Revealing molecular mechanisms of early-onset tongue cancer by spatial transcriptomics.

Humans Tongue Neoplasms / genetics Male Adult Middle Aged Female Transcriptome Gene Expression Profiling Gene Expression Regulation, Neoplastic Aged Age of Onset Tumor Microenvironment / genetics Carcinoma, Squamous Cell / genetics
Oral cancer Single cell sequencing Spatial transcriptomics Tongue squamous cell carcinoma Young adults

Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
01 Nov 2024
Historique:
received: 22 03 2024
accepted: 10 10 2024
medline: 1 11 2024
pubmed: 1 11 2024
entrez: 1 11 2024
Statut: epublish

Résumé

Tongue cancer at a young age demonstrates an increase in incidence, aggressiveness, and poor response to therapy. Classic etiological factors for head and neck tumors such as tobacco, alcohol, and human papillomavirus are not related to early-onset tongue cancer. Mechanisms of development and progression of this cancer remain unclear. In this study, we performed spatial whole-transcriptome profiling of tongue cancer in young adults compared with older patients. Nine patients with tongue squamous cell carcinoma (T2-3N0-1M0) were included and divided into two groups: younger (n = 5) and older than 45 years (n = 4). Formalin-fixed paraffin-embedded (FFPE) and fresh frozen (FF) samples of tumor tissue from 4 young and 5 older patients, respectively, were used for spatial transcriptomic profiling using the 10 × Genomics Visium. The findings were validated using SeekGene single cell full-length RNA sequencing (1 young vs 1 older patient) and TCGA data (15 young vs 70 older patients). As a result, we performed the first successful integration of spatial transcriptomics data from FF and FFPE samples and revealed distinctive features of tongue cancer in young adults. Oxidative stress, vascular mimicry, and MAPK and JAK-STAT pathways were enriched in early-onset tongue cancer. Tumor microenvironment demonstrated increased gene signatures corresponding to myeloid-derived suppressor cells, tumor-associated macrophages, and plasma cells. The invasive front was accompanied by vascular mimicry with arrangement of tumor-associated macrophages and aggregations of plasma cells and lymphocytes organized into tertiary lymphoid structures. Taken together, these results indicate that early-onset tongue cancer has distinct transcriptomic features and molecular mechanisms compared to older patients.

Identifiants

DOI: 10.1038/s41598-024-76044-2 PMID: 39482351
pubmed: 39482351
doi: 10.1038/s41598-024-76044-2
pii: 10.1038/s41598-024-76044-2
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

26255

Subventions

Organisme : Russian Science Foundation
ID : 22-15-00308

Informations de copyright

© 2024. The Author(s).

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Auteurs

Marina R Patysheva (MR)

Laboratory of Cancer Progression Biology, Cancer Research Institute, Tomsk National Research Medical Center, Russian Academy of Sciences, Tomsk, Russia.

Elena S Kolegova (ES)

Laboratory of Cancer Progression Biology, Cancer Research Institute, Tomsk National Research Medical Center, Russian Academy of Sciences, Tomsk, Russia. elenakolegowa@mail.ru.

Anna A Khozyainova (AA)

Laboratory of Cancer Progression Biology, Cancer Research Institute, Tomsk National Research Medical Center, Russian Academy of Sciences, Tomsk, Russia.

Elizaveta A Prostakishina (EA)

Laboratory of Cancer Progression Biology, Cancer Research Institute, Tomsk National Research Medical Center, Russian Academy of Sciences, Tomsk, Russia.

Vyacheslav Y Korobeynikov (VY)

Laboratory of Cancer Progression Biology, Cancer Research Institute, Tomsk National Research Medical Center, Russian Academy of Sciences, Tomsk, Russia.

Maxim E Menyailo (ME)

Laboratory of Cancer Progression Biology, Cancer Research Institute, Tomsk National Research Medical Center, Russian Academy of Sciences, Tomsk, Russia.
Laboratory of Single Cell Biology, Research Institute of Molecular and Cellular Medicine, Peoples' Friendship University of Russia (RUDN University), Moscow, Russia.

Pavel S Iamshchikov (PS)

Laboratory of Cancer Progression Biology, Cancer Research Institute, Tomsk National Research Medical Center, Russian Academy of Sciences, Tomsk, Russia.

Dmitry M Loos (DM)

Department of Pathological Anatomy, Siberian State Medical University, Tomsk, Russia.
Department of General and Molecular Pathology, Cancer Research Institute, Tomsk National Research Medical Center, Russian Academy of Sciences, Tomsk, Russia.

Oleg I Kovalev (OI)

Department of Pathological Anatomy, Siberian State Medical University, Tomsk, Russia.
Department of General and Molecular Pathology, Cancer Research Institute, Tomsk National Research Medical Center, Russian Academy of Sciences, Tomsk, Russia.

