NCAPG Promotes Tumor Progression and Modulates Immune Cell Infiltration in Glioma

Glioma is one of the most deadly types of brain cancer. As it is highly invasive, the prognosis for glioma patients remains dismal, with median survival rarely exceeding 16 months. Thus, developing a new prognostic biomarker for glioma and investigating its molecular mechanisms is necessary for the...

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Main Authors: Guangrong Zheng, Tao Han, Xiaomu Hu, Zhou Yang, Jin Wang, Zhenyi Wen, Hengyu Li, Hongjin Wang
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-03-01
Series:Frontiers in Oncology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fonc.2022.770628/full
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author Guangrong Zheng
Guangrong Zheng
Tao Han
Xiaomu Hu
Zhou Yang
Jin Wang
Zhenyi Wen
Hengyu Li
Hongjin Wang
author_facet Guangrong Zheng
Guangrong Zheng
Tao Han
Xiaomu Hu
Zhou Yang
Jin Wang
Zhenyi Wen
Hengyu Li
Hongjin Wang
author_sort Guangrong Zheng
collection DOAJ
description Glioma is one of the most deadly types of brain cancer. As it is highly invasive, the prognosis for glioma patients remains dismal, with median survival rarely exceeding 16 months. Thus, developing a new prognostic biomarker for glioma and investigating its molecular mechanisms is necessary for the development of an efficient treatment strategy. In this study, we analyzed a cohort of 1,131 glioma patients using RNA-seq data from The Cancer Genome Atlas (TCGA project) and Gene Expression Omnibus (GSE4290 and GSE16011 datasets), and validated the results using the RNA-seq data of 1,018 gliomas from the Chinese Glioma Genome Atlas (CGGA project). We used the R language as the main tool for statistical analysis and data visualization. We found that NCAPG, a mitosis-associated chromosomal condensing protein, is highly expressed in glioma tissues. Furthermore, the expression of NCAPG increased significantly with the increase in tumor grade, and high NCAPG expression was found to be a predictor of poor overall survival in glioma patients (P < 0.001). This result shows that NCAPG expression could be an independent prognostic factor. Importantly, when the expression of NCAPG was knocked down, the CCK-8 assay revealed that the proliferation of glioma cells (LN-229 and T98G cell lines) decreased significantly compared with the control group. In addition, the healing rates of these cells were significantly lower in the si-NCAPG group than in the control group (P < 0.001). We then used the CIBERSORT algorithm to analyze the expression levels of 22 subpopulations of immune cells and found that NCAPG was significantly negatively correlated with natural killer cell activation. In addition, it was positively correlated with MHC-I molecules and ADAM17. Our study is first in comprehensively describing the high expression of NCAPG in glioma. It also shows that NCAPG can function as an independent prognostic predictor of glioma, and that targeting NCAPG can be a new strategy for the treatment of glioma patients.
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spelling doaj.art-9fe55533c45e474fb6e82c345e0424232022-12-21T23:18:15ZengFrontiers Media S.A.Frontiers in Oncology2234-943X2022-03-011210.3389/fonc.2022.770628770628NCAPG Promotes Tumor Progression and Modulates Immune Cell Infiltration in GliomaGuangrong Zheng0Guangrong Zheng1Tao Han2Xiaomu Hu3Zhou Yang4Jin Wang5Zhenyi Wen6Hengyu Li7Hongjin Wang8Department of Neurology, The Second Hospital of Dalian Medical University, Dalian, ChinaDepartment of Radiology, Changhai Hospital, Navy Medical University, Shanghai, ChinaDepartment of Oncology, The First Affiliated Hospital of China Medical University, Shenyang, ChinaDepartment of Pathology, Huashan Hospital, FuDan University, Shanghai, ChinaDepartment of General Surgery, The Second Hospital of Dalian Medical University, Dalian, ChinaDepartment of Pathology, Changhai Hospital, Navy Medical University, Shanghai, ChinaDepartment of Neurology, The Second Hospital of Dalian Medical University, Dalian, ChinaDepartment of Breast and Thyroid Surgery, Changhai Hospital, Navy Medical University, Shanghai, ChinaDepartment of Neurology, The Second Hospital of Dalian Medical University, Dalian, ChinaGlioma is one of the most deadly types of brain cancer. As it is highly invasive, the prognosis for glioma patients remains dismal, with median survival rarely exceeding 16 months. Thus, developing a new prognostic biomarker for glioma and investigating its molecular mechanisms is necessary for the development of an efficient treatment strategy. In this study, we analyzed a cohort of 1,131 glioma patients using RNA-seq data from The Cancer Genome Atlas (TCGA project) and Gene Expression Omnibus (GSE4290 and GSE16011 datasets), and validated the results using the RNA-seq data of 1,018 gliomas from the Chinese Glioma Genome Atlas (CGGA project). We used the R language as the main tool for statistical analysis and data visualization. We found that NCAPG, a mitosis-associated chromosomal condensing protein, is highly expressed in glioma tissues. Furthermore, the expression of NCAPG increased significantly with the increase in tumor grade, and high NCAPG expression was found to be a predictor of poor overall survival in glioma patients (P < 0.001). This result shows that NCAPG expression could be an independent prognostic factor. Importantly, when the expression of NCAPG was knocked down, the CCK-8 assay revealed that the proliferation of glioma cells (LN-229 and T98G cell lines) decreased significantly compared with the control group. In addition, the healing rates of these cells were significantly lower in the si-NCAPG group than in the control group (P < 0.001). We then used the CIBERSORT algorithm to analyze the expression levels of 22 subpopulations of immune cells and found that NCAPG was significantly negatively correlated with natural killer cell activation. In addition, it was positively correlated with MHC-I molecules and ADAM17. Our study is first in comprehensively describing the high expression of NCAPG in glioma. It also shows that NCAPG can function as an independent prognostic predictor of glioma, and that targeting NCAPG can be a new strategy for the treatment of glioma patients.https://www.frontiersin.org/articles/10.3389/fonc.2022.770628/fullNCAPGgliomaimmune infiltratesNK cellsimmunohistochemistry
spellingShingle Guangrong Zheng
Guangrong Zheng
Tao Han
Xiaomu Hu
Zhou Yang
Jin Wang
Zhenyi Wen
Hengyu Li
Hongjin Wang
NCAPG Promotes Tumor Progression and Modulates Immune Cell Infiltration in Glioma
Frontiers in Oncology
NCAPG
glioma
immune infiltrates
NK cells
immunohistochemistry
title NCAPG Promotes Tumor Progression and Modulates Immune Cell Infiltration in Glioma
title_full NCAPG Promotes Tumor Progression and Modulates Immune Cell Infiltration in Glioma
title_fullStr NCAPG Promotes Tumor Progression and Modulates Immune Cell Infiltration in Glioma
title_full_unstemmed NCAPG Promotes Tumor Progression and Modulates Immune Cell Infiltration in Glioma
title_short NCAPG Promotes Tumor Progression and Modulates Immune Cell Infiltration in Glioma
title_sort ncapg promotes tumor progression and modulates immune cell infiltration in glioma
topic NCAPG
glioma
immune infiltrates
NK cells
immunohistochemistry
url https://www.frontiersin.org/articles/10.3389/fonc.2022.770628/full
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