Vaccine breakthrough hypoxemic COVID-19 pneumonia in patients with auto-Abs neutralizing type I IFNs
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- Paul Bastard
- Laboratory of Human Genetics of Infectious Diseases, Necker Branch, INSERM U1163, Necker Hospital for Sick Children, Paris, France.
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- Sara E. Vazquez
- Medical Scientist Training Program, University of California, San Francisco, San Francisco, CA 94143, USA.
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- Jamin Liu
- Department of Biochemistry and Biophysics, University of California, San Francisco, San Francisco, CA 94158, USA.
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- Matthew T. Laurie
- Department of Biochemistry and Biophysics, University of California, San Francisco, San Francisco, CA 94158, USA.
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- Chung Yu Wang
- Chan Zuckerberg Biohub, San Francisco, CA 94158, USA.
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- Adrian Gervais
- Laboratory of Human Genetics of Infectious Diseases, Necker Branch, INSERM U1163, Necