M7G-Related lncRNAs predict prognosis and regulate the immune microenvironment in lung squamous cell carcinoma

Abstract Background N7-Methylguanosine (m7G) and long non-coding RNAs (lncRNAs) have been widely studied in cancer and have been found to be useful for assessing tumor progression. However, the role of m7G-related lncRNAs in lung squamous cell carcinoma (LUSC) remains unclear. Thus, it is crucial to...

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Main Authors: Junfan Pan, Zhidong Huang, Hancui Lin, Wenfang Cheng, Jinhuo Lai, Jiancheng Li
Format: Article
Language:English
Published: BMC 2022-11-01
Series:BMC Cancer
Subjects:
Online Access:https://doi.org/10.1186/s12885-022-10232-z
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author Junfan Pan
Zhidong Huang
Hancui Lin
Wenfang Cheng
Jinhuo Lai
Jiancheng Li
author_facet Junfan Pan
Zhidong Huang
Hancui Lin
Wenfang Cheng
Jinhuo Lai
Jiancheng Li
author_sort Junfan Pan
collection DOAJ
description Abstract Background N7-Methylguanosine (m7G) and long non-coding RNAs (lncRNAs) have been widely studied in cancer and have been found to be useful for assessing tumor progression. However, the role of m7G-related lncRNAs in lung squamous cell carcinoma (LUSC) remains unclear. Thus, it is crucial to identify m7G-associated lncRNAs with definitive prognostic value. This study aimed to investigate the prognostic value, correlation with tumor mutation burden, and impact on the tumor immune microenvironment of m7G-related lncRNAs in LUSC.  Methods LUSC transcriptome data and clinical data were downloaded from The Cancer Genome Atlas, and an m7G-related lncRNA-mRNA co-expression network was constructed using Pearson’s correlation analysis. Cox regression analyses were used to determine a risk model for m7G-associated lncRNAs with prognostic value. The risk signature was verified using the Kaplan–Meier method, receiver operating characteristic curve analysis, and principal component analysis. A nomogram based on risk scores and clinical characteristics was then developed. Gene set enrichment analysis was used for functional annotation to analyze the risk signature. The association among the risk signature, tumor mutational burden, and tumor-infiltrating immune cells was then analyzed. RT-qPCR was used to investigate the expression of 6 m7G-related lncRNAs in LUSC cells. The cytological function of SRP14-AS1 was verified by wound-healing assay and transwell assay. Results A total of 293 m7G-related lncRNAs were identifed, 27 candidate m7G-related lncRNAs were signifcantly associated with overall survival (OS). Six of these lncRNAs (CYP4F26P, LINC02178, MIR22HG, SRP14-AS1, TMEM99, PTCSC2) were selected for establishment of the risk model. The OS of patients in the low-risk group was higher than that of patients in the high-risk group (p < 0.001). Multivariate cox regression analysis indicated that the model could be an independent prognostic factor for LUSC (HR = 1.859; 95% CI 1.452–2.380, p < 0.001). The ROC curve analysis revealed that the AUCs for OS in the 3-, and 5-year were 0.682, 0.657, respectively. GSEA analysis revealed that the risk model was closely related to immune-related pathways. Compared with normal lung epithelial cells, four m7G-related lncRNAs were higher expressed in cancer cells and two were lower expressed, among which knockdown of SRP14-AS1 promoted the proliferation and migration of LUSC cells. Conclusion A risk model based on six m7G-related lncRNAs with prognostic value may be a promising prognostic tool in LUSC and guide individualized patient treatment.
