Spermine accumulation via spermine synthase promotes tumor cell proliferation in head and neck squamous cell carcinoma

Abstract Background Head and neck squamous cell carcinoma (HNSCC) is among the most aggressive malignancies, underscoring the need for early diagnosis to improve patient outcomes. Tumor-derived exosomes, which can be non-invasively obtained and reflect the metabolic state of tumors in real-time, are...

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Main Authors: Xi Chen, Fei Song, Peng Xiao, Yisong Yao, Dongxian Li, Yuhui Fang, Shijun Lv, Yakui Mou, Yumei Li, Xicheng Song
Format: Article
Language:English
Published: BMC 2025-03-01
Series:BMC Cancer
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Online Access:https://doi.org/10.1186/s12885-025-13820-x
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author Xi Chen
Fei Song
Peng Xiao
Yisong Yao
Dongxian Li
Yuhui Fang
Shijun Lv
Yakui Mou
Yumei Li
Xicheng Song
author_facet Xi Chen
Fei Song
Peng Xiao
Yisong Yao
Dongxian Li
Yuhui Fang
Shijun Lv
Yakui Mou
Yumei Li
Xicheng Song
author_sort Xi Chen
collection DOAJ
description Abstract Background Head and neck squamous cell carcinoma (HNSCC) is among the most aggressive malignancies, underscoring the need for early diagnosis to improve patient outcomes. Tumor-derived exosomes, which can be non-invasively obtained and reflect the metabolic state of tumors in real-time, are under increasing investigation for their diagnostic potential. Herein we analyzed metabolite differences in exosomes, serum, and tissues from patients with HNSCC to identify potential diagnostic biomarkers of clinical relevance. Methods Non-targeted metabolomics based on liquid chromatography–mass spectrometry was employed to quantify metabolites in exosome, serum, and tissue samples from 11 patients with HNSCC and six patients without cancer. The metabolic profiles of HNSCC were analyzed through univariate and multivariate statistical methods, differential metabolite analysis, and pathway enrichment analysis. Results We identified three differential metabolites in exosomes, 45 in serum, and 33 in tissues. Notably, patients with HNSCC exhibited significant disruptions in protein and amino acid metabolism. Spermine was exclusively detected in exosomes and tissues from patients with HNSCC. We hypothesize that spermine is extracellularly secreted by malignant cells via exosomes and subsequently enters the bloodstream. Moreover, spermine synthase was highly expressed in HNSCC tissues. Knocking down spermine synthase markedly impaired HNSCC cell proliferation and migration. Conclusions This study provides a preliminarily characterization of the metabolic profile of HNSCC and highlights spermine and its synthetic pathways as potential diagnostic and therapeutic targets. Future studies are warranted to elucidate the mechanism of action of spermine in HNSCC and explore its utility in early diagnosis and therapeutic development.
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spelling doaj-art-c962805b7acf4bf1a27c0f461fddd5f92025-08-20T02:59:58ZengBMCBMC Cancer1471-24072025-03-0125111410.1186/s12885-025-13820-xSpermine accumulation via spermine synthase promotes tumor cell proliferation in head and neck squamous cell carcinomaXi Chen0Fei Song1Peng Xiao2Yisong Yao3Dongxian Li4Yuhui Fang5Shijun Lv6Yakui Mou7Yumei Li8Xicheng Song9Department of Otorhinolaryngology, Head and Neck Surgery, Yantai Yuhuangding Hospital, Qingdao UniversityLudong UniversityDepartment of Otorhinolaryngology, Head and Neck Surgery, Yantai Yuhuangding Hospital, Qingdao UniversityDepartment of Otorhinolaryngology, Head and Neck Surgery, Yantai Yuhuangding Hospital, Qingdao UniversityDepartment of Otorhinolaryngology, Head and Neck Surgery, Yantai Yuhuangding Hospital, Qingdao UniversityDepartment of Otorhinolaryngology, Head and Neck Surgery, Yantai Yuhuangding Hospital, Qingdao UniversityDepartment of Otorhinolaryngology, Head and Neck Surgery, Yantai Yuhuangding Hospital, Qingdao UniversityDepartment of Otorhinolaryngology, Head and Neck Surgery, Yantai Yuhuangding Hospital, Qingdao UniversityDepartment of Otorhinolaryngology, Head and Neck Surgery, Yantai Yuhuangding Hospital, Qingdao UniversityDepartment of Otorhinolaryngology, Head and Neck Surgery, Yantai Yuhuangding Hospital, Qingdao UniversityAbstract Background Head and neck squamous cell carcinoma (HNSCC) is among the most aggressive malignancies, underscoring the need for early diagnosis to improve patient outcomes. Tumor-derived exosomes, which can be non-invasively obtained and reflect the metabolic state of tumors in real-time, are under increasing investigation for their diagnostic potential. Herein we analyzed metabolite differences in exosomes, serum, and tissues from patients with HNSCC to identify potential diagnostic biomarkers of clinical relevance. Methods Non-targeted metabolomics based on liquid chromatography–mass spectrometry was employed to quantify metabolites in exosome, serum, and tissue samples from 11 patients with HNSCC and six patients without cancer. The metabolic profiles of HNSCC were analyzed through univariate and multivariate statistical methods, differential metabolite analysis, and pathway enrichment analysis. Results We identified three differential metabolites in exosomes, 45 in serum, and 33 in tissues. Notably, patients with HNSCC exhibited significant disruptions in protein and amino acid metabolism. Spermine was exclusively detected in exosomes and tissues from patients with HNSCC. We hypothesize that spermine is extracellularly secreted by malignant cells via exosomes and subsequently enters the bloodstream. Moreover, spermine synthase was highly expressed in HNSCC tissues. Knocking down spermine synthase markedly impaired HNSCC cell proliferation and migration. Conclusions This study provides a preliminarily characterization of the metabolic profile of HNSCC and highlights spermine and its synthetic pathways as potential diagnostic and therapeutic targets. Future studies are warranted to elucidate the mechanism of action of spermine in HNSCC and explore its utility in early diagnosis and therapeutic development.https://doi.org/10.1186/s12885-025-13820-xHNSCCSpermine synthaseMetabolomicsLiquid chromatography–mass spectrometryDiagnostic biomarkersTumor metabolism
spellingShingle Xi Chen
Fei Song
Peng Xiao
Yisong Yao
Dongxian Li
Yuhui Fang
Shijun Lv
Yakui Mou
Yumei Li
Xicheng Song
Spermine accumulation via spermine synthase promotes tumor cell proliferation in head and neck squamous cell carcinoma
BMC Cancer
HNSCC
Spermine synthase
Metabolomics
Liquid chromatography–mass spectrometry
Diagnostic biomarkers
Tumor metabolism
title Spermine accumulation via spermine synthase promotes tumor cell proliferation in head and neck squamous cell carcinoma
title_full Spermine accumulation via spermine synthase promotes tumor cell proliferation in head and neck squamous cell carcinoma
title_fullStr Spermine accumulation via spermine synthase promotes tumor cell proliferation in head and neck squamous cell carcinoma
title_full_unstemmed Spermine accumulation via spermine synthase promotes tumor cell proliferation in head and neck squamous cell carcinoma
title_short Spermine accumulation via spermine synthase promotes tumor cell proliferation in head and neck squamous cell carcinoma
title_sort spermine accumulation via spermine synthase promotes tumor cell proliferation in head and neck squamous cell carcinoma
topic HNSCC
Spermine synthase
Metabolomics
Liquid chromatography–mass spectrometry
Diagnostic biomarkers
Tumor metabolism
url https://doi.org/10.1186/s12885-025-13820-x
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