Regulator of nonsense transcripts 3B is a prognostic biomarker and associated with immune cell infiltration in lung squamous cell and hepatocellular carcinoma.

Immune infiltration Pan-cancer Prognosis analysis RENT3B

Journal

Discover oncology
ISSN: 2730-6011
Titre abrégé: Discov Oncol
Pays: United States
ID NLM: 101775142

Informations de publication

Date de publication:
27 Sep 2024
Historique:
received: 21 06 2024
accepted: 18 09 2024
medline: 27 9 2024
pubmed: 27 9 2024
entrez: 27 9 2024
Statut: epublish

Résumé

The characteristic of RENT3B in cancer remains ambiguous. We aimed to study the relationship between RENT3B and immune infiltration in liver hepatocellular carcinoma (LIHC) and lung squamous cell carcinoma (LUSC). We investigated the expression levels of RENT3B using ONCOMINE and TIMER databases, and assessed the interrelationship between RENT3B expression and survival using PrognoScan, GEPIA, and Kaplan-Meier plotter. Additionally, we examined the association between RENT3B and immune cells in the tumor microenvironment (TME), as well as markers of immune cells, using TIMER. Subsequently, we performed prognostic analysis based on the expression level of RENT3B within specific immune cell subgroups. Furthermore, we evaluated the promoter methylation profile of RENT3B between tumor and normal tissues in LIHC and LUSC using the DNMIVD database. RENT3B exhibited increased levels in both in LIHC and LUSC. High RENT3B expression was associated with unfavorable prognosis in LIHC, whereas it indicated a beneficial prognosis in LUSC. In LIHC, the expression of RENT3B positively correlated with immune infiltration levels of B cells, CD4 + T cells, CD8 + T cells, neutrophils, macrophages, and dendritic cells. However, in LUSC, the expression of RENT3B showed a negative correlation with immune infiltration levels of B cells, CD8 + T cells, neutrophils, macrophages, and dendritic cells. RENT3B exhibited positive correlations with 42 immune markers in LIHC, while it displayed negative associations with 10 immune markers in LUSC. Despite variations in immune cell enrichment and reduction subgroups, high RENT3B expression consistently indicated poor prognosis in LIHC, whereas it remained favorable in LUSC. Additionally, there were no significant differences observed in RENT3B promoter methylation between tumor and normal tissues in both LIHC and LUSC. RENT3B can affect the overall tumor prognosis and is associated with immune infiltration, especially in LIHC and LUSC. Consequently, RENT3B can become a prognostic biomarker for LIHC and LUSC.

Identifiants

DOI: 10.1007/s12672-024-01369-3 PMID: 39331207
pubmed: 39331207
doi: 10.1007/s12672-024-01369-3
pii: 10.1007/s12672-024-01369-3
doi:

Types de publication

Journal Article

Langues

eng

Pagination

479

Subventions

Organisme : the National Nature Science Foundation of China
ID : 82273441
Organisme : Knowledge Innovation Program of Wuhan-Shuguang Project
ID : 2022020801020456
Organisme : the first level of the public health youth top talent project of Hubei province
ID : 2022SCZ051
Organisme : National Basic Research Program of China
ID : 2020YFA0710700
Organisme : Tongji Hospital (HUST) Foundation for Excellent Young Scientist
ID : 2020YQ05

Informations de copyright

© 2024. The Author(s).

