Plasma galectins and metabolites in advanced head and neck carcinomas: evidence of distinct immune characteristics linked to hypopharyngeal tumors

Extra-cellular galectins 1, 3 and 9 (gal-1, −3 and −9) are known to act as soluble immunosuppressive agents in various malignancies. Previous publications have suggested that their expression is dependent on the metabolic status of producing cells and reciprocally that they can influence metabolic p...

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Main Authors: Bao-Tram Thi Tran, Aurore Gelin, Sylvère Durand, Matthieu Texier, Amaury Daste, Clémence Toullec, Karim Benihoud, Ingrid Breuskin, Philippe Gorphe, Florence Garic, Catherine Brenner, Christophe Le Tourneau, Jérôme Fayette, Toshiro Niki, Muriel David, Pierre Busson, Caroline Even
Format: Article
Language:English
Published: Taylor & Francis Group 2023-12-01
Series:OncoImmunology
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Online Access:https://www.tandfonline.com/doi/10.1080/2162402X.2022.2150472
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author Bao-Tram Thi Tran
Aurore Gelin
Sylvère Durand
Matthieu Texier
Amaury Daste
Clémence Toullec
Karim Benihoud
Ingrid Breuskin
Philippe Gorphe
Florence Garic
Catherine Brenner
Christophe Le Tourneau
Jérôme Fayette
Toshiro Niki
Muriel David
Pierre Busson
Caroline Even
author_facet Bao-Tram Thi Tran
Aurore Gelin
Sylvère Durand
Matthieu Texier
Amaury Daste
Clémence Toullec
Karim Benihoud
Ingrid Breuskin
Philippe Gorphe
Florence Garic
Catherine Brenner
Christophe Le Tourneau
Jérôme Fayette
Toshiro Niki
Muriel David
Pierre Busson
Caroline Even
author_sort Bao-Tram Thi Tran
collection DOAJ
description Extra-cellular galectins 1, 3 and 9 (gal-1, −3 and −9) are known to act as soluble immunosuppressive agents in various malignancies. Previous publications have suggested that their expression is dependent on the metabolic status of producing cells and reciprocally that they can influence metabolic pathways in their target cells. Very little is known about the status of gal-1, −3 and −9 in patients bearing head and neck squamous cell carcinomas (HNSCC) and about their relationships with the systemic metabolic condition. This study was conducted in plasma samples from a prospective cohort of 83 HNSCC patients with advanced disease. These samples were used to explore the distribution of gal-1, −3 and −9 and simultaneously to profile a series of 87 metabolites assessed by mass spectrometry. We identified galectin and metabolic patterns within five disease categories defined according to the primary site and human papillomavirus (HPV) status (HPV-positive and -negative oropharyngeal carcinomas, carcinomas of the oral cavity, hypopharynx and larynx carcinomas). Remarkably, samples related to hypopharyngeal carcinomas displayed the highest average concentration of gal-9 (p = .017) and a trend toward higher concentrations of kynurenine, a potential factor of tumor growth and immune suppression. In contrast, there was a tendency toward higher concentrations of fatty acids in samples related to oral cavity. These observations emphasize the diversity of HPV-negative HNSCCs. Depending on their primary site, they evolve into distinct types of immune and metabolic landscapes that seem to be congruent with specific oncogenic mechanisms.
