HCV-related hepatocellular carcinoma: gene signatures associated with TERT promoter mutations and sex

Abstract Background Hepatocellular carcinoma (HCC) is a rapidly progressing disease, frequently caused by hepatitis C virus (HCV) infection and a higher prevalence in males than females. Over 60% of HCCs harbour frequent activating mutations in the telomerase reverse transcriptase promoter (TERTp)....

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Main Authors: Patrizia Bonelli, Anna Lucia Tornesello, Franca Maria Tuccillo, Noemy Starita, Andrea Cerasuolo, Tiziana Pecchillo Cimmino, Sara Amiranda, Francesco Izzo, Gerardo Ferrara, Luigi Buonaguro, Valli De Re, Franco Maria Buonaguro, Maria Lina Tornesello
Format: Article
Language:English
Published: BMC 2025-06-01
Series:Journal of Translational Medicine
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Online Access:https://doi.org/10.1186/s12967-025-06560-w
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author Patrizia Bonelli
Anna Lucia Tornesello
Franca Maria Tuccillo
Noemy Starita
Andrea Cerasuolo
Tiziana Pecchillo Cimmino
Sara Amiranda
Francesco Izzo
Gerardo Ferrara
Luigi Buonaguro
Valli De Re
Franco Maria Buonaguro
Maria Lina Tornesello
author_facet Patrizia Bonelli
Anna Lucia Tornesello
Franca Maria Tuccillo
Noemy Starita
Andrea Cerasuolo
Tiziana Pecchillo Cimmino
Sara Amiranda
Francesco Izzo
Gerardo Ferrara
Luigi Buonaguro
Valli De Re
Franco Maria Buonaguro
Maria Lina Tornesello
author_sort Patrizia Bonelli
collection DOAJ
description Abstract Background Hepatocellular carcinoma (HCC) is a rapidly progressing disease, frequently caused by hepatitis C virus (HCV) infection and a higher prevalence in males than females. Over 60% of HCCs harbour frequent activating mutations in the telomerase reverse transcriptase promoter (TERTp). However, the relationship between TERTp status, sex, and expression of specific genes remains poorly understood. Methods We conducted a literature search to identify genes that were significantly upregulated in HCV-related HCC, compared to the respective peri-tumour tissues, in at least two independent studies. We identified 90 genes and validated their expression in 59 matched HCV-related HCC and peri-tumour tissues using a custom multiplex array qPCR. HCV-related HCC patients were stratified by TERTp mutations and sex. Statistical analysis was performed to identify relationships between different variables. Results Overall, validation analysis confirmed the upregulation of 39 out of 90 genes. Expression levels of 24 genes differed significantly between HCV-related HCC with mutant and wild type TERTp. The expression of FASTK and FLVCR1 genes correlated with TNM and tumour size (p < 0.05). High expression of NUCKS1 was associated with mortality, particularly in male patients. Overall, the expression of 57 genes was sex-linked, with 26 and 48 genes significantly overexpressed in males and in females, respectively, some of which were also associated with mutant TERTp status. Conclusions We identified unique molecular signatures in TERTp mutant HCC associated with the activation of specific genes. Such results suggest that TERTp mutant HCC might represent a distinct clinical entity. Furthermore, the up-regulation of several genes in HCV-related HCC is sex-linked. These results are crucial for understanding the mechanisms underlying TERTp mutations in tumour progression and sex-related HCC risk and for developing more effective diagnostic and prognostic biomarkers.
