Metabolic reprogramming in saliva of mice treated with the environmental and tobacco carcinogen dibenzo[def, p]chrysene

Abstract The goal of this study is to develop a non-invasive approach for early detection of oral squamous cell carcinoma (OSCC) using our established mouse model that faithfully recapitulates the human disease. We present for the first time a comparative metabolomic profiling of saliva samples of t...

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Main Authors: Yuan-Wan Sun, Kun-Ming Chen, Cesar Aliaga, Karam El-Bayoumy
Format: Article
Language:English
Published: Nature Portfolio 2024-11-01
Series:Scientific Reports
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Online Access:https://doi.org/10.1038/s41598-024-80921-1
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author Yuan-Wan Sun
Kun-Ming Chen
Cesar Aliaga
Karam El-Bayoumy
author_facet Yuan-Wan Sun
Kun-Ming Chen
Cesar Aliaga
Karam El-Bayoumy
author_sort Yuan-Wan Sun
collection DOAJ
description Abstract The goal of this study is to develop a non-invasive approach for early detection of oral squamous cell carcinoma (OSCC) using our established mouse model that faithfully recapitulates the human disease. We present for the first time a comparative metabolomic profiling of saliva samples of the tobacco smoke constituent, dibenzo[def, p]pyrene, (DB[a, l]P) vs. DMSO (control)-treated mice using an established and highly sensitive LC-MS/MS approach. DB[a, l]P was administered by topical application into the mouse oral cavity (25 µmol, 3x week for 6 weeks) and saliva was collected 24 h after the last dose of carcinogen administration. Using an untargeted metabolomics approach (negative and positive modes), we found that DB[a, l]P differentially altered several metabolites known to be involved in the carcinogenesis process when compared to DMSO. Of particular significance, we found that DB[a, l]P significantly enriched the levels of phosphatidic acid, known to bind and activate mTORC which can enhance proliferation and promote carcinogenesis. Pathway enrichment analysis revealed that DB[a, l]P altered two major lipid metabolism pathways (phospholipid biosynthesis and glycerolipid metabolism). Collectively, our results using saliva as a safe and non-invasive approach, provide additional mechanistic insights on DB[a, l]P-induced OSCC and potential biomarkers for early detection and an opportunity for cancer interception via reprogramming lipid metabolism.
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spelling doaj-art-e685e8a574f742d1841d51140278c20f2024-12-01T12:24:33ZengNature PortfolioScientific Reports2045-23222024-11-0114111010.1038/s41598-024-80921-1Metabolic reprogramming in saliva of mice treated with the environmental and tobacco carcinogen dibenzo[def, p]chryseneYuan-Wan Sun0Kun-Ming Chen1Cesar Aliaga2Karam El-Bayoumy3Department of Biochemistry and Molecular Biology, Pennsylvania State University College of MedicineDepartment of Biochemistry and Molecular Biology, Pennsylvania State University College of MedicineDepartment of Biochemistry and Molecular Biology, Pennsylvania State University College of MedicineDepartment of Biochemistry and Molecular Biology, Pennsylvania State University College of MedicineAbstract The goal of this study is to develop a non-invasive approach for early detection of oral squamous cell carcinoma (OSCC) using our established mouse model that faithfully recapitulates the human disease. We present for the first time a comparative metabolomic profiling of saliva samples of the tobacco smoke constituent, dibenzo[def, p]pyrene, (DB[a, l]P) vs. DMSO (control)-treated mice using an established and highly sensitive LC-MS/MS approach. DB[a, l]P was administered by topical application into the mouse oral cavity (25 µmol, 3x week for 6 weeks) and saliva was collected 24 h after the last dose of carcinogen administration. Using an untargeted metabolomics approach (negative and positive modes), we found that DB[a, l]P differentially altered several metabolites known to be involved in the carcinogenesis process when compared to DMSO. Of particular significance, we found that DB[a, l]P significantly enriched the levels of phosphatidic acid, known to bind and activate mTORC which can enhance proliferation and promote carcinogenesis. Pathway enrichment analysis revealed that DB[a, l]P altered two major lipid metabolism pathways (phospholipid biosynthesis and glycerolipid metabolism). Collectively, our results using saliva as a safe and non-invasive approach, provide additional mechanistic insights on DB[a, l]P-induced OSCC and potential biomarkers for early detection and an opportunity for cancer interception via reprogramming lipid metabolism.https://doi.org/10.1038/s41598-024-80921-1Tobacco and Environmental CarcinogensOral squamous cell carcinomaMouse modelSalivaMetabolic profiles
spellingShingle Yuan-Wan Sun
Kun-Ming Chen
Cesar Aliaga
Karam El-Bayoumy
Metabolic reprogramming in saliva of mice treated with the environmental and tobacco carcinogen dibenzo[def, p]chrysene
Scientific Reports
Tobacco and Environmental Carcinogens
Oral squamous cell carcinoma
Mouse model
Saliva
Metabolic profiles
title Metabolic reprogramming in saliva of mice treated with the environmental and tobacco carcinogen dibenzo[def, p]chrysene
title_full Metabolic reprogramming in saliva of mice treated with the environmental and tobacco carcinogen dibenzo[def, p]chrysene
title_fullStr Metabolic reprogramming in saliva of mice treated with the environmental and tobacco carcinogen dibenzo[def, p]chrysene
title_full_unstemmed Metabolic reprogramming in saliva of mice treated with the environmental and tobacco carcinogen dibenzo[def, p]chrysene
title_short Metabolic reprogramming in saliva of mice treated with the environmental and tobacco carcinogen dibenzo[def, p]chrysene
title_sort metabolic reprogramming in saliva of mice treated with the environmental and tobacco carcinogen dibenzo def p chrysene
topic Tobacco and Environmental Carcinogens
Oral squamous cell carcinoma
Mouse model
Saliva
Metabolic profiles
url https://doi.org/10.1038/s41598-024-80921-1
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