that both CN tissue and cultured primary cells recapitulate the hierarchal cellular composition of subventricular zone (SVZ), which is comprised of neural stem cells (NSCs), transit amplifying progenitors (TAPs), and neuroblasts. We then derived spheroids from CN which displayed EGFR+/ MASH+ TAP and BLBP+ radial glial cell (RGC) characteristic, and mitotic neurogenesis and gliogenesis by single spheroids were observed with cycling multipotential cells. CN-spheroids expressed increased levels of pluripotency and tumor stem cell genes such as KLF4 and TPD5L1, when compared to their differentiated cells and human NSCs. Importantly, Gene Set Enrichment Analysis showed that gene sets of GBM-Spheroids, EGFR Signaling, and Packaging of Telomere Ends are enriched in CN-spheroids in comparison with their differentiated cells. We speculate that CN tumor stem cells have TAP and RGC characteristics, and upregulation of EGFR signaling as well as downregulation of eph-ephrin signaling have critical roles in tumorigenesis of CN. And their ephemeral nature of TAPs destined to neuroblasts, might reflect benign nature of CN. KCI Citation Count: 4 Central neurocytoma (CN) has been known as a benign neuronal tumor. In rare cases, CN undergoes malignant transformation to glioblastomas (GBM). Here we examined its cellular origin by characterizing differentiation potential and gene expression of CN-spheroids. First, we demonstrate that both CN tissue and cultured primary cells recapitulate the hierarchal cellular composition of subventricular zone (SVZ), which is comprised of neural stem cells (NSCs), transit amplifying progenitors (TAPs), and neuroblasts. We then derived spheroids from CN which displayed EGFR+/ MASH+ TAP and BLBP+ radial glial cell (RGC) characteristic, and mitotic neurogenesis and gliogenesis by single spheroids were observed with cycling multipotential cells. CN-spheroids expressed increased levels of pluripotency and tumor stem cell genes such as and , when compared to their differentiated cells and human NSCs. Importantly, Gene Set Enrichment Analysis showed that gene sets of GBM-Spheroids, EGFR Signaling, and Packaging of Telomere Ends are enriched in CN-spheroids in comparison with their differentiated cells. We speculate that CN tumor stem cells have TAP and RGC characteristics, and upregulation of EGFR signaling as well as downregulation of eph-ephrin signaling have critical roles in tumorigenesis of CN. And their ephemeral nature of TAPs destined to neuroblasts, might reflect benign nature of CN. Central neurocytoma (CN) has been known as a benign neuronal tumor. In rare cases, CN undergoes malignant transformation to glioblastomas (GBM). Here we examined its cellular origin by characterizing differentiation potential and gene expression of CN-spheroids. First, we demonstrate that both CN tissue and cultured primary cells recapitulate the hierarchal cellular composition of subventricular zone (SVZ), which is comprised of neural stem cells (NSCs), transit amplifying progenitors (TAPs), and neuroblasts. We then derived spheroids from CN which displayed EGFR+/ MASH+ TAP and BLBP+ radial glial cell (RGC) characteristic, and mitotic neurogenesis and gliogenesis by single spheroids were observed with cycling multipotential cells. CN-spheroids expressed increased levels of pluripotency and tumor stem cell genes such as KLF4 and TPD5L1, when compared to their differentiated cells and human NSCs. Importantly, Gene Set Enrichment Analysis showed that gene sets of GBM-Spheroids, EGFR Signaling, and Packaging of Telomere Ends are enriched in CN-spheroids in comparison with their differentiated cells. We speculate that CN tumor stem cells have TAP and RGC characteristics, and upregulation of EGFR signaling as well as downregulation of eph-ephrin signaling have critical roles in tumorigenesis of CN. And their ephemeral nature of TAPs destined to neuroblasts, might reflect benign nature of CN.Central neurocytoma (CN) has been known as a benign neuronal tumor. In rare cases, CN undergoes malignant transformation to glioblastomas (GBM). Here we examined its cellular origin by characterizing differentiation potential and gene expression of