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Influenza infection rewires energy metabolism and induces browning features in adipose cells and tissues

Title: Influenza infection rewires energy metabolism and induces browning features in adipose cells and tissues
Authors: Ayari, Asma; Rosa-Calatrava, Manuel; Lancel, Steve; Barthelemy, Johanna; Pizzorno, Andrés; Mayeuf-Louchart, Alicia; Baron, Morgane; Hot, David; Deruyter, Lucie; Soulard, Daphnée; Julien, Thomas; Faveeuw, Christelle; Molendi-Coste, Olivier; Dombrowicz, David; Sedano, Laura; Sencio, Valentin; Le Goffic, Ronan; Trottein, François; Wolowczuk, Isabelle
Contributors: Centre d’Infection et d’Immunité de Lille - INSERM U 1019 - UMR 9017 - UMR 8204 (CIIL); Centre National de la Recherche Scientifique (CNRS)-Centre Hospitalier Régional Universitaire Lille (CHRU Lille)-Université de Lille-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut Pasteur de Lille; Réseau International des Instituts Pasteur (RIIP)-Réseau International des Instituts Pasteur (RIIP); Virpath-Grippe, de l'émergence au contrôle -- Virpath-Influenza, from emergence to control (Virpath); Centre International de Recherche en Infectiologie - UMR (CIRI); École normale supérieure - Lyon (ENS Lyon)-Université Claude Bernard Lyon 1 (UCBL); Université de Lyon-Université de Lyon-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-École normale supérieure - Lyon (ENS Lyon)-Université Claude Bernard Lyon 1 (UCBL); Université de Lyon-Université de Lyon-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS); Récepteurs nucléaires, maladies cardiovasculaires et diabète - U 1011 (RNMCD); Institut Pasteur de Lille; Réseau International des Instituts Pasteur (RIIP)-Réseau International des Instituts Pasteur (RIIP)-Université de Lille-Centre Hospitalier Régional Universitaire Lille (CHRU Lille)-Institut National de la Santé et de la Recherche Médicale (INSERM); Virologie et Immunologie Moléculaires (VIM (UR 0892)); Université de Versailles Saint-Quentin-en-Yvelines (UVSQ)-Université Paris-Saclay-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE); The CPER-Région Hauts-de-France’s financial contribution to the acquisition of the Oroboros O2k-respirometer is acknowledged. This study was supported by the Centre National de la Recherche Scientifique (CNRS) and the Institut National de la Santé et de la Recherche Médicale (INSERM). AA received a grant from Lille University. I.W. and F.T. received a grant from CNRS.; We appreciate valuable discussions with Drs. Kassem Makki and Sandra Weller, and advice and support from Drs. Jean-Claude Sirard and Jean Dubuisson, and from Sia Praline and Nor Snø. We thank Dr. Corinne Grangette for providing reagents needed for mouse preadipocyte and adipocyte culture and differentiation, Dr. Odile Poulain-Godefroy for the kind gift of human primary Preadipocytes, and Marie-Josée Ghoris for technical help. Jérôme Lecardonnel (INRA, UMR GABI, Jouy-en-Josas, France) and Marie-Hélène Gevaert (Laboratoire d’Histologie, Faculté de Médecine, Lille, France) are acknowledged for their expert technical assistance in, respectively, microarray hybridization (adipose cells) and WAT histology. We also thank Denis Ressnikoff and Elisabeth Erazzuriz (Centre Imagerie Quantitative Lyon Est (CIQLE), Université Lyon 1, Lyon, France) for their technical assistance in confocal and transmission electron microscopy. We thank Antonino Bongiovanni and Sophie Salomé-Desnoulez as well as Drs. Elizabeth Werkmeister, Nicolas Barois and Hélène Bauderlique of the BioImaging Center Lille (BICeL, Lille, France) for access to systems and expert advises on microscopy and flow cytometry. Dr. Cécile Lecoeur and Peggy Bouquet (Transcriptomics and Applied Genomics Group, Lille) are thanked for, respectively, advice on transcriptomic analyses, and technical assistance in microarray hybridization (adipose tissues). Institut Pasteur’s animal facility staff is also thanked for its assistance.
Source: ISSN: 2399-3642 ; Communications Biology ; https://hal.archives-ouvertes.fr/hal-02959942 ; Communications Biology, Nature Publishing Group, 2020, 3 (1), ⟨10.1038/s42003-020-0965-6⟩.
Publisher Information: HAL CCSD; Nature Publishing Group
Publication Year: 2020
Collection: Archive ouverte HAL (Hyper Article en Ligne, CCSD - Centre pour la Communication Scientifique Directe)
Subject Terms: [SDV.MP.VIR]Life Sciences [q-bio]/Microbiology and Parasitology/Virology
Description: International audience ; Like all obligate intracellular pathogens, influenza A virus (IAV) reprograms host cell’s glucose and lipid metabolism to promote its own replication. However, the impact of influenza infection on white adipose tissue (WAT), a key tissue in the control of systemic energy homeostasis, has not been yet characterized. Here, we show that influenza infection induces alterations in whole-body glucose metabolism that persist long after the virus has been cleared. We report depot-specific changes in the WAT of IAV-infected mice, notably characterized by the appearance of thermogenic brown-like adipocytes within the subcutaneous fat depot. Importantly, viral RNA- and viral antigen-harboring cells are detected in the WAT of infected mice. Using in vitro approaches, we find that IAV infection enhances the expression of brown-adipogenesis-related genes in preadipocytes. Overall, our findings shed light on the role that the white adipose tissue, which lies at the crossroads of nutrition, metabolism and immunity, may play in influenza infection.
Document Type: article in journal/newspaper
Language: English
Relation: info:eu-repo/semantics/altIdentifier/pmid/32409640; hal-02959942; https://hal.archives-ouvertes.fr/hal-02959942; https://hal.archives-ouvertes.fr/hal-02959942v2/document; https://hal.archives-ouvertes.fr/hal-02959942v2/file/s42003-020-0965-6.pdf; PUBMED: 32409640; PUBMEDCENTRAL: PMC7224208; WOS: 000618915300002
DOI: 10.1038/s42003-020-0965-6
Availability: https://hal.archives-ouvertes.fr/hal-02959942; https://hal.archives-ouvertes.fr/hal-02959942v2/document; https://hal.archives-ouvertes.fr/hal-02959942v2/file/s42003-020-0965-6.pdf; https://doi.org/10.1038/s42003-020-0965-6
Rights: http://creativecommons.org/licenses/by/ ; info:eu-repo/semantics/OpenAccess
Accession Number: edsbas.715D3EE1
Database: BASE