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spelling doaj-art-719766cfc1884b85a06769ebea03df1c2025-08-20T02:50:44ZengTaylor & Francis GroupOncoImmunology2162-402X2023-12-0112110.1080/2162402X.2022.2150472Plasma galectins and metabolites in advanced head and neck carcinomas: evidence of distinct immune characteristics linked to hypopharyngeal tumorsBao-Tram Thi Tran0Aurore Gelin1Sylvère Durand2Matthieu Texier3Amaury Daste4Clémence Toullec5Karim Benihoud6Ingrid Breuskin7Philippe Gorphe8Florence Garic9Catherine Brenner10Christophe Le Tourneau11Jérôme Fayette12Toshiro Niki13Muriel David14Pierre Busson15Caroline Even16CNRS UMR 9018-METSY, Gustave Roussy and Université Paris-Saclay, Villejuif, FranceCNRS UMR 9018-METSY, Gustave Roussy and Université Paris-Saclay, Villejuif, FrancePlateforme de Métabolomique/UMR 1138, Gustave Roussy and Université Paris-Saclay, Villejuif, FranceService d’Epidémiologie et de Biostatistiques, Gustave Roussy and Université Paris-Saclay, Villejuif, FranceDepartment of Medical Oncology, Hôpital Saint André, Bordeaux, FranceGI and Liver/Head and Neck unit, Institut du Cancer-Avignon Provence, Avignon, FranceCNRS UMR 9018-METSY, Gustave Roussy and Université Paris-Saclay, Villejuif, FranceService de Cancérologie Cervico-Faciale, Gustave Roussy, Villejuif, FranceService de Cancérologie Cervico-Faciale, Gustave Roussy, Villejuif, FranceDepartment R&D, Unicancer, Paris cedex 13, FranceCNRS UMR 9018-METSY, Gustave Roussy and Université Paris-Saclay, Villejuif, FranceDepartment of Drug Development and Innovation (D3i), Institut Curie and Paris-Saclay University, Paris, FranceClaude Bernard Lyon 1 University, INSERM 1052, CNRS 5286 & Department of Medical Oncology, Centre Léon Bérard, Cancer Research Center of Lyon, Lyon, FranceDepartment of Immunology, Kagawa University, Kita-gun, JapanHiFiBiO Therapeutics, Pépinière Paris Santé Cochin, Paris, FranceCNRS UMR 9018-METSY, Gustave Roussy and Université Paris-Saclay, Villejuif, FranceService de Cancérologie Cervico-Faciale, Gustave Roussy, Villejuif, FranceExtra-cellular galectins 1, 3 and 9 (gal-1, −3 and −9) are known to act as soluble immunosuppressive agents in various malignancies. Previous publications have suggested that their expression is dependent on the metabolic status of producing cells and reciprocally that they can influence metabolic pathways in their target cells. Very little is known about the status of gal-1, −3 and −9 in patients bearing head and neck squamous cell carcinomas (HNSCC) and about their relationships with the systemic metabolic condition. This study was conducted in plasma samples from a prospective cohort of 83 HNSCC patients with advanced disease. These samples were used to explore the distribution of gal-1, −3 and −9 and simultaneously to profile a series of 87 metabolites assessed by mass spectrometry. We identified galectin and metabolic patterns within five disease categories defined according to the primary site and human papillomavirus (HPV) status (HPV-positive and -negative oropharyngeal carcinomas, carcinomas of the oral cavity, hypopharynx and larynx carcinomas). Remarkably, samples related to hypopharyngeal carcinomas displayed the highest average concentration of gal-9 (p = .017) and a trend toward higher concentrations of kynurenine, a potential factor of tumor growth and immune suppression. In contrast, there was a tendency toward higher concentrations of fatty acids in samples related to oral cavity. These observations emphasize the diversity of HPV-negative HNSCCs. Depending on their primary site, they evolve into distinct types of immune and metabolic landscapes that seem to be congruent with specific oncogenic mechanisms.https://www.tandfonline.com/doi/10.1080/2162402X.2022.2150472Head and neck carcinomasplasma galectinsplasma metaboliteskynurenine
spellingShingle Bao-Tram Thi Tran
Aurore Gelin
Sylvère Durand
Matthieu Texier
Amaury Daste
Clémence Toullec
Karim Benihoud
Ingrid Breuskin
Philippe Gorphe
Florence Garic
Catherine Brenner
Christophe Le Tourneau
Jérôme Fayette
Toshiro Niki
Muriel David
Pierre Busson
Caroline Even
Plasma galectins and metabolites in advanced head and neck carcinomas: evidence of distinct immune characteristics linked to hypopharyngeal tumors
OncoImmunology
Head and neck carcinomas
plasma galectins
plasma metabolites
kynurenine
title Plasma galectins and metabolites in advanced head and neck carcinomas: evidence of distinct immune characteristics linked to hypopharyngeal tumors
title_full Plasma galectins and metabolites in advanced head and neck carcinomas: evidence of distinct immune characteristics linked to hypopharyngeal tumors
title_fullStr Plasma galectins and metabolites in advanced head and neck carcinomas: evidence of distinct immune characteristics linked to hypopharyngeal tumors
title_full_unstemmed Plasma galectins and metabolites in advanced head and neck carcinomas: evidence of distinct immune characteristics linked to hypopharyngeal tumors
title_short Plasma galectins and metabolites in advanced head and neck carcinomas: evidence of distinct immune characteristics linked to hypopharyngeal tumors
title_sort plasma galectins and metabolites in advanced head and neck carcinomas evidence of distinct immune characteristics linked to hypopharyngeal tumors
topic Head and neck carcinomas
plasma galectins
plasma metabolites
kynurenine
url https://www.tandfonline.com/doi/10.1080/2162402X.2022.2150472
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