CN-spheroids. First, we demonstrate that both CN tissue and cultured primary cells recapitulate the hierarchal cellular composition of subventricular zone (SVZ), which is comprised of neural stem cells (NSCs), transit amplifying progenitors (TAPs), and neuroblasts. We then derived spheroids from CN which displayed EGFR+/ MASH+ TAP and BLBP+ radial glial cell (RGC) characteristic, and mitotic neurogenesis and gliogenesis by single spheroids were observed with cycling multipotential cells. CN-spheroids expressed increased levels of pluripotency and tumor stem cell genes such as KLF4 and TPD5L1, when compared to their differentiated cells and human NSCs. Importantly, Gene Set Enrichment Analysis showed that gene sets of GBM-Spheroids, EGFR Signaling, and Packaging of Telomere Ends are enriched in CN-spheroids in comparison with their differentiated cells. We speculate that CN tumor stem cells have TAP and RGC characteristics, and upregulation of EGFR signaling as well as downregulation of eph-ephrin signaling have critical roles in tumorigenesis of CN. And their ephemeral nature of TAPs destined to neuroblasts, might reflect benign nature of CN. Central neurocytoma (CN) has been known as a benign neuronal tumor. In rare cases, CN undergoes malignant transformation to glioblastomas (GBM). Here we examined its cellular origin by characterizing differentiation potential and gene expression of CN-spheroids. First, we demonstrate that both CN tissue and cultured primary cells recapitulate the hierarchal cellular composition of subventricular zone (SVZ), which is comprised of neural stem cells (NSCs), transit amplifying progenitors (TAPs), and neuroblasts. We then derived spheroids from CN which displayed EGFR+/MASH+ TAP and BLBP+ radial glial cell (RGC) characteristic, and mitotic neurogenesis and gliogenesis by single spheroids were observed with cycling multipotential cells. CN-spheroids expressed increased levels of pluripotency and tumor stem cell genes such as KLF4 and TPD5L1 , when compared to their differentiated cells and human NSCs. Importantly, Gene Set Enrichment Analysis showed that gene sets of GBM-Spheroids, EGFR Signaling, and Packaging of Telomere Ends are enriched in CN-spheroids in comparison with their differentiated cells. We speculate that CN tumor stem cells have TAP and RGC characteristics, and upregulation of EGFR signaling as well as downregulation of eph-ephrin signaling have critical roles in tumorigenesis of CN. And their ephemeral nature of TAPs destined to neuroblasts, might reflect benign nature of CN. |
| Author | Park, Sung-Hye Han, Kyung-Seok Kim, Dong Gyu Lee, Kiyoung Moon, Hyo Eun Park, Hyung Woo Kim, Sang Jeong Park, Kwang Woo Lee, C. Justin Heo, Man Seung Paek, Sun Ha Hong, Yun Hwa Shin, Hye Young Park, Hye Ran Kim, Yona |
| AuthorAffiliation | 3 Department of Neurophysiology, Seoul National University College of Medicine, Seoul 03082, Korea 6 Ischemic/Hypoxic Disease Institute, Cancer Research Institute, Seoul National University College of Medicine, Seoul 03082, Korea 5 Department of Pathology, Seoul National University College of Medicine, Seoul 03082, Korea 1 Department of Neurosurgery, Seoul National University College of Medicine, Seoul 03082, Korea 2 Center for Cognition and Sociality, Institute for Basic Science, Daejeon 34126, Korea 4 Smart Healthcare Medical Device Research Center, Samsung Medical Center, Seoul 06351, Korea 7 Clinical Research Institute, Seoul National University Hospital, Seoul 03082, Korea |
| AuthorAffiliation_xml | – name: 1 Department of Neurosurgery, Seoul National University College of Medicine, Seoul 03082, Korea – name: 3 Department of Neurophysiology, Seoul National University College of Medicine, Seoul 03082, Korea – name: 7 Clinical Research Institute, Seoul National University Hospital, Seoul 03082, Korea – name: 2 Center for Cognition and Sociality, Institute for Basic Science, Daejeon 34126, Korea – name: 5 Department of Pathology, Seoul National University College of Medicine, Seoul 03082, Korea – name: 4 Smart Healthcare Medical Device Research Center, Samsung Medical Center, Seoul 06351, Korea – name: 6 Ischemic/Hypoxic Disease Institute, Cancer Research Institute, Seoul National University College of Medicine, Seoul 03082, Korea |
