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4. Involvement of the M-CSF/IL-34/CSF- 1R pathway in malignant pleural mesothelioma

Author

Blondy, Thibaut, d'Almeida, Senan Mickael, Briolay, Tina, Tabiasco, Julie, Meiller, Clement, Chene, Anne-Laure, Cellerin, Laurent, Deshayes, Sophie, Delneste, Yves, Fonteneau, Jean-Francois, Boisgerault, Nicolas, Bennouna, Jaafar, Gregoire, Marc, Jean, Didier, Blanquart, Christophe, Immunogenic Cell Death and Mesothelioma Therapy (CRCINA-ÉQUIPE 4), Centre de Recherche en Cancérologie et Immunologie Nantes-Angers (CRCINA), Institut National de la Santé et de la Recherche Médicale (INSERM)-Université de Nantes - UFR de Médecine et des Techniques Médicales (UFR MEDECINE), Université de Nantes (UN)-Université de Nantes (UN)-Centre hospitalier universitaire de Nantes (CHU Nantes)-Centre National de la Recherche Scientifique (CNRS)-Université d'Angers (UA)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université de Nantes - UFR de Médecine et des Techniques Médicales (UFR MEDECINE), Université de Nantes (UN)-Université de Nantes (UN)-Centre hospitalier universitaire de Nantes (CHU Nantes)-Centre National de la Recherche Scientifique (CNRS)-Université d'Angers (UA), Innate Immunity and Immunotherapy (CRCINA-ÉQUIPE 7), Université de Lausanne (UNIL), Centre de Recherche des Cordeliers (CRC (UMR_S_1138 / U1138)), École pratique des hautes études (EPHE), Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Sorbonne Université (SU)-Université de Paris (UP), Service d'Oncologie Médicale Thoracique et Digestive [CHU Nantes], Centre hospitalier universitaire de Nantes (CHU Nantes), Laboratoire d'Immunologie et d'Allergologie [CHU Angers], Centre Hospitalier Universitaire d'Angers (CHU Angers), PRES Université Nantes Angers Le Mans (UNAM)-PRES Université Nantes Angers Le Mans (UNAM), Université d'Angers (UA)-Université de Nantes (UN)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Centre hospitalier universitaire de Nantes (CHU Nantes)-Université d'Angers (UA)-Université de Nantes (UN)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Centre hospitalier universitaire de Nantes (CHU Nantes), Université de Lausanne = University of Lausanne (UNIL), Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Sorbonne Université (SU)-Université Paris Cité (UPCité), and Bernardo, Elizabeth

Subjects
Male, tumors, interleukin-34, Pleural Neoplasms, [SDV.CAN]Life Sciences [q-bio]/Cancer, CD8-Positive T-Lymphocytes, survival, Monocytes, immunology, [SDV.CAN] Life Sciences [q-bio]/Cancer, cytokine, Biomarkers, Tumor, Tumor Microenvironment, cancer, Humans, Aged, tumor-associated macrophages, Interleukins, Macrophage Colony-Stimulating Factor, Macrophages, Mesothelioma, Malignant, Basic Tumor Immunology, Prognosis, Pleural Effusion, Survival Rate, classification, Receptors, Granulocyte-Macrophage Colony-Stimulating Factor, oncology, cells, identification, Cytokines, Female, Follow-Up Studies, T-Lymphocytes, Cytotoxic
Abstract

International audience; Background: Malignant pleural mesothelioma (MPM) is a rare and aggressive cancer related to asbestos exposure. The tumor microenvironment content, particularly the presence of macrophages, was described as crucial for the development of the disease. This work aimed at studying the involvement of the M-CSF (CSF-1)/IL-34/CSF-1R pathway in the formation of macrophages in MPM, using samples from patients.Methods: Pleural effusions (PEs), frozen tumors, primary MPM cells and MPM cell lines used in this study belong to biocollections associated with clinical databases. Cytokine expressions were studied using real-time PCR and ELISA. The Cancer Genome Atlas database was used to confirm our results on an independent cohort. An original three-dimensional (3D) coculture model including MPM cells, monocytes from healthy donors and a tumor antigen-specific cytotoxic CD8 T cell clone was used.Results: We observed that high interleukin (IL)-34 levels in PE were significantly associated with a shorter survival of patients. In tumors, expression of CSF1 was correlated with 'M2-like macrophages' markers, whereas this was not the case with IL34 expression, suggesting two distinct modes of action of these cytokines. Expression of IL34 was higher in MPM cells compared with primary mesothelial cells. Particularly, high expression of IL34 was observed in MPM cells with an alteration of CDKN2A. Finally, using 3D coculture model, we demonstrated the direct involvement of MPM cells in the formation of immunosuppressive macrophages, through activation of the colony stimulating factor-1 receptor (CSF1-R) pathway, causing the inhibition of cytotoxicity of tumor antigen-specific CD8+ T cells.Conclusions: The M-CSF/IL-34/CSF-1R pathway seems strongly implicated in MPM and could constitute a therapeutic target to act on immunosuppression and to support immunotherapeutic strategies.

