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Tetraspanins predict the prognosis and characterize the tumor immune microenvironment of glioblastoma

Glioblastoma (GBM) is the most aggressive and lethal primary brain tumor. Conventional treatments have not achieved breakthroughs in improving survival. Therefore, novel molecular targets and biomarkers need to be identified. As signal transduction docks on the cell membrane, tetraspanins (TSPANs) a...

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Autores principales: Li, Yu-Chao, Wu, Yue, Chen, Gang, Zhu, Li-Zhi, Luo, Xiu, Nie, Qian-Qian, Zhang, Lu, Zuo, Chang-Jing
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10432458/
https://www.ncbi.nlm.nih.gov/pubmed/37587203
http://dx.doi.org/10.1038/s41598-023-40425-w
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author Li, Yu-Chao
Wu, Yue
Chen, Gang
Zhu, Li-Zhi
Luo, Xiu
Nie, Qian-Qian
Zhang, Lu
Zuo, Chang-Jing
author_facet Li, Yu-Chao
Wu, Yue
Chen, Gang
Zhu, Li-Zhi
Luo, Xiu
Nie, Qian-Qian
Zhang, Lu
Zuo, Chang-Jing
author_sort Li, Yu-Chao
collection PubMed
description Glioblastoma (GBM) is the most aggressive and lethal primary brain tumor. Conventional treatments have not achieved breakthroughs in improving survival. Therefore, novel molecular targets and biomarkers need to be identified. As signal transduction docks on the cell membrane, tetraspanins (TSPANs) are associated with various tumors; however, research on their role in GBM remains extremely scarce. Gene expression and clinicopathological characteristic data were obtained from GEPIA, CGGA, HPA, cBioPortal, and GSCA databases to analyze the mRNA and protein expression levels, prognostic value, clinical relevance, mutation status, and targeted drug sensitivity of TSPANs in GBM. Gene set enrichment analysis (GSEA), Gene Ontology (GO), and the Kyoto Encyclopedia of Genes and Genomes (KEGG) analysis were used for biological process enrichment. Data from TCGA and TCIA were used to construct the tumor immune microenvironment landscape of TSPANs. Different R software algorithms were used to analyze the immune score, immune cell infiltration, and immune checkpoint correlation. Univariate and multivariate analyses were performed for TSPAN4, which had the most significant predictive prognostic value, and a nomogram model was constructed to predict individual outcomes. The expression and function of TSPAN4 were verified in vitro. TSPAN3/4/6/11/12/18/23/24/25/26/27/28/29/30/31expressions were significantly upregulated in GBM, and TSPAN3/4/6/11/18/24/25/26/29/30 were strongly correlated with prognosis. The expression of multiple TSPANs significantly correlated with 1p/19q co-deletion status, IDH mutation status, recurrence, age, and tumor grade. GSEA and GO analyses revealed the potential contribution of TSPANs in cell adhesion and migration. Immune correlation analysis revealed that TSPANs are related to the formation of the GBM tumor microenvironment (TME) and may influence immunotherapy outcomes. TSPAN4 is an independent prognostic factor and TSPAN4 knockdown has been demonstrated to strongly inhibit glioma cell proliferation, invasion, and migration in vitro. We comprehensively elaborated the prognostic value and potential role of differentially expressed TSPANs in GBM, including molecules that scientists have previously overlooked. This study provides a novel and comprehensive perspective on the pathological mechanisms of GBM and the future direction of individualized tumor immunotherapy, which may be a critical link between GBM malignant progression and TME remodeling.
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spelling pubmed-104324582023-08-18 Tetraspanins predict the prognosis and characterize the tumor immune microenvironment of glioblastoma Li, Yu-Chao Wu, Yue Chen, Gang Zhu, Li-Zhi Luo, Xiu Nie, Qian-Qian Zhang, Lu Zuo, Chang-Jing Sci Rep Article Glioblastoma (GBM) is the most aggressive and lethal primary brain tumor. Conventional treatments have not achieved breakthroughs in improving survival. Therefore, novel molecular targets and biomarkers need to be identified. As signal transduction docks on the cell membrane, tetraspanins (TSPANs) are associated with various tumors; however, research on their role in GBM remains extremely scarce. Gene expression and clinicopathological characteristic data were obtained from GEPIA, CGGA, HPA, cBioPortal, and GSCA databases to analyze the mRNA and protein expression levels, prognostic value, clinical relevance, mutation status, and targeted drug sensitivity of TSPANs in GBM. Gene set enrichment analysis (GSEA), Gene Ontology (GO), and the Kyoto Encyclopedia of Genes and Genomes (KEGG) analysis were used for biological process enrichment. Data from TCGA and TCIA were used to construct the tumor immune microenvironment landscape of TSPANs. Different R software algorithms were used to analyze the immune score, immune cell infiltration, and immune checkpoint correlation. Univariate and multivariate analyses were performed for TSPAN4, which had the most significant predictive prognostic value, and a nomogram model was constructed to predict individual outcomes. The expression and function of TSPAN4 were verified in vitro. TSPAN3/4/6/11/12/18/23/24/25/26/27/28/29/30/31expressions were significantly upregulated in GBM, and TSPAN3/4/6/11/18/24/25/26/29/30 were strongly correlated with prognosis. The expression of multiple TSPANs significantly correlated with 1p/19q co-deletion status, IDH mutation status, recurrence, age, and tumor grade. GSEA and GO analyses revealed the potential contribution of TSPANs in cell adhesion and migration. Immune correlation analysis revealed that TSPANs are related to the formation of the GBM tumor microenvironment (TME) and may influence immunotherapy outcomes. TSPAN4 is an independent prognostic factor and TSPAN4 knockdown has been demonstrated to strongly inhibit glioma cell proliferation, invasion, and migration in vitro. We comprehensively elaborated the prognostic value and potential role of differentially expressed TSPANs in GBM, including molecules that scientists have previously overlooked. This study provides a novel and comprehensive perspective on the pathological mechanisms of GBM and the future direction of individualized tumor immunotherapy, which may be a critical link between GBM malignant progression and TME remodeling. Nature Publishing Group UK 2023-08-16 /pmc/articles/PMC10432458/ /pubmed/37587203 http://dx.doi.org/10.1038/s41598-023-40425-w Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Li, Yu-Chao
Wu, Yue
Chen, Gang
Zhu, Li-Zhi
Luo, Xiu
Nie, Qian-Qian
Zhang, Lu
Zuo, Chang-Jing
Tetraspanins predict the prognosis and characterize the tumor immune microenvironment of glioblastoma
title Tetraspanins predict the prognosis and characterize the tumor immune microenvironment of glioblastoma
title_full Tetraspanins predict the prognosis and characterize the tumor immune microenvironment of glioblastoma
title_fullStr Tetraspanins predict the prognosis and characterize the tumor immune microenvironment of glioblastoma
title_full_unstemmed Tetraspanins predict the prognosis and characterize the tumor immune microenvironment of glioblastoma
title_short Tetraspanins predict the prognosis and characterize the tumor immune microenvironment of glioblastoma
title_sort tetraspanins predict the prognosis and characterize the tumor immune microenvironment of glioblastoma
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10432458/
https://www.ncbi.nlm.nih.gov/pubmed/37587203
http://dx.doi.org/10.1038/s41598-023-40425-w
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