Neural G0: a quiescent‐like state found in neuroepithelial‐derived cells and glioma

Abstract Single‐cell RNA sequencing has emerged as a powerful tool for resolving cellular states associated with normal and maligned developmental processes. Here, we used scRNA‐seq to examine the cell cycle states of expanding human neural stem cells (hNSCs). From these data, we constructed a cell...

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Main Authors: Samantha A O’Connor, Heather M Feldman, Sonali Arora, Pia Hoellerbauer, Chad M Toledo, Philip Corrin, Lucas Carter, Megan Kufeld, Hamid Bolouri, Ryan Basom, Jeffrey Delrow, José L McFaline‐Figueroa, Cole Trapnell, Steven M Pollard, Anoop Patel, Patrick J Paddison, Christopher L Plaisier
Format: Article
Language:English
Published: Springer Nature 2021-06-01
Series:Molecular Systems Biology
Subjects:
Online Access:https://doi.org/10.15252/msb.20209522
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author Samantha A O’Connor
Heather M Feldman
Sonali Arora
Pia Hoellerbauer
Chad M Toledo
Philip Corrin
Lucas Carter
Megan Kufeld
Hamid Bolouri
Ryan Basom
Jeffrey Delrow
José L McFaline‐Figueroa
Cole Trapnell
Steven M Pollard
Anoop Patel
Patrick J Paddison
Christopher L Plaisier
author_facet Samantha A O’Connor
Heather M Feldman
Sonali Arora
Pia Hoellerbauer
Chad M Toledo
Philip Corrin
Lucas Carter
Megan Kufeld
Hamid Bolouri
Ryan Basom
Jeffrey Delrow
José L McFaline‐Figueroa
Cole Trapnell
Steven M Pollard
Anoop Patel
Patrick J Paddison
Christopher L Plaisier
author_sort Samantha A O’Connor
collection DOAJ
description Abstract Single‐cell RNA sequencing has emerged as a powerful tool for resolving cellular states associated with normal and maligned developmental processes. Here, we used scRNA‐seq to examine the cell cycle states of expanding human neural stem cells (hNSCs). From these data, we constructed a cell cycle classifier that identifies traditional cell cycle phases and a putative quiescent‐like state in neuroepithelial‐derived cell types during mammalian neurogenesis and in gliomas. The Neural G0 markers are enriched with quiescent NSC genes and other neurodevelopmental markers found in non‐dividing neural progenitors. Putative glioblastoma stem‐like cells were significantly enriched in the Neural G0 cell population. Neural G0 cell populations and gene expression are significantly associated with less aggressive tumors and extended patient survival for gliomas. Genetic screens to identify modulators of Neural G0 revealed that knockout of genes associated with the Hippo/Yap and p53 pathways diminished Neural G0 in vitro, resulting in faster G1 transit, down‐regulation of quiescence‐associated markers, and loss of Neural G0 gene expression. Thus, Neural G0 represents a dynamic quiescent‐like state found in neuroepithelial‐derived cells and gliomas.
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spelling doaj-art-58249d732dc642c29b1b9c5be97d78eb2025-08-20T03:42:04ZengSpringer NatureMolecular Systems Biology1744-42922021-06-0117612910.15252/msb.20209522Neural G0: a quiescent‐like state found in neuroepithelial‐derived cells and gliomaSamantha A O’Connor0Heather M Feldman1Sonali Arora2Pia Hoellerbauer3Chad M Toledo4Philip Corrin5Lucas Carter6Megan Kufeld7Hamid Bolouri8Ryan Basom9Jeffrey Delrow10José L McFaline‐Figueroa11Cole Trapnell12Steven M Pollard13Anoop Patel14Patrick J Paddison15Christopher L Plaisier16School of Biological and Health Systems Engineering, Arizona State UniversityHuman Biology Division, Fred Hutchinson Cancer Research CenterHuman Biology Division, Fred Hutchinson Cancer Research CenterHuman Biology Division, Fred Hutchinson Cancer Research CenterHuman Biology Division, Fred Hutchinson Cancer Research CenterHuman Biology Division, Fred Hutchinson Cancer Research CenterHuman Biology Division, Fred Hutchinson Cancer Research CenterHuman Biology Division, Fred Hutchinson Cancer Research CenterHuman Biology Division, Fred Hutchinson Cancer Research CenterGenomics and Bioinformatics Shared Resources, Fred Hutchinson Cancer Research CenterGenomics and Bioinformatics Shared Resources, Fred Hutchinson Cancer Research CenterDepartment of Genome Sciences, University of WashingtonDepartment of Genome Sciences, University of WashingtonEdinburgh CRUK Cancer Research Centre, MRC Centre for Regenerative Medicine, The University of EdinburghHuman Biology Division, Fred Hutchinson Cancer Research CenterHuman Biology Division, Fred Hutchinson Cancer Research CenterSchool of Biological and Health Systems Engineering, Arizona State UniversityAbstract Single‐cell RNA sequencing has emerged as a powerful tool for resolving cellular states associated with normal and maligned developmental processes. Here, we used scRNA‐seq to examine the cell cycle states of expanding human neural stem cells (hNSCs). From these data, we constructed a cell cycle classifier that identifies traditional cell cycle phases and a putative quiescent‐like state in neuroepithelial‐derived cell types during mammalian neurogenesis and in gliomas. The Neural G0 markers are enriched with quiescent NSC genes and other neurodevelopmental markers found in non‐dividing neural progenitors. Putative glioblastoma stem‐like cells were significantly enriched in the Neural G0 cell population. Neural G0 cell populations and gene expression are significantly associated with less aggressive tumors and extended patient survival for gliomas. Genetic screens to identify modulators of Neural G0 revealed that knockout of genes associated with the Hippo/Yap and p53 pathways diminished Neural G0 in vitro, resulting in faster G1 transit, down‐regulation of quiescence‐associated markers, and loss of Neural G0 gene expression. Thus, Neural G0 represents a dynamic quiescent‐like state found in neuroepithelial‐derived cells and gliomas.https://doi.org/10.15252/msb.20209522G0gliomaneural stem cellsquiescencescRNA‐seq
spellingShingle Samantha A O’Connor
Heather M Feldman
Sonali Arora
Pia Hoellerbauer
Chad M Toledo
Philip Corrin
Lucas Carter
Megan Kufeld
Hamid Bolouri
Ryan Basom
Jeffrey Delrow
José L McFaline‐Figueroa
Cole Trapnell
Steven M Pollard
Anoop Patel
Patrick J Paddison
Christopher L Plaisier
Neural G0: a quiescent‐like state found in neuroepithelial‐derived cells and glioma
Molecular Systems Biology
G0
glioma
neural stem cells
quiescence
scRNA‐seq
title Neural G0: a quiescent‐like state found in neuroepithelial‐derived cells and glioma
title_full Neural G0: a quiescent‐like state found in neuroepithelial‐derived cells and glioma
title_fullStr Neural G0: a quiescent‐like state found in neuroepithelial‐derived cells and glioma
title_full_unstemmed Neural G0: a quiescent‐like state found in neuroepithelial‐derived cells and glioma
title_short Neural G0: a quiescent‐like state found in neuroepithelial‐derived cells and glioma
title_sort neural g0 a quiescent like state found in neuroepithelial derived cells and glioma
topic G0
glioma
neural stem cells
quiescence
scRNA‐seq
url https://doi.org/10.15252/msb.20209522
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