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spelling doaj.art-7826554457b84ed38d4ae56035b22c442022-12-22T03:35:17ZengBMCBMC Cancer1471-24072022-11-0122111710.1186/s12885-022-10232-zM7G-Related lncRNAs predict prognosis and regulate the immune microenvironment in lung squamous cell carcinomaJunfan Pan0Zhidong Huang1Hancui Lin2Wenfang Cheng3Jinhuo Lai4Jiancheng Li5Clinical Oncology School of Fujian Medical University, Fujian Cancer HospitalThe Second Surgical Department of Breast Cancer, Tianjin Medical University Cancer Institute and HospitalClinical Oncology School of Fujian Medical University, Fujian Cancer HospitalClinical Oncology School of Fujian Medical University, Fujian Cancer HospitalDepartment of Medical Oncology, Fujian Medical University Union HospitalClinical Oncology School of Fujian Medical University, Fujian Cancer HospitalAbstract Background N7-Methylguanosine (m7G) and long non-coding RNAs (lncRNAs) have been widely studied in cancer and have been found to be useful for assessing tumor progression. However, the role of m7G-related lncRNAs in lung squamous cell carcinoma (LUSC) remains unclear. Thus, it is crucial to identify m7G-associated lncRNAs with definitive prognostic value. This study aimed to investigate the prognostic value, correlation with tumor mutation burden, and impact on the tumor immune microenvironment of m7G-related lncRNAs in LUSC.  Methods LUSC transcriptome data and clinical data were downloaded from The Cancer Genome Atlas, and an m7G-related lncRNA-mRNA co-expression network was constructed using Pearson’s correlation analysis. Cox regression analyses were used to determine a risk model for m7G-associated lncRNAs with prognostic value. The risk signature was verified using the Kaplan–Meier method, receiver operating characteristic curve analysis, and principal component analysis. A nomogram based on risk scores and clinical characteristics was then developed. Gene set enrichment analysis was used for functional annotation to analyze the risk signature. The association among the risk signature, tumor mutational burden, and tumor-infiltrating immune cells was then analyzed. RT-qPCR was used to investigate the expression of 6 m7G-related lncRNAs in LUSC cells. The cytological function of SRP14-AS1 was verified by wound-healing assay and transwell assay. Results A total of 293 m7G-related lncRNAs were identifed, 27 candidate m7G-related lncRNAs were signifcantly associated with overall survival (OS). Six of these lncRNAs (CYP4F26P, LINC02178, MIR22HG, SRP14-AS1, TMEM99, PTCSC2) were selected for establishment of the risk model. The OS of patients in the low-risk group was higher than that of patients in the high-risk group (p < 0.001). Multivariate cox regression analysis indicated that the model could be an independent prognostic factor for LUSC (HR = 1.859; 95% CI 1.452–2.380, p < 0.001). The ROC curve analysis revealed that the AUCs for OS in the 3-, and 5-year were 0.682, 0.657, respectively. GSEA analysis revealed that the risk model was closely related to immune-related pathways. Compared with normal lung epithelial cells, four m7G-related lncRNAs were higher expressed in cancer cells and two were lower expressed, among which knockdown of SRP14-AS1 promoted the proliferation and migration of LUSC cells. Conclusion A risk model based on six m7G-related lncRNAs with prognostic value may be a promising prognostic tool in LUSC and guide individualized patient treatment.https://doi.org/10.1186/s12885-022-10232-zLung squamous cell carcinomaPrognosism7GlncRNATumor immuneMicroenvironment
spellingShingle Junfan Pan
Zhidong Huang
Hancui Lin
Wenfang Cheng
Jinhuo Lai
Jiancheng Li
M7G-Related lncRNAs predict prognosis and regulate the immune microenvironment in lung squamous cell carcinoma
BMC Cancer
Lung squamous cell carcinoma
Prognosis
m7G
lncRNA
Tumor immune
Microenvironment
title M7G-Related lncRNAs predict prognosis and regulate the immune microenvironment in lung squamous cell carcinoma
title_full M7G-Related lncRNAs predict prognosis and regulate the immune microenvironment in lung squamous cell carcinoma
title_fullStr M7G-Related lncRNAs predict prognosis and regulate the immune microenvironment in lung squamous cell carcinoma
title_full_unstemmed M7G-Related lncRNAs predict prognosis and regulate the immune microenvironment in lung squamous cell carcinoma
title_short M7G-Related lncRNAs predict prognosis and regulate the immune microenvironment in lung squamous cell carcinoma
title_sort m7g related lncrnas predict prognosis and regulate the immune microenvironment in lung squamous cell carcinoma
topic Lung squamous cell carcinoma
Prognosis
m7G
lncRNA
Tumor immune
Microenvironment
url https://doi.org/10.1186/s12885-022-10232-z
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