Post-translational regulation of stemness under DNA damage response contributes to the gingivobuccal oral squamous cell carcinoma relapse and progression

Tobacco consumption (smoking and specifically smokeless form) in India contributes to a high prevalence of gingivobuccal oral squamous cell carcinoma (OSCC-GB). OSCC-GB exhibits high rates of locoregional relapse and therapeutic resistance, often attributed to the involvement of cancer stem cells (C...

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Main Authors: Sachendra Kumar, Annapoorni Rangarajan, Debnath Pal
Format: Article
Language:English
Published: Elsevier 2025-03-01
Series:Oral Oncology Reports
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Online Access:http://www.sciencedirect.com/science/article/pii/S2772906025000184
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author Sachendra Kumar
Annapoorni Rangarajan
Debnath Pal
author_facet Sachendra Kumar
Annapoorni Rangarajan
Debnath Pal
author_sort Sachendra Kumar
collection DOAJ
description Tobacco consumption (smoking and specifically smokeless form) in India contributes to a high prevalence of gingivobuccal oral squamous cell carcinoma (OSCC-GB). OSCC-GB exhibits high rates of locoregional relapse and therapeutic resistance, often attributed to the involvement of cancer stem cells (CSCs). The goal of this study is to leverage the generalizability of the machine learning prediction model for ‘Tumor Status’ for a comparative somatic mutation analysis between ‘With Tumor’ (recurred/relapsed/progressed) and ‘Tumor Free’ (disease-free/complete remission) OSCC-GB patients. Our results showed that support vector machines (SVM) classified the ‘Tumor Status’ classes at a mean accuracy of 89% based on clinical features. Furthermore, RNA-seq based somatic mutation analysis using the classified groups revealed molecular mechanisms underlying tumor progression and remission within OSCC-GB subgroups. The identified mutational signature (C>T mutations) related to DNA damage indicates the influence of tobacco-related carcinogens in OSCC-GB subgroups. The analysis of distinct somatic variants, functional impact predictions, protein-protein interactions, and survival analysis highlights the involvement of DNA damage response (DDR)-related genes in ‘With Tumor’, with particular focus on the significant role of the Mitogen-activated protein kinase associated protein 1 (MAPKAP1) gene, a key player in the mTORC2 signaling pathway. The study indicates that loss-of-function in the identified MAPKAP1 somatic variant may promote stemness and elevated risk of relapse and disease progression in OSCC-GB under conditions of DDR in ‘With Tumor’ OSCC-GB, potentially contributing to increased mortality rates among Indian OSCC-GB patients.
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spelling doaj-art-a54503036a2346fc830f4ac7d0f23b072025-08-20T03:42:44ZengElsevierOral Oncology Reports2772-90602025-03-011310073010.1016/j.oor.2025.100730Post-translational regulation of stemness under DNA damage response contributes to the gingivobuccal oral squamous cell carcinoma relapse and progressionSachendra Kumar0Annapoorni Rangarajan1Debnath Pal2IISc Mathematics Initiative, Indian Institute of Science, Bengaluru, 560 012, Karnataka, India; Computational and Data Science, Indian Institute of Science, Bengaluru, 560 012, Karnataka, IndiaDevelopmental Biology and Genetics, Indian Institute of Science, Bengaluru, 560 012, Karnataka, IndiaComputational and Data Science, Indian Institute of Science, Bengaluru, 560 012, Karnataka, India; Corresponding author.Tobacco consumption (smoking and specifically smokeless form) in India contributes to a high prevalence of gingivobuccal oral squamous cell carcinoma (OSCC-GB). OSCC-GB exhibits high rates of locoregional relapse and therapeutic resistance, often attributed to the involvement of cancer stem cells (CSCs). The goal of this study is to leverage the generalizability of the machine learning prediction model for ‘Tumor Status’ for a comparative somatic mutation analysis between ‘With Tumor’ (recurred/relapsed/progressed) and ‘Tumor Free’ (disease-free/complete remission) OSCC-GB patients. Our results showed that support vector machines (SVM) classified the ‘Tumor Status’ classes at a mean accuracy of 89% based on clinical features. Furthermore, RNA-seq based somatic mutation analysis using the classified groups revealed molecular mechanisms underlying tumor progression and remission within OSCC-GB subgroups. The identified mutational signature (C>T mutations) related to DNA damage indicates the influence of tobacco-related carcinogens in OSCC-GB subgroups. The analysis of distinct somatic variants, functional impact predictions, protein-protein interactions, and survival analysis highlights the involvement of DNA damage response (DDR)-related genes in ‘With Tumor’, with particular focus on the significant role of the Mitogen-activated protein kinase associated protein 1 (MAPKAP1) gene, a key player in the mTORC2 signaling pathway. The study indicates that loss-of-function in the identified MAPKAP1 somatic variant may promote stemness and elevated risk of relapse and disease progression in OSCC-GB under conditions of DDR in ‘With Tumor’ OSCC-GB, potentially contributing to increased mortality rates among Indian OSCC-GB patients.http://www.sciencedirect.com/science/article/pii/S2772906025000184GingivobuccalRelapseMachine learningPost-translational modificationmTORC2RNA-sequencing
spellingShingle Sachendra Kumar
Annapoorni Rangarajan
Debnath Pal
Post-translational regulation of stemness under DNA damage response contributes to the gingivobuccal oral squamous cell carcinoma relapse and progression
Oral Oncology Reports
Gingivobuccal
Relapse
Machine learning
Post-translational modification
mTORC2
RNA-sequencing
title Post-translational regulation of stemness under DNA damage response contributes to the gingivobuccal oral squamous cell carcinoma relapse and progression
title_full Post-translational regulation of stemness under DNA damage response contributes to the gingivobuccal oral squamous cell carcinoma relapse and progression
title_fullStr Post-translational regulation of stemness under DNA damage response contributes to the gingivobuccal oral squamous cell carcinoma relapse and progression
title_full_unstemmed Post-translational regulation of stemness under DNA damage response contributes to the gingivobuccal oral squamous cell carcinoma relapse and progression
title_short Post-translational regulation of stemness under DNA damage response contributes to the gingivobuccal oral squamous cell carcinoma relapse and progression
title_sort post translational regulation of stemness under dna damage response contributes to the gingivobuccal oral squamous cell carcinoma relapse and progression
topic Gingivobuccal
Relapse
Machine learning
Post-translational modification
mTORC2
RNA-sequencing
url http://www.sciencedirect.com/science/article/pii/S2772906025000184
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AT annapoornirangarajan posttranslationalregulationofstemnessunderdnadamageresponsecontributestothegingivobuccaloralsquamouscellcarcinomarelapseandprogression
AT debnathpal posttranslationalregulationofstemnessunderdnadamageresponsecontributestothegingivobuccaloralsquamouscellcarcinomarelapseandprogression