Immune alterations and overexpression of CTCF in endometrial carcinoma: insights from molecular subtyping

Abstract Background Endometrial cancer (EC) is a prevalent epithelial malignancy originating in the female endometrium, and its global incidence has been on the rise over the past decade. Despite significant scientific progress has been achieved recently, the genetic factors underlying EC pathogenes...

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Main Authors: Caiping Wei, Guowei Chen, Kun Chen, Shuang Fang, Hongying He
Format: Article
Language:English
Published: BMC 2024-12-01
Series:Cancer Cell International
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Online Access:https://doi.org/10.1186/s12935-024-03576-y
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author Caiping Wei
Guowei Chen
Kun Chen
Shuang Fang
Hongying He
author_facet Caiping Wei
Guowei Chen
Kun Chen
Shuang Fang
Hongying He
author_sort Caiping Wei
collection DOAJ
description Abstract Background Endometrial cancer (EC) is a prevalent epithelial malignancy originating in the female endometrium, and its global incidence has been on the rise over the past decade. Despite significant scientific progress has been achieved recently, the genetic factors underlying EC pathogenesis remain poorly understood, warranting further investigation. Methods We employed transcriptomic datasets from the Genomic Data Commons database to extract variable and clinical data. Quantile normalization and log2 transformations were applied to obtain a gene expression matrix for the sample cohort. Various assays, such as quantitative real-time polymerase chain reaction (qRT-PCR), western blotting, immunohistochemistry (IHC), wound healing assay, transwell assay, and TUNEL assay, were employed in the study to examine the involvement of CTCF in EC cell biology. Additionally, in vivo experiments were conducted using a subcutaneous transplantation tumor model in athymic nude mice. The potential mechanism of action of CTCF was also illustrated by identifying differentially expressed genes (DEGs) and functions after interfering with CTCF gene expression through the GSPAdb online database. Results After categorizing 543 samples into cohorts with high and low ImmuneScores, we discovered 1025 genes that were differentially expressed, including 745 genes that were up-regulated and 280 genes that were down-regulated in the high scores group compared to the low scores group. Tumor mutation burden (TMB) analysis highlighted 11 genes with the highest mutation frequency. Furthermore, 16 immune checkpoints and 50 immune regulatory factors exhibited differential expression. Among these, CTCF was up-regulated in EC. We found that CTCF knockdown could diminish EC's invasive ability and metastatic potential while enhancing apoptosis. In vivo experiments corroborated that CTCF knockdown could reduce tumor growth. The GSPAdb online database identified differential expression pathways mainly enriched in cellular metabolism as well as some intracellular classical signaling pathways after interfering with CTCF gene expression. In addition, we identified potential downstream regulators of CTCF through protein interaction networks. Conclusion This study unveiled comprehensive molecular characteristics and DEGs in EC, emphasizing the up-regulation of CTCF in EC. Our findings collectively suggest that CTCF represents a promising therapeutic target, and our gene molecular typing model offers a novel approach for prognostic evaluation in EC.
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spelling doaj-art-f4b0955aab0149bc8f57a03d4e7aa8042024-12-08T12:46:34ZengBMCCancer Cell International1475-28672024-12-0124111410.1186/s12935-024-03576-yImmune alterations and overexpression of CTCF in endometrial carcinoma: insights from molecular subtypingCaiping Wei0Guowei Chen1Kun Chen2Shuang Fang3Hongying He4Department of Gynecology, Liuzhou Municipal Liutie Central HospitalDepartment of Gynecology, Liuzhou Worker’s HospitalDepartment of Gynecology, Liuzhou Municipal Liutie Central HospitalDepartment of Gynecology, Liuzhou Worker’s HospitalDepartment of Gynecology, Liuzhou Municipal Liutie Central HospitalAbstract Background Endometrial cancer (EC) is a prevalent epithelial malignancy originating in the female endometrium, and its global incidence has been on the rise over the past decade. Despite significant scientific progress has been achieved recently, the genetic factors underlying EC pathogenesis remain poorly understood, warranting further investigation. Methods We employed transcriptomic datasets from the Genomic Data Commons database to extract variable and clinical data. Quantile normalization and log2 transformations were applied to obtain a gene expression matrix for the sample cohort. Various assays, such as quantitative real-time polymerase chain reaction (qRT-PCR), western blotting, immunohistochemistry (IHC), wound healing assay, transwell assay, and TUNEL assay, were employed in the study to examine the involvement of CTCF in EC cell biology. Additionally, in vivo experiments were conducted using a subcutaneous transplantation tumor model in athymic nude mice. The potential mechanism of action of CTCF was also illustrated by identifying differentially expressed genes (DEGs) and functions after interfering with CTCF gene expression through the GSPAdb online database. Results After categorizing 543 samples into cohorts with high and low ImmuneScores, we discovered 1025 genes that were differentially expressed, including 745 genes that were up-regulated and 280 genes that were down-regulated in the high scores group compared to the low scores group. Tumor mutation burden (TMB) analysis highlighted 11 genes with the highest mutation frequency. Furthermore, 16 immune checkpoints and 50 immune regulatory factors exhibited differential expression. Among these, CTCF was up-regulated in EC. We found that CTCF knockdown could diminish EC's invasive ability and metastatic potential while enhancing apoptosis. In vivo experiments corroborated that CTCF knockdown could reduce tumor growth. The GSPAdb online database identified differential expression pathways mainly enriched in cellular metabolism as well as some intracellular classical signaling pathways after interfering with CTCF gene expression. In addition, we identified potential downstream regulators of CTCF through protein interaction networks. Conclusion This study unveiled comprehensive molecular characteristics and DEGs in EC, emphasizing the up-regulation of CTCF in EC. Our findings collectively suggest that CTCF represents a promising therapeutic target, and our gene molecular typing model offers a novel approach for prognostic evaluation in EC.https://doi.org/10.1186/s12935-024-03576-yEndometrial cancerMolecular subtypingDEGsCTCF
spellingShingle Caiping Wei
Guowei Chen
Kun Chen
Shuang Fang
Hongying He
Immune alterations and overexpression of CTCF in endometrial carcinoma: insights from molecular subtyping
Cancer Cell International
Endometrial cancer
Molecular subtyping
DEGs
CTCF
title Immune alterations and overexpression of CTCF in endometrial carcinoma: insights from molecular subtyping
title_full Immune alterations and overexpression of CTCF in endometrial carcinoma: insights from molecular subtyping
title_fullStr Immune alterations and overexpression of CTCF in endometrial carcinoma: insights from molecular subtyping
title_full_unstemmed Immune alterations and overexpression of CTCF in endometrial carcinoma: insights from molecular subtyping
title_short Immune alterations and overexpression of CTCF in endometrial carcinoma: insights from molecular subtyping
title_sort immune alterations and overexpression of ctcf in endometrial carcinoma insights from molecular subtyping
topic Endometrial cancer
Molecular subtyping
DEGs
CTCF
url https://doi.org/10.1186/s12935-024-03576-y
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AT guoweichen immunealterationsandoverexpressionofctcfinendometrialcarcinomainsightsfrommolecularsubtyping
AT kunchen immunealterationsandoverexpressionofctcfinendometrialcarcinomainsightsfrommolecularsubtyping
AT shuangfang immunealterationsandoverexpressionofctcfinendometrialcarcinomainsightsfrommolecularsubtyping
AT hongyinghe immunealterationsandoverexpressionofctcfinendometrialcarcinomainsightsfrommolecularsubtyping