Références

Netea-Maier RT, Smit JWA, Netea MG. Metabolic changes in tumor cells and tumor-associated macrophages: a mutual relationship. Cancer Lett. 2018;413:102–9. https://doi.org/10.1016/j.canlet.2017.10.037 .
doi: 10.1016/j.canlet.2017.10.037 pubmed: 29111350
Bindea G, Mlecnik B, Tosolini M, et al. Spatiotemporal dynamics of intratumoral immune cells reveal the immune landscape in human cancer. Immunity. 2013;39(4):782–95. https://doi.org/10.1016/j.immuni.2013.10.003 .
doi: 10.1016/j.immuni.2013.10.003 pubmed: 24138885
Quail DF, Joyce JA. Microenvironmental regulation of tumor progression and metastasis. Nat Med. 2013;19(11):1423–37. https://doi.org/10.1038/nm.3394 .
doi: 10.1038/nm.3394 pubmed: 24202395 pmcid: 3954707
Zhu Y, Yang J, Xu D, et al. Disruption of tumour-associated macrophage trafficking by the osteopontin-induced colony-stimulating factor-1 signalling sensitises hepatocellular carcinoma to anti-PD-L1 blockade. Gut. 2019;68(9):1653–66. https://doi.org/10.1136/gutjnl-2019-318419 .
doi: 10.1136/gutjnl-2019-318419 pubmed: 30902885
De Palma M, Biziato D, Petrova TV. Microenvironmental regulation of tumour angiogenesis. Nat Rev Cancer. 2017;17(8):457–74. https://doi.org/10.1038/nrc.2017.51 .
doi: 10.1038/nrc.2017.51 pubmed: 28706266
Li X, Yao W, Yuan Y, et al. Targeting of tumour-infiltrating macrophages via CCL2/CCR2 signalling as a therapeutic strategy against hepatocellular carcinoma. Gut. 2017;66(1):157–67. https://doi.org/10.1136/gutjnl-2015-310514 .
doi: 10.1136/gutjnl-2015-310514 pubmed: 26452628
Cully M. Re-educating tumour-associated macrophages with nanoparticles. Nat Rev Drug Discov. 2018;17(7):468–468. https://doi.org/10.1038/nrd.2018.102 .
doi: 10.1038/nrd.2018.102 pubmed: 29904193
Stelzer G, Rosen N, Plaschkes I, et al. The GeneCards suite: from gene data mining to disease genome sequence analyses. CP Bioinformatics. 2016. https://doi.org/10.1002/cpbi.5 .
doi: 10.1002/cpbi.5
Laumonnier F. Mutations of the UPF3B gene, which encodes a protein widely expressed in neurons, are associated with nonspecific mental retardation with or without autism. Mol Psychiatry. 2010;15:767–76.
doi: 10.1038/mp.2009.14 pubmed: 19238151
Tarpey PS, Lucy Raymond F, Nguyen LS, et al. Mutations in UPF3B, a member of the nonsense-mediated mRNA decay complex, cause syndromic and nonsyndromic mental retardation. Nat Genet. 2007;39(9):1127–33. https://doi.org/10.1038/ng2100 .
doi: 10.1038/ng2100 pubmed: 17704778 pmcid: 2872770
Addington AM, Gauthier J, Piton A, et al. A novel frameshift mutation in UPF3B identified in brothers affected with childhood onset schizophrenia and autism spectrum disorders. Mol Psychiatry. 2011;16(3):238–9. https://doi.org/10.1038/mp.2010.59 .
doi: 10.1038/mp.2010.59 pubmed: 20479756
Rhodes DR, Kalyana-Sundaram S, Mahavisno V, et al. Oncomine 3.0: genes, pathways, and networks in a collection of 18,000 cancer gene expression profiles. Neoplasia. 2007;9(2):166–80. https://doi.org/10.1593/neo.07112 .
doi: 10.1593/neo.07112 pubmed: 17356713 pmcid: 1813932
Li T, Fan J, Wang B, et al. TIMER: a web server for comprehensive analysis of tumor-infiltrating immune cells. Can Res. 2017;77(21):e108–10. https://doi.org/10.1158/0008-5472.CAN-17-0307 .
doi: 10.1158/0008-5472.CAN-17-0307
Mizuno H, Kitada K, Nakai K, Sarai A. PrognoScan: a new database for meta-analysis of the prognostic value of genes. BMC Med Genomics. 2009;2(1):18. https://doi.org/10.1186/1755-8794-2-18 .
doi: 10.1186/1755-8794-2-18 pubmed: 19393097 pmcid: 2689870
Tang Z, Li C, Kang B, Gao G, Li C, Zhang Z. GEPIA: a web server for cancer and normal gene expression profiling and interactive analyses. Nucleic Acids Res. 2017;45(W1):W98–102. https://doi.org/10.1093/nar/gkx247 .
doi: 10.1093/nar/gkx247 pubmed: 28407145 pmcid: 5570223
Győrffy B. Integrated analysis of public datasets for the discovery and validation of survival-associated genes in solid tumors. The Innovation. 2024;5(3): 100625. https://doi.org/10.1016/j.xinn.2024.100625 .
doi: 10.1016/j.xinn.2024.100625 pubmed: 38706955 pmcid: 11066458
Győrffy B. Transcriptome-level discovery of survival-associated biomarkers and therapy targets in non-small-cell lung cancer. Br J Pharmacol. 2024;181(3):362–74. https://doi.org/10.1111/bph.16257 .
doi: 10.1111/bph.16257 pubmed: 37783508
Ding W, Chen G, Shi T. Integrative analysis identifies potential DNA methylation biomarkers for pan-cancer diagnosis and prognosis. Epigenetics. 2019;14(1):67–80. https://doi.org/10.1080/15592294.2019.1568178 .
doi: 10.1080/15592294.2019.1568178 pubmed: 30696380 pmcid: 6380428
Neu-Yilik G, Raimondeau E, Eliseev B, et al. Dual function of UPF3B in early and late translation termination. EMBO J. 2017;36(20):2968–86. https://doi.org/10.15252/embj.201797079 .
doi: 10.15252/embj.201797079 pubmed: 28899899 pmcid: 5641913
Alrahbeni T, Sartor F, Anderson J, Miedzybrodzka Z, McCaig C, Müller B. Full UPF3B function is critical for neuronal differentiation of neural stem cells. Mol Brain. 2015;8(1):33. https://doi.org/10.1186/s13041-015-0122-1 .
doi: 10.1186/s13041-015-0122-1 pubmed: 26012578 pmcid: 4445987
Giladi A, Amit I. Single-cell genomics: a stepping stone for future immunology discoveries. Cell. 2018;172(1–2):14–21. https://doi.org/10.1016/j.cell.2017.11.011 .
doi: 10.1016/j.cell.2017.11.011 pubmed: 29328909
Papalexi E, Satija R. Single-cell RNA sequencing to explore immune cell heterogeneity. Nat Rev Immunol. 2018;18(1):35–45. https://doi.org/10.1038/nri.2017.76 .
doi: 10.1038/nri.2017.76 pubmed: 28787399