Published
2020
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6. Involvement of the M-CSF/IL-34/CSF-1R pathway in malignant pleural mesothelioma.

Author

Blondy T, d'Almeida SM, Briolay T, Tabiasco J, Meiller C, Chéné AL, Cellerin L, Deshayes S, Delneste Y, Fonteneau JF, Boisgerault N, Bennouna J, Grégoire M, Jean D, and Blanquart C

Subjects
Aged, Biomarkers, Tumor genetics, CD8-Positive T-Lymphocytes immunology, CD8-Positive T-Lymphocytes metabolism, CD8-Positive T-Lymphocytes pathology, Cytokines metabolism, Female, Follow-Up Studies, Humans, Interleukins genetics, Macrophage Colony-Stimulating Factor genetics, Macrophages immunology, Macrophages metabolism, Macrophages pathology, Male, Mesothelioma, Malignant genetics, Mesothelioma, Malignant immunology, Mesothelioma, Malignant metabolism, Monocytes immunology, Monocytes metabolism, Monocytes pathology, Pleural Effusion immunology, Pleural Effusion metabolism, Pleural Neoplasms genetics, Pleural Neoplasms immunology, Pleural Neoplasms metabolism, Prognosis, Receptors, Granulocyte-Macrophage Colony-Stimulating Factor genetics, Survival Rate, T-Lymphocytes, Cytotoxic immunology, Tumor Microenvironment immunology, Biomarkers, Tumor metabolism, Interleukins metabolism, Macrophage Colony-Stimulating Factor metabolism, Mesothelioma, Malignant pathology, Pleural Effusion pathology, Pleural Neoplasms pathology, Receptors, Granulocyte-Macrophage Colony-Stimulating Factor metabolism
Abstract

Background: Malignant pleural mesothelioma (MPM) is a rare and aggressive cancer related to asbestos exposure. The tumor microenvironment content, particularly the presence of macrophages, was described as crucial for the development of the disease. This work aimed at studying the involvement of the M-CSF (CSF-1)/IL-34/CSF-1R pathway in the formation of macrophages in MPM, using samples from patients., Methods: Pleural effusions (PEs), frozen tumors, primary MPM cells and MPM cell lines used in this study belong to biocollections associated with clinical databases. Cytokine expressions were studied using real-time PCR and ELISA. The Cancer Genome Atlas database was used to confirm our results on an independent cohort. An original three-dimensional (3D) coculture model including MPM cells, monocytes from healthy donors and a tumor antigen-specific cytotoxic CD8 T cell clone was used., Results: We observed that high interleukin (IL)-34 levels in PE were significantly associated with a shorter survival of patients. In tumors, expression of CSF1 was correlated with 'M2-like macrophages' markers, whereas this was not the case with IL34 expression, suggesting two distinct modes of action of these cytokines. Expression of IL34 was higher in MPM cells compared with primary mesothelial cells. Particularly, high expression of IL34 was observed in MPM cells with an alteration of CDKN2A . Finally, using 3D coculture model, we demonstrated the direct involvement of MPM cells in the formation of immunosuppressive macrophages, through activation of the colony stimulating factor-1 receptor (CSF1-R) pathway, causing the inhibition of cytotoxicity of tumor antigen-specific CD8 + T cells., Conclusions: The M-CSF/IL-34/CSF-1R pathway seems strongly implicated in MPM and could constitute a therapeutic target to act on immunosuppression and to support immunotherapeutic strategies., Competing Interests: Competing interests: None declared., (© Author(s) (or their employer(s)) 2020. Re-use permitted under CC BY-NC. No commercial re-use. See rights and permissions. Published by BMJ.)

Published
2020
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