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Respiratory Syncytial Virus Infects Regulatory B Cells in Human Neonates via Chemokine Receptor CX3CR1 and Promotes Lung Disease Severity

Title: Respiratory Syncytial Virus Infects Regulatory B Cells in Human Neonates via Chemokine Receptor CX3CR1 and Promotes Lung Disease Severity
Authors: Zhivaki, Dania; Lemoine, Sébastien; Lim, Annick; Morva, Ahsen; Vidalain, Pierre-Olivier; Schandene, Liliane; Casartelli, Nicoletta; Rameix-Welti, Marie-Anne; Hervé, Pierre-Louis; Dériaud, Edith; Beitz, Benoit; Ripaux-Lefevre, Maryline; Miatello, Jordi; Lemercier, Brigitte; Lorin, Valerie; Descamps, Delphyne; Fix, Jenna; Éléouët, Jean-François; Riffault, Sabine; Schwartz, Olivier; Porcheray, Fabrice; Mascart, Françoise; Mouquet, Hugo; Zhang, Xiaoming; Tissières, Pierre; Lo-Man, Richard
Contributors: Histopathologie humaine et Modèles animaux; Institut Pasteur Paris (IP); Université Paris Diderot - Paris 7 (UPD7); Régulation Immunitaire et Vaccinologie; Institut Pasteur Paris (IP)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Paris-Est Créteil Val-de-Marne - Paris 12 (UPEC UP12); Département d'Immunologie - Department of Immunology; Génomique virale et vaccination; Institut Pasteur Paris (IP)-Centre National de la Recherche Scientifique (CNRS); Hôpital Erasme = Erasmus Hospital = Erasmus Ziekenhuis (HUB-ULB); Virus et Immunité - Virus and immunity (CNRS-UMR3569); Infection et inflammation (2I); Université de Versailles Saint-Quentin-en-Yvelines (UVSQ)-Institut National de la Santé et de la Recherche Médicale (INSERM); Hôpital Ambroise Paré AP-HP; Assistance publique - Hôpitaux de Paris (AP-HP) (AP-HP); Unité de recherche Virologie et Immunologie Moléculaires (VIM (UR 0892)); Institut National de la Recherche Agronomique (INRA); BIOASTER Microbiology Technology Institute Lyon; Université Paris-Sud - Paris 11 (UP11); Rétrovirus endogènes et éléments rétroïdes des eucaryotes supérieurs (UMR 9196); Université Paris-Sud - Paris 11 (UP11)-Institut Gustave Roussy (IGR)-Centre National de la Recherche Scientifique (CNRS); Hôpital Bicêtre AP-HP, Le Kremlin-Bicêtre; Réponse humorale aux pathogènes; Institut Pasteur Paris (IP)-Institut National de la Santé et de la Recherche Médicale (INSERM); Université libre de Bruxelles = Free University of Brussels (ULB); Institut Pasteur de Shanghai, Académie des Sciences de Chine - Chinese Academy of Sciences (IPS-CAS); Pasteur Network (Réseau International des Instituts Pasteur); This work was supported by an ANR grant (ANR 13-BSV3-0016) and by the Fondation pour la Recherche Médicale (grant no. DEQ20120323719). This study also received funding from the French Government’s Investissement d’Avenir program, Laboratoire d’Excellence “Integrative Biology of Emerging Infectious Diseases” (grant no. ANR-10-LABX-62-IBEID). X.Z. and S.L. were supported by ANR and by the European Commission FP7 ADITEC program (HEALTH-F4-2011-280873). X.Z. was also partially supported by the Major Basic Research Project of Shanghai Science and Technology Commission (no. 13JC1405600); National Natural Science Foundation of China (31270961, 31470879); Interdisciplinary Innovation Team and External Cooperation Program (no. GJHZ201312); and Chinese Academy of Sciences. D.Z. was supported by DIM Malinf of Region IdF. Work in the O.S. lab is also supported by ANRS, Sidaction and Fondation Areva.; ANR-13-BSV3-0016,SyncBreg,Signature moléculaire et fonction des lymphocytes B régulateurs dans l'infection VRS(2013); ANR-10-LABX-0062,IBEID,Integrative Biology of Emerging Infectious Diseases(2010); European Project: 280873,FP7-HEALTH-2011-single-stage,FP7-HEALTH-2011-single-stage,ADITEC(2011)
Source: ISSN: 1074-7613 ; Immunity ; https://hal.science/hal-04635836 ; Immunity, 2017, 46 (2), pp.301-314. ⟨10.1016/j.immuni.2017.01.010⟩.
Publisher Information: CCSD; Elsevier
Publication Year: 2017
Collection: Université de Versailles Saint-Quentin-en-Yvelines: HAL-UVSQ
Subject Terms: newborn; bronchiolitis; respiratory syncytial virus; Breg cell; [SDV.MHEP.MI]Life Sciences [q-bio]/Human health and pathology/Infectious diseases; [SDV.IMM.IA]Life Sciences [q-bio]/Immunology/Adaptive immunology; [SDV.MHEP.PED]Life Sciences [q-bio]/Human health and pathology/Pediatrics; [SDV.MHEP.PSR]Life Sciences [q-bio]/Human health and pathology/Pulmonology and respiratory tract; [SDV.MP.VIR]Life Sciences [q-bio]/Microbiology and Parasitology/Virology
Description: International audience ; Respiratory syncytial virus (RSV) is the major cause of lower respiratory tract infections in infants and is characterized by pulmonary infiltration of B cells in fatal cases. We analyzed the B cell compartment in human newborns and identified a population of neonatal regulatory B lymphocytes (nBreg cells) that produced interleukin 10 (IL-10) in response to RSV infection. The polyreactive B cell receptor of nBreg cells interacted with RSV protein F and induced upregulation of chemokine receptor CX3CR1. CX3CR1 interacted with RSV glycoprotein G, leading to nBreg cell infection and IL-10 production that dampened T helper 1 (Th1) cytokine production. In the respiratory tract of neonates with severe RSV-induced acute bronchiolitis, RSV-infected nBreg cell frequencies correlated with increased viral load and decreased blood memory Th1 cell frequencies. Thus, the frequency of nBreg cells is predictive of the severity of acute bronchiolitis disease and nBreg cell activity may constitute an early-life host response that favors microbial pathogenesis
Document Type: article in journal/newspaper
Language: English
Relation: info:eu-repo/semantics/altIdentifier/pmid/28228284; info:eu-repo/grantAgreement//280873/EU/Advanced Immunization Technologies/ADITEC; PUBMED: 28228284; PUBMEDCENTRAL: PMC7128247
DOI: 10.1016/j.immuni.2017.01.010
Availability: https://hal.science/hal-04635836; https://hal.science/hal-04635836v1/document; https://hal.science/hal-04635836v1/file/IMMUNITY-D-16-00286_R4.1.pdf; https://doi.org/10.1016/j.immuni.2017.01.010
Rights: info:eu-repo/semantics/OpenAccess
Accession Number: edsbas.B2DA7A9C
Database: BASE