| Author_xml | – sequence: 1 givenname: Hye Young surname: Shin fullname: Shin, Hye Young organization: Department of Neurosurgery, Seoul National University College of Medicine, Seoul 03082, Korea – sequence: 2 givenname: Kyung-Seok surname: Han fullname: Han, Kyung-Seok organization: Center for Cognition and Sociality, Institute for Basic Science, Daejeon 34126, Korea – sequence: 3 givenname: Hyung Woo surname: Park fullname: Park, Hyung Woo organization: Department of Neurosurgery, Seoul National University College of Medicine, Seoul 03082, Korea – sequence: 4 givenname: Yun Hwa surname: Hong fullname: Hong, Yun Hwa organization: Department of Neurophysiology, Seoul National University College of Medicine, Seoul 03082, Korea – sequence: 5 givenname: Yona surname: Kim fullname: Kim, Yona organization: Department of Neurosurgery, Seoul National University College of Medicine, Seoul 03082, Korea – sequence: 6 givenname: Hyo Eun surname: Moon fullname: Moon, Hyo Eun organization: Department of Neurosurgery, Seoul National University College of Medicine, Seoul 03082, Korea – sequence: 7 givenname: Kwang Woo surname: Park fullname: Park, Kwang Woo organization: Department of Neurosurgery, Seoul National University College of Medicine, Seoul 03082, Korea – sequence: 8 givenname: Hye Ran surname: Park fullname: Park, Hye Ran organization: Department of Neurosurgery, Seoul National University College of Medicine, Seoul 03082, Korea – sequence: 9 givenname: C. Justin surname: Lee fullname: Lee, C. Justin organization: Center for Cognition and Sociality, Institute for Basic Science, Daejeon 34126, Korea – sequence: 10 givenname: Kiyoung surname: Lee fullname: Lee, Kiyoung organization: Department of Neurosurgery, Seoul National University College of Medicine, Seoul 03082, Korea – sequence: 11 givenname: Sang Jeong surname: Kim fullname: Kim, Sang Jeong organization: Department of Neurophysiology, Seoul National University College of Medicine, Seoul 03082, Korea – sequence: 12 givenname: Man Seung surname: Heo fullname: Heo, Man Seung organization: Smart Healthcare Medical Device Research Center, Samsung Medical Center, Seoul 06351, Korea – sequence: 13 givenname: Sung-Hye surname: Park fullname: Park, Sung-Hye organization: Department of Pathology, Seoul National University College of Medicine, Seoul 03082, Korea – sequence: 14 givenname: Dong Gyu surname: Kim fullname: Kim, Dong Gyu organization: Department of Neurosurgery, Seoul National University College of Medicine, Seoul 03082, Korea – sequence: 15 givenname: Sun Ha surname: Paek fullname: Paek, Sun Ha organization: Department of Neurosurgery, Seoul National University College of Medicine, Seoul 03082, Korea, Ischemic/Hypoxic Disease Institute, Cancer Research Institute, Seoul National University College of Medicine, Seoul 03082, Korea, Clinical Research Institute, Seoul National University Hospital, Seoul 03082, Korea |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/33972466$$D View this record in MEDLINE/PubMed https://www.kci.go.kr/kciportal/ci/sereArticleSearch/ciSereArtiView.kci?sereArticleSearchBean.artiId=ART002716152$$DAccess content in National Research Foundation of Korea (NRF) |
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| CitedBy_id | crossref_primary_10_3390_cancers15123154 crossref_primary_10_1038_s12276_024_01204_3 crossref_primary_10_1016_j_labinv_2023_100159 |
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| Keywords | Gene Set Enrichment Analysis Central neurocytoma Radial glia cells Transit-amplifying cells Neural stem cell Subventricular zone Tumor spheroids |
| Language | English |
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| Snippet | Central neurocytoma (CN) has been known as a benign neuronal tumor. In rare cases, CN undergoes malignant transformation to glioblastomas (GBM). Here we... |
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| Title | Tumor Spheroids of an Aggressive Form of Central Neurocytoma Have Transit-Amplifying Progenitor Characteristics with Enhanced EGFR and Tumor Stem Cell Signaling |
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