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A novel hypoxia-driven gene signature that can predict the prognosis and drug resistance of gliomas

Hypoxia spontaneously forms in the interior of glioma tissues and regulates the expression of various genes. However, the status of hypoxia-driven genes in glioma tissues is not completely known. In the current study, RNA-seq data of 695 glioma tissues in The Cancer Genome Atlas (TCGA) were set as a...

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Autores principales: Ren, Peng, Wang, Jing-Ya, Zeng, Zhi-Rui, Li, Nan-Xi, Chen, Hong-Lei, Peng, Xin-Ge, Bhawal, Ujjal K., Guo, Wen-Zhi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9478203/
https://www.ncbi.nlm.nih.gov/pubmed/36118887
http://dx.doi.org/10.3389/fgene.2022.976356
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author Ren, Peng
Wang, Jing-Ya
Zeng, Zhi-Rui
Li, Nan-Xi
Chen, Hong-Lei
Peng, Xin-Ge
Bhawal, Ujjal K.
Guo, Wen-Zhi
author_facet Ren, Peng
Wang, Jing-Ya
Zeng, Zhi-Rui
Li, Nan-Xi
Chen, Hong-Lei
Peng, Xin-Ge
Bhawal, Ujjal K.
Guo, Wen-Zhi
author_sort Ren, Peng
collection PubMed
description Hypoxia spontaneously forms in the interior of glioma tissues and regulates the expression of various genes. However, the status of hypoxia-driven genes in glioma tissues is not completely known. In the current study, RNA-seq data of 695 glioma tissues in The Cancer Genome Atlas (TCGA) were set as a discovery cohort and were used to identify hypoxia-driven genes and construct a novel gene signature. The prognostic values of that signature were verified in data from the TCGA and the Chinese Glioma Genome Atlas (CGGA). The expression and diagnostic values of hypoxia-driven genes were analyzed using immunohistochemistry and receiver operator characteristic curves. Finally, the effects of hypoxia-driven genes on temozolomide (TMZ) resistance were analyzed by western blot, CCK-8 and colony formation assay. A total of 169 hypoxia-driven genes were identified, which were associated with a poor outcome in glioma patients. Among them, 22 genes had a degree score ≥10 and 6 genes (WT1, HOXA2, HOXC6, MMP9, SHOX2 and MYOD1) were selected to construct a signature to classify glioma patients into low- or high-risk groups. That signature had a remarkable prognostic value for glioma patients in TCGA and CGGA. The expression of HOXC6, MMP9, SHOX2 and MYOD1 was associated with hypoxia degree in glioma tissues and in recurrent cases, had a remarkable diagnostic value and a significant relationship with disease free survival in glioma patients. Moreover, SHOX2 was highly expressed in glioma tissues with O-6-methylguanine-DNA methyltransferase (MGMT)-unmethylation and temozolomide (TMZ) resistant glioma cell lines, and associated with MGMT expression. Knockdown the expression of SHOX2 significantly reduced the TMZ-resistance induced by hypoxia in glioma cells. Ultimately, we identified six novel hypoxia-driven genes for reliable prognostic prediction in gliomas and found that SHOX2 might be a potential target to overcome the TMZ resistance induced by hypoxia.
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spelling pubmed-94782032022-09-17 A novel hypoxia-driven gene signature that can predict the prognosis and drug resistance of gliomas Ren, Peng Wang, Jing-Ya Zeng, Zhi-Rui Li, Nan-Xi Chen, Hong-Lei Peng, Xin-Ge Bhawal, Ujjal K. Guo, Wen-Zhi Front Genet Genetics Hypoxia spontaneously forms in the interior of glioma tissues and regulates the expression of various genes. However, the status of hypoxia-driven genes in glioma tissues is not completely known. In the current study, RNA-seq data of 695 glioma tissues in The Cancer Genome Atlas (TCGA) were set as a discovery cohort and were used to identify hypoxia-driven genes and construct a novel gene signature. The prognostic values of that signature were verified in data from the TCGA and the Chinese Glioma Genome Atlas (CGGA). The expression and diagnostic values of hypoxia-driven genes were analyzed using immunohistochemistry and receiver operator characteristic curves. Finally, the effects of hypoxia-driven genes on temozolomide (TMZ) resistance were analyzed by western blot, CCK-8 and colony formation assay. A total of 169 hypoxia-driven genes were identified, which were associated with a poor outcome in glioma patients. Among them, 22 genes had a degree score ≥10 and 6 genes (WT1, HOXA2, HOXC6, MMP9, SHOX2 and MYOD1) were selected to construct a signature to classify glioma patients into low- or high-risk groups. That signature had a remarkable prognostic value for glioma patients in TCGA and CGGA. The expression of HOXC6, MMP9, SHOX2 and MYOD1 was associated with hypoxia degree in glioma tissues and in recurrent cases, had a remarkable diagnostic value and a significant relationship with disease free survival in glioma patients. Moreover, SHOX2 was highly expressed in glioma tissues with O-6-methylguanine-DNA methyltransferase (MGMT)-unmethylation and temozolomide (TMZ) resistant glioma cell lines, and associated with MGMT expression. Knockdown the expression of SHOX2 significantly reduced the TMZ-resistance induced by hypoxia in glioma cells. Ultimately, we identified six novel hypoxia-driven genes for reliable prognostic prediction in gliomas and found that SHOX2 might be a potential target to overcome the TMZ resistance induced by hypoxia. Frontiers Media S.A. 2022-09-02 /pmc/articles/PMC9478203/ /pubmed/36118887 http://dx.doi.org/10.3389/fgene.2022.976356 Text en Copyright © 2022 Ren, Wang, Zeng, Li, Chen, Peng, Bhawal and Guo. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Genetics
Ren, Peng
Wang, Jing-Ya
Zeng, Zhi-Rui
Li, Nan-Xi
Chen, Hong-Lei
Peng, Xin-Ge
Bhawal, Ujjal K.
Guo, Wen-Zhi
A novel hypoxia-driven gene signature that can predict the prognosis and drug resistance of gliomas
title A novel hypoxia-driven gene signature that can predict the prognosis and drug resistance of gliomas
title_full A novel hypoxia-driven gene signature that can predict the prognosis and drug resistance of gliomas
title_fullStr A novel hypoxia-driven gene signature that can predict the prognosis and drug resistance of gliomas
title_full_unstemmed A novel hypoxia-driven gene signature that can predict the prognosis and drug resistance of gliomas
title_short A novel hypoxia-driven gene signature that can predict the prognosis and drug resistance of gliomas
title_sort novel hypoxia-driven gene signature that can predict the prognosis and drug resistance of gliomas
topic Genetics
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9478203/
https://www.ncbi.nlm.nih.gov/pubmed/36118887
http://dx.doi.org/10.3389/fgene.2022.976356
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