Auteurs

Pengcheng Li (P)

Hepatic Surgery Center, Clinical Medicine Research Centre for Hepatic Surgery of Hubei Province, and Hubei Key Laboratory of Hepato-Pancreato-Biliary Diseases, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, Hubei, 430030, People's Republic of China.

Mi Zhou (M)

Hepatic Surgery Center, Clinical Medicine Research Centre for Hepatic Surgery of Hubei Province, and Hubei Key Laboratory of Hepato-Pancreato-Biliary Diseases, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, Hubei, 430030, People's Republic of China.

Xiaoli Gan (X)

Hepatic Surgery Center, Clinical Medicine Research Centre for Hepatic Surgery of Hubei Province, and Hubei Key Laboratory of Hepato-Pancreato-Biliary Diseases, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, Hubei, 430030, People's Republic of China.

Chaoyi Yuan (C)

Hepatic Surgery Center, Clinical Medicine Research Centre for Hepatic Surgery of Hubei Province, and Hubei Key Laboratory of Hepato-Pancreato-Biliary Diseases, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, Hubei, 430030, People's Republic of China.

Ganxun Li (G)

Hepatic Surgery Center, Clinical Medicine Research Centre for Hepatic Surgery of Hubei Province, and Hubei Key Laboratory of Hepato-Pancreato-Biliary Diseases, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, Hubei, 430030, People's Republic of China.

Guan-Nan Jin (GN)

Hepatic Surgery Center, Clinical Medicine Research Centre for Hepatic Surgery of Hubei Province, and Hubei Key Laboratory of Hepato-Pancreato-Biliary Diseases, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, Hubei, 430030, People's Republic of China. jgnlh@163.com.
Department of Internal Medicine, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, Hubei, 430071, People's Republic of China. jgnlh@163.com.

Ze-Yang Ding (ZY)

Hepatic Surgery Center, Clinical Medicine Research Centre for Hepatic Surgery of Hubei Province, and Hubei Key Laboratory of Hepato-Pancreato-Biliary Diseases, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, Hubei, 430030, People's Republic of China. zyding@tjh.tjmu.edu.cn.

Classifications MeSH