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spelling doaj-art-92fc232864e346918f74a97bc753dbfd2025-08-20T03:45:32ZengBMCJournal of Translational Medicine1479-58762025-06-0123111610.1186/s12967-025-06560-wHCV-related hepatocellular carcinoma: gene signatures associated with TERT promoter mutations and sexPatrizia Bonelli0Anna Lucia Tornesello1Franca Maria Tuccillo2Noemy Starita3Andrea Cerasuolo4Tiziana Pecchillo Cimmino5Sara Amiranda6Francesco Izzo7Gerardo Ferrara8Luigi Buonaguro9Valli De Re10Franco Maria Buonaguro11Maria Lina Tornesello12Molecular Biology and Viral Oncology Unit, Istituto Nazionale Tumori-IRCCS-Fondazione G. PascaleInnovative Immunological Models Unit, Istituto Nazionale Tumori-IRCCS-Fondazione G. PascaleMolecular Biology and Viral Oncology Unit, Istituto Nazionale Tumori-IRCCS-Fondazione G. PascaleMolecular Biology and Viral Oncology Unit, Istituto Nazionale Tumori-IRCCS-Fondazione G. PascaleMolecular Biology and Viral Oncology Unit, Istituto Nazionale Tumori-IRCCS-Fondazione G. PascaleMolecular Biology and Viral Oncology Unit, Istituto Nazionale Tumori-IRCCS-Fondazione G. PascaleMolecular Biology and Viral Oncology Unit, Istituto Nazionale Tumori-IRCCS-Fondazione G. PascaleDivision of Hepatobiliary Surgical Oncology, Istituto Nazionale Tumori-IRCCS-Fondazione G. PascaleAnatomic Pathology and Cytopathology Unit, Istituto Nazionale Tumori-IRCCS-Fondazione G. PascaleInnovative Immunological Models Unit, Istituto Nazionale Tumori-IRCCS-Fondazione G. PascaleImmunopathology and Cancer Biomarkers Unit, Centro di Riferimento Oncologico di Aviano (CRO), Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS)Molecular Biology and Viral Oncology Unit, Istituto Nazionale Tumori-IRCCS-Fondazione G. PascaleMolecular Biology and Viral Oncology Unit, Istituto Nazionale Tumori-IRCCS-Fondazione G. PascaleAbstract Background Hepatocellular carcinoma (HCC) is a rapidly progressing disease, frequently caused by hepatitis C virus (HCV) infection and a higher prevalence in males than females. Over 60% of HCCs harbour frequent activating mutations in the telomerase reverse transcriptase promoter (TERTp). However, the relationship between TERTp status, sex, and expression of specific genes remains poorly understood. Methods We conducted a literature search to identify genes that were significantly upregulated in HCV-related HCC, compared to the respective peri-tumour tissues, in at least two independent studies. We identified 90 genes and validated their expression in 59 matched HCV-related HCC and peri-tumour tissues using a custom multiplex array qPCR. HCV-related HCC patients were stratified by TERTp mutations and sex. Statistical analysis was performed to identify relationships between different variables. Results Overall, validation analysis confirmed the upregulation of 39 out of 90 genes. Expression levels of 24 genes differed significantly between HCV-related HCC with mutant and wild type TERTp. The expression of FASTK and FLVCR1 genes correlated with TNM and tumour size (p < 0.05). High expression of NUCKS1 was associated with mortality, particularly in male patients. Overall, the expression of 57 genes was sex-linked, with 26 and 48 genes significantly overexpressed in males and in females, respectively, some of which were also associated with mutant TERTp status. Conclusions We identified unique molecular signatures in TERTp mutant HCC associated with the activation of specific genes. Such results suggest that TERTp mutant HCC might represent a distinct clinical entity. Furthermore, the up-regulation of several genes in HCV-related HCC is sex-linked. These results are crucial for understanding the mechanisms underlying TERTp mutations in tumour progression and sex-related HCC risk and for developing more effective diagnostic and prognostic biomarkers.https://doi.org/10.1186/s12967-025-06560-wHCVGene signaturesTERTSexMaleFemale
spellingShingle Patrizia Bonelli
Anna Lucia Tornesello
Franca Maria Tuccillo
Noemy Starita
Andrea Cerasuolo
Tiziana Pecchillo Cimmino
Sara Amiranda
Francesco Izzo
Gerardo Ferrara
Luigi Buonaguro
Valli De Re
Franco Maria Buonaguro
Maria Lina Tornesello
HCV-related hepatocellular carcinoma: gene signatures associated with TERT promoter mutations and sex
Journal of Translational Medicine
HCV
Gene signatures
TERT
Sex
Male
Female
title HCV-related hepatocellular carcinoma: gene signatures associated with TERT promoter mutations and sex
title_full HCV-related hepatocellular carcinoma: gene signatures associated with TERT promoter mutations and sex
title_fullStr HCV-related hepatocellular carcinoma: gene signatures associated with TERT promoter mutations and sex
title_full_unstemmed HCV-related hepatocellular carcinoma: gene signatures associated with TERT promoter mutations and sex
title_short HCV-related hepatocellular carcinoma: gene signatures associated with TERT promoter mutations and sex
title_sort hcv related hepatocellular carcinoma gene signatures associated with tert promoter mutations and sex
topic HCV
Gene signatures
TERT
Sex
Male
Female
url https://doi.org/10.1186/s12967-025-06560-w
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