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Gene signatures of quiescent glioblastoma cells reveal mesenchymal shift and interactions with niche microenvironment.

Abstract：

BACKGROUND:Glioblastoma (GBM), a highly malignant brain tumor, invariably recurs after therapy. Quiescent GBM cells represent a potential source of tumor recurrence, but little is known about their molecular underpinnings. METHODS:Patient-derived GBM cells were engineered by CRISPR/Cas9-assisted knock-in of an inducible histone2B-GFP (iH2B-GFP) reporter to track cell division history. We utilized an in vitro 3D GBM organoid approach to isolate live quiescent GBM (qGBM) cells and their proliferative counterparts (pGBM) to compare stem cell properties and therapy resistance. Gene expression programs of qGBM and pGBM cells were analyzed by RNA-Seq and NanoString platforms. FINDINGS:H2B-GFP-retaining qGBM cells exhibited comparable self-renewal capacity but higher therapy resistance relative to pGBM. Quiescent GBM cells expressed distinct gene programs that affect cell cycle control, metabolic adaptation, and extracellular matrix (ECM) interactions. Transcriptome analysis also revealed a mesenchymal shift in qGBM cells of both proneural and mesenchymal GBM subtypes. Bioinformatic analyses and functional assays in GBM organoids established hypoxia and TGFβ signaling as potential niche factors that promote quiescence in GBM. Finally, network co-expression analysis of TCGA glioma patient data identified gene modules that are enriched for qGBM signatures and also associated with survival rate. INTERPRETATION:Our in vitro study in 3D GBM organoids supports the presence of a quiescent cell population that displays self-renewal capacity, high therapy resistance, and mesenchymal gene signatures. It also sheds light on how GBM cells may acquire and maintain quiescence through ECM organization and interaction with niche factors such as TGFβ and hypoxia. Our findings provide a starting point for developing strategies to tackle the quiescent population of GBM. FUND: National Institutes of Health (NIH) and Deutsche Forschungsgemeinschaft (DFG).

journal_name

EBioMedicine

journal_title

EBioMedicine

authors

Tejero R,Huang Y,Katsyv I,Kluge M,Lin JY,Tome-Garcia J,Daviaud N,Wang Y,Zhang B,Tsankova NM,Friedel CC,Zou H,Friedel RH

doi

10.1016/j.ebiom.2019.03.064

subject

Has Abstract

pub_date

2019-04-01 00:00:00

pages

252-269

issn

2352-3964

pii

S2352-3964(19)30209-9

journal_volume

42

pub_type

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