Radioresistance-related gene signatures identified by transcriptomics characterize the prognosis and immune landscape of pancreatic cancer patients

Abstract Background Radiotherapy (RT) is an important means of local treatment of solid tumors, and radioresistance is the main reason for RT failure for tumors, especially pancreatic cancer (PC). It is urgent to distinguish key genes and mechanisms of radioresistance in PC. Methods We acquired the...

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Main Authors: Dandan Wang, Jun Cao, Yanhui Chen, Lisha Zhang, Chan Zhou, Litao Huang, Yanliang Chen
Format: Article
Language:English
Published: BMC 2024-12-01
Series:BMC Cancer
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Online Access:https://doi.org/10.1186/s12885-024-13231-4
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author Dandan Wang
Jun Cao
Yanhui Chen
Lisha Zhang
Chan Zhou
Litao Huang
Yanliang Chen
author_facet Dandan Wang
Jun Cao
Yanhui Chen
Lisha Zhang
Chan Zhou
Litao Huang
Yanliang Chen
author_sort Dandan Wang
collection DOAJ
description Abstract Background Radiotherapy (RT) is an important means of local treatment of solid tumors, and radioresistance is the main reason for RT failure for tumors, especially pancreatic cancer (PC). It is urgent to distinguish key genes and mechanisms of radioresistance in PC. Methods We acquired the data from The Cancer Genome Atlas (TCGA), obtained the gene modules associated with radioresistance by weighted gene coexpression network analysis (WGCNA), and identified differentially expressed genes (DEGs) between normal and tumor samples. Radioresistance-related genes (RRRGs) were determined with the intersection of WGCNA and DEGs. The hub RRRGs associated with prognosis were distinguished by the least absolute shrinkage and selection operator (LASSO) regression. We established a risk score model using multivariate Cox regression. Immune cell infiltration and drug sensitivity were evaluated through the CIBERSORT algorithm and the “OncoPredict” software package, respectively. The association of the key gene RIC3 and PC clinical features was verified in public databases, and its biological behaviors were explored in vitro. Results The intersection of DEGs and WGCNA confirmed 14 RRRGs, then six hub RRRGs were identified using LASSO. A key four genes (DUSP4, ADORA2B, SCGB2A1, and RIC3) risk score model was constructed and proved to be capable of independently estimating the prognosis of PC. There is no significant difference between risk score groups in various immune cell infiltration and response to immunotherapy. Although the low-risk group seemed to exhibit greater sensitivity to antitumor drugs, the four drugs (5-fluorouracil [5-FU], leucovorin, irinotecan, and oxaliplatin) currently used for PC patients had no statistical difference for the low- and high- group. The overexpression of RIC3 had a synergy effect with irradiation on inhibited malignant biological properties of PC cells, which was verified by detecting the proliferation ability, apoptosis rate, cell cycle distribution, and migration ability of PANC-1 cells. Conclusions We herein presented signature genes correlated with radioresistance in PC and established a risk score model competent in estimating patients’ clinical outcomes and response to antitumor drugs. The above evidence could contribute to comprehending the mechanisms of radioresistance and identifying the underlying therapy targeting.
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spelling doaj-art-210d609a45e946c59c00f81e9ccdc7032024-12-08T12:33:33ZengBMCBMC Cancer1471-24072024-12-0124111910.1186/s12885-024-13231-4Radioresistance-related gene signatures identified by transcriptomics characterize the prognosis and immune landscape of pancreatic cancer patientsDandan Wang0Jun Cao1Yanhui Chen2Lisha Zhang3Chan Zhou4Litao Huang5Yanliang Chen6The First School of Clinical Medicine, Lanzhou UniversityDepartment of Outpatient, Taihe Hospital, Hubei University of MedicineDepartment of Neuroscience and Endocrinology, Tangshan Caofeidian District HospitalDepartment of Obstetrics, Tangshan Caofeidian District HospitalDepartment of Geriatrics, Taihe Hospital, Hubei University of MedicineDepartment of Clinical Research Management, West China Hospital of Sichuan UniversityThe First School of Clinical Medicine, Lanzhou UniversityAbstract Background Radiotherapy (RT) is an important means of local treatment of solid tumors, and radioresistance is the main reason for RT failure for tumors, especially pancreatic cancer (PC). It is urgent to distinguish key genes and mechanisms of radioresistance in PC. Methods We acquired the data from The Cancer Genome Atlas (TCGA), obtained the gene modules associated with radioresistance by weighted gene coexpression network analysis (WGCNA), and identified differentially expressed genes (DEGs) between normal and tumor samples. Radioresistance-related genes (RRRGs) were determined with the intersection of WGCNA and DEGs. The hub RRRGs associated with prognosis were distinguished by the least absolute shrinkage and selection operator (LASSO) regression. We established a risk score model using multivariate Cox regression. Immune cell infiltration and drug sensitivity were evaluated through the CIBERSORT algorithm and the “OncoPredict” software package, respectively. The association of the key gene RIC3 and PC clinical features was verified in public databases, and its biological behaviors were explored in vitro. Results The intersection of DEGs and WGCNA confirmed 14 RRRGs, then six hub RRRGs were identified using LASSO. A key four genes (DUSP4, ADORA2B, SCGB2A1, and RIC3) risk score model was constructed and proved to be capable of independently estimating the prognosis of PC. There is no significant difference between risk score groups in various immune cell infiltration and response to immunotherapy. Although the low-risk group seemed to exhibit greater sensitivity to antitumor drugs, the four drugs (5-fluorouracil [5-FU], leucovorin, irinotecan, and oxaliplatin) currently used for PC patients had no statistical difference for the low- and high- group. The overexpression of RIC3 had a synergy effect with irradiation on inhibited malignant biological properties of PC cells, which was verified by detecting the proliferation ability, apoptosis rate, cell cycle distribution, and migration ability of PANC-1 cells. Conclusions We herein presented signature genes correlated with radioresistance in PC and established a risk score model competent in estimating patients’ clinical outcomes and response to antitumor drugs. The above evidence could contribute to comprehending the mechanisms of radioresistance and identifying the underlying therapy targeting.https://doi.org/10.1186/s12885-024-13231-4Pancreatic cancerRadioresistanceGene signatureRisk score modelImmune landscape
spellingShingle Dandan Wang
Jun Cao
Yanhui Chen
Lisha Zhang
Chan Zhou
Litao Huang
Yanliang Chen
Radioresistance-related gene signatures identified by transcriptomics characterize the prognosis and immune landscape of pancreatic cancer patients
BMC Cancer
Pancreatic cancer
Radioresistance
Gene signature
Risk score model
Immune landscape
title Radioresistance-related gene signatures identified by transcriptomics characterize the prognosis and immune landscape of pancreatic cancer patients
title_full Radioresistance-related gene signatures identified by transcriptomics characterize the prognosis and immune landscape of pancreatic cancer patients
title_fullStr Radioresistance-related gene signatures identified by transcriptomics characterize the prognosis and immune landscape of pancreatic cancer patients
title_full_unstemmed Radioresistance-related gene signatures identified by transcriptomics characterize the prognosis and immune landscape of pancreatic cancer patients
title_short Radioresistance-related gene signatures identified by transcriptomics characterize the prognosis and immune landscape of pancreatic cancer patients
title_sort radioresistance related gene signatures identified by transcriptomics characterize the prognosis and immune landscape of pancreatic cancer patients
topic Pancreatic cancer
Radioresistance
Gene signature
Risk score model
Immune landscape
url https://doi.org/10.1186/s12885-024-13231-4
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