Marina V Zavyalova (MV)

Department of Pathological Anatomy, Siberian State Medical University, Tomsk, Russia.
Department of General and Molecular Pathology, Cancer Research Institute, Tomsk National Research Medical Center, Russian Academy of Sciences, Tomsk, Russia.

Irina K Fedorova (IK)

Department of Head and Neck Tumors, Cancer Research Institute, Tomsk National Research Medical Center, Russian Academy of Sciences, Tomsk, Russia.

Denis E Kulbakin (DE)

Department of Head and Neck Tumors, Cancer Research Institute, Tomsk National Research Medical Center, Russian Academy of Sciences, Tomsk, Russia.

Irina V Larionova (IV)

Laboratory of Cancer Progression Biology, Cancer Research Institute, Tomsk National Research Medical Center, Russian Academy of Sciences, Tomsk, Russia.
Laboratory of Molecular Cancer Therapy, Cancer Research Institute, Tomsk National Research Medical Center Tomsk, Russian Academy of Sciences, Tomsk, Russia.

Andrey P Polyakov (AP)

Microsurgery Department, P.A. Herzen Moscow Oncology Research Institute - a branch of the National Medical Research Radiological Center, Moscow, Russia.

Liliya P Yakovleva (LP)

Department of Head and Neck Tumors, A.S. Loginov Moscow Clinical Scientific Center, Moscow Healthcare Department, Moscow, Russia.

Mikhail A Kropotov (MA)

Surgical Department N10 of Head and Neck Tumors, N.N. Blokhin National Medical Research Center of Oncology, Ministry of Health of the Russian Federation, Moscow, Russia.

Natalya S Sukortseva (NS)

Department of Oncology, Radiotherapy and Plastic Surgery, I.M. Sechenov First Moscow State Medical University, Ministry of Health of the Russian Federation, Moscow, Russia.

Yusheng Lu (Y)

College of Materials and Chemical Engineering, Minjiang University, Fuzhou, Fujian, China.

Lee Jia (L)

The First Affiliated Hospital, Henan University, Kaifeng, Henan, China.

Rohit Arora (R)

Department of Biochemistry & Molecular Biology, Cumming School of Medicine, University of Calgary, Calgary, AB, Canada.

Evgeny L Choinzonov (EL)

Department of Head and Neck Tumors, Cancer Research Institute, Tomsk National Research Medical Center, Russian Academy of Sciences, Tomsk, Russia.

Pinaki Bose (P)

Department of Biochemistry & Molecular Biology, Cumming School of Medicine, University of Calgary, Calgary, AB, Canada.

Evgeny V Denisov (EV)

Laboratory of Cancer Progression Biology, Cancer Research Institute, Tomsk National Research Medical Center, Russian Academy of Sciences, Tomsk, Russia.
Laboratory of Single Cell Biology, Research Institute of Molecular and Cellular Medicine, Peoples' Friendship University of Russia (RUDN University), Moscow, Russia.

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Classifications MeSH

questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Primates › Haplorhini › Catarrhini › Hominidae › Humains › Revealing molecular mechanisms of early-onset...
questionsmedicales.fr › Maladies du système stomatognathique › Maladies de la bouche › Maladies de la langue › Tumeurs de la langue › Revealing molecular mechanisms of early-onset...
questionsmedicales.fr › Personnes › Tranches d'âge › Adulte › Revealing molecular mechanisms of early-onset...
questionsmedicales.fr › Personnes › Tranches d'âge › Adulte › Adulte d'âge moyen › Revealing molecular mechanisms of early-onset...
questionsmedicales.fr › Phénomènes génétiques › Structures génétiques › Transcriptome › Revealing molecular mechanisms of early-onset...
questionsmedicales.fr › Techniques d'investigation › Techniques génétiques › Analyse de profil d'expression de gènes › Revealing molecular mechanisms of early-onset...
questionsmedicales.fr › Phénomènes génétiques › Régulation de l'expression des gènes › Régulation de l'expression des gènes tumoraux › Revealing molecular mechanisms of early-onset...
questionsmedicales.fr › Personnes › Tranches d'âge › Adulte › Sujet âgé › Revealing molecular mechanisms of early-onset...
questionsmedicales.fr › Environnement et santé publique › Santé publique › Facteurs épidémiologiques › Facteurs âges › Âge de début › Revealing molecular mechanisms of early-onset...
questionsmedicales.fr › Phénomènes physiologiques cellulaires › Microenvironnement cellulaire › Microenvironnement tumoral › Revealing molecular mechanisms of early-onset...
questionsmedicales.fr › Tumeurs › Tumeurs par type histologique › Tumeurs épithéliales épidermoïdes et glandulaires › Tumeurs épidermoïdes › Carcinome épidermoïde › Revealing molecular mechanisms of early-onset...