Single‐cell transcriptomic analysis of glioblastoma reveals pericytes contributing to the blood–brain–tumor barrier and tumor progression

Abstract The blood–brain barrier is often altered in glioblastoma (GBM) creating a blood–brain–tumor barrier (BBTB) composed of pericytes. The BBTB affects chemotherapy efficacy. However, the expression signatures of BBTB‐associated pericytes remain unclear. We aimed to identify BBTB‐associated peri...

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Main Authors: Yuzhe Li, Changwu Wu, Xinmiao Long, Xiangyu Wang, Wei Gao, Kun Deng, Bo Xie, Sen Zhang, Minghua Wu, Qing Liu
Format: Article
Language:English
Published: Wiley 2024-12-01
Series:MedComm
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Online Access:https://doi.org/10.1002/mco2.70014
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author Yuzhe Li
Changwu Wu
Xinmiao Long
Xiangyu Wang
Wei Gao
Kun Deng
Bo Xie
Sen Zhang
Minghua Wu
Qing Liu
author_facet Yuzhe Li
Changwu Wu
Xinmiao Long
Xiangyu Wang
Wei Gao
Kun Deng
Bo Xie
Sen Zhang
Minghua Wu
Qing Liu
author_sort Yuzhe Li
collection DOAJ
description Abstract The blood–brain barrier is often altered in glioblastoma (GBM) creating a blood–brain–tumor barrier (BBTB) composed of pericytes. The BBTB affects chemotherapy efficacy. However, the expression signatures of BBTB‐associated pericytes remain unclear. We aimed to identify BBTB‐associated pericytes in single‐cell RNA sequencing data of GBM using pericyte markers, a normal brain pericyte expression signature, and functional enrichment. We identified parathyroid hormone receptor‐1 (PTH1R) as a potential marker of pericytes associated with BBTB function. These pericytes interact with other cells in GBM mainly through extracellular matrix–integrin signaling pathways. Compared with normal pericytes, pericytes in GBM exhibited upregulation of several ECM genes (including collagen IV and FN1), and high expression levels of these genes were associated with a poor prognosis. Cell line experiments showed that PTH1R knockdown in pericytes increased collagen IV and FN1 expression levels. In mice models, the expression levels of PTH1R, collagen IV, and FN1 were consistent with these trends. Evans Blue leakage and IgG detection in the brain tissue suggested a negative correlation between PTH1R expression levels and blood–brain barrier function. Further, a risk model based on differentially expressed genes in PTH1R+ pericytes had predictive value for GBM, as validated using independent and in‐house cohorts.
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spelling doaj-art-60297dc566c34fb2a1d4ab89ef2667bc2025-08-20T01:58:11ZengWileyMedComm2688-26632024-12-01512n/an/a10.1002/mco2.70014Single‐cell transcriptomic analysis of glioblastoma reveals pericytes contributing to the blood–brain–tumor barrier and tumor progressionYuzhe Li0Changwu Wu1Xinmiao Long2Xiangyu Wang3Wei Gao4Kun Deng5Bo Xie6Sen Zhang7Minghua Wu8Qing Liu9Department of Neurosurgery Xiangya Hospital Central South University Changsha Hunan ChinaDepartment of Neurosurgery Xiangya Hospital Central South University Changsha Hunan ChinaCancer Research Institute Central South University Changsha Hunan ChinaDepartment of Neurosurgery Xiangya Hospital Central South University Changsha Hunan ChinaCancer Research Institute Central South University Changsha Hunan ChinaCancer Research Institute Central South University Changsha Hunan ChinaDepartment of Neurosurgery Xiangya Hospital Central South University Changsha Hunan ChinaDepartment of Neurosurgery Xiangya Hospital Central South University Changsha Hunan ChinaDepartment of Neurosurgery Xiangya Hospital Central South University Changsha Hunan ChinaDepartment of Neurosurgery Xiangya Hospital Central South University Changsha Hunan ChinaAbstract The blood–brain barrier is often altered in glioblastoma (GBM) creating a blood–brain–tumor barrier (BBTB) composed of pericytes. The BBTB affects chemotherapy efficacy. However, the expression signatures of BBTB‐associated pericytes remain unclear. We aimed to identify BBTB‐associated pericytes in single‐cell RNA sequencing data of GBM using pericyte markers, a normal brain pericyte expression signature, and functional enrichment. We identified parathyroid hormone receptor‐1 (PTH1R) as a potential marker of pericytes associated with BBTB function. These pericytes interact with other cells in GBM mainly through extracellular matrix–integrin signaling pathways. Compared with normal pericytes, pericytes in GBM exhibited upregulation of several ECM genes (including collagen IV and FN1), and high expression levels of these genes were associated with a poor prognosis. Cell line experiments showed that PTH1R knockdown in pericytes increased collagen IV and FN1 expression levels. In mice models, the expression levels of PTH1R, collagen IV, and FN1 were consistent with these trends. Evans Blue leakage and IgG detection in the brain tissue suggested a negative correlation between PTH1R expression levels and blood–brain barrier function. Further, a risk model based on differentially expressed genes in PTH1R+ pericytes had predictive value for GBM, as validated using independent and in‐house cohorts.https://doi.org/10.1002/mco2.70014blood–brain–tumor barrierglioblastomapericyteprognosis
spellingShingle Yuzhe Li
Changwu Wu
Xinmiao Long
Xiangyu Wang
Wei Gao
Kun Deng
Bo Xie
Sen Zhang
Minghua Wu
Qing Liu
Single‐cell transcriptomic analysis of glioblastoma reveals pericytes contributing to the blood–brain–tumor barrier and tumor progression
MedComm
blood–brain–tumor barrier
glioblastoma
pericyte
prognosis
title Single‐cell transcriptomic analysis of glioblastoma reveals pericytes contributing to the blood–brain–tumor barrier and tumor progression
title_full Single‐cell transcriptomic analysis of glioblastoma reveals pericytes contributing to the blood–brain–tumor barrier and tumor progression
title_fullStr Single‐cell transcriptomic analysis of glioblastoma reveals pericytes contributing to the blood–brain–tumor barrier and tumor progression
title_full_unstemmed Single‐cell transcriptomic analysis of glioblastoma reveals pericytes contributing to the blood–brain–tumor barrier and tumor progression
title_short Single‐cell transcriptomic analysis of glioblastoma reveals pericytes contributing to the blood–brain–tumor barrier and tumor progression
title_sort single cell transcriptomic analysis of glioblastoma reveals pericytes contributing to the blood brain tumor barrier and tumor progression
topic blood–brain–tumor barrier
glioblastoma
pericyte
prognosis
url https://doi.org/10.1002/mco2.70014
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