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

Autor: Pierre Tissieres, Benoit Beitz, Jean-François Eléouët, Maryline M Ripaux-Lefevre, Delphyne Descamps, Fabrice Porcheray, Marie-Anne Rameix-Welti, Sébastien Lemoine, Nicoletta Casartelli, Jenna Fix, Richard Lo-Man, Valérie Lorin, Sabine Riffault, Ahsen Morva, Hugo Mouquet, Pierre-Louis Hervé, Françoise Mascart, Liliane Schandené, Jordi Miatello, Dania Zhivaki, Pierre-Olivier Vidalain, Edith Dériaud, Brigitte Lemercier, Xiaoming X Zhang, Olivier Schwartz, Annick Lim
Přispěvatelé: Histopathologie humaine et Modèles animaux, Institut Pasteur [Paris], Université Paris Diderot - Paris 7 (UPD7), Régulation Immunitaire et Vaccinologie, Université Paris-Est Créteil Val-de-Marne - Paris 12 (UPEC UP12)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut Pasteur [Paris], Département d'Immunologie - Department of Immunology, Génomique virale et vaccination, Institut Pasteur [Paris]-Centre National de la Recherche Scientifique (CNRS), Immunobiology Clinic, Hôpital Erasme [Bruxelles] (ULB), Faculté de Médecine [Bruxelles] (ULB), Université libre de Bruxelles (ULB)-Université libre de Bruxelles (ULB)-Faculté de Médecine [Bruxelles] (ULB), Université libre de Bruxelles (ULB)-Université libre de Bruxelles (ULB), Virus et Immunité - Virus and immunity, Infection et inflammation (2I), Université de Versailles Saint-Quentin-en-Yvelines (UVSQ)-Institut National de la Santé et de la Recherche Médicale (INSERM), Université de Versailles Saint-Quentin-en-Yvelines (UVSQ), Laboratoire de Microbiologie, Hôpital Raymond Poincareé, Unité de recherche Virologie et Immunologie Moléculaires (VIM (UR 0892)), Institut National de la Recherche Agronomique (INRA), Université Paris-Saclay, Microbiology Technology Institute, BIOASTER Microbiology Technology Institute [Lyon], School of Medicine, University of Patras [Greece], UMR9196, Physiologie et Pathologie Moléculaires des Rétrovirus Endogènes et Infectieux, Centre National de la Recherche Scientifique (CNRS), APHP, Pediatric ICU and Neonatal Medicine, Hôpitaux Universitaires Paris Sud, Réponse humorale aux pathogènes, Institut Pasteur [Paris]-Institut National de la Santé et de la Recherche Médicale (INSERM), Laboratory of Vaccinology and Mucosal Immunity, Université libre de Bruxelles (ULB), Institut Pasteur de Shanghai, Académie des Sciences de Chine - Chinese Academy of Sciences (IPS-CAS), Réseau International des Instituts Pasteur (RIIP), 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. We acknowledge the Center for Human Immunology at Institut Pasteur for support in conducting these studies., We are very grateful to T. Domet (Therapie Cellulaire, Hopital Saint-Louis) for the cord blood sample collection and M. Lucas-Hourani for some viral preparation. We thank F. Huetz for helpful discussion about B lymphocytes., 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,EC:FP7:HEALTH,FP7-HEALTH-2011-single-stage,ADITEC(2011), Institut Pasteur [Paris] (IP), 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), Institut Pasteur [Paris] (IP)-Centre National de la Recherche Scientifique (CNRS), Virus et Immunité - Virus and immunity (CNRS-UMR3569), University of Patras, Physiologie et physiopathologie des rétrovirus endogènes et infectieux (RETRO-ENDO), Institut Gustave Roussy (IGR)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS), Hôpitaux Universitaires Paris Sud [AP-HP] (HUPS), Institut Pasteur [Paris] (IP)-Institut National de la Santé et de la Recherche Médicale (INSERM), Institut Pasteur [Paris]-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Paris-Est Créteil Val-de-Marne - Paris 12 (UPEC UP12), Centre National de la Recherche Scientifique (CNRS)-Institut Pasteur [Paris], Hôpital Erasme, Virus et Immunité, Infection et inflammation chronique (2I), Institut National de la Santé et de la Recherche Médicale (INSERM)-Université de Versailles Saint-Quentin-en-Yvelines (UVSQ), Unité de recherche Virologie et Immunologie Moléculaires (VIM), BIOASTER, Université Libre de Bruxelles [Bruxelles] (ULB), ANR-10-LABX-62-IBEID,IBEID,Laboratoire d'Excellence 'Integrative Biology of Emerging Infectious Diseases'(2010), University of Patras [Patras]
Jazyk: angličtina
Rok vydání: 2017
Předmět:
CD4-Positive T-Lymphocytes
0301 basic medicine
Enzyme-Linked Immunospot Assay
Regulatory B cells
respiratory syncytial virus
[SDV]Life Sciences [q-bio]
Immunology
B-cell receptor
CX3C Chemokine Receptor 1
Enzyme-Linked Immunosorbent Assay
Respiratory Syncytial Virus Infections
Biology
Lymphocyte Activation
Article
03 medical and health sciences
Chemokine receptor
0302 clinical medicine
newborn
CX3CR1
medicine
Bronchiolitis
Viral

Humans
Immunology and Allergy
B cell
Oligonucleotide Array Sequence Analysis
B-Lymphocytes
Regulatory

Respiratory tract infections
Gene Expression Profiling
Infant
Newborn

medicine.disease
Virology
Respiratory Syncytial Viruses
3. Good health
Breg cell
Interleukin 10
030104 developmental biology
Infectious Diseases
medicine.anatomical_structure
Bronchiolitis
030220 oncology & carcinogenesis
[SDV.IMM]Life Sciences [q-bio]/Immunology
Receptors
Chemokine

bronchiolitis
Transcriptome
Zdroj: Immunity
Immunity, Elsevier, 2017, 46 (2), pp.301-314. ⟨10.1016/j.immuni.2017.01.010⟩
Immunity, 2017, 46 (2), pp.301-314. ⟨10.1016/j.immuni.2017.01.010⟩
ISSN: 1074-7613
DOI: 10.1016/j.immuni.2017.01.010⟩
Popis: 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.
Databáze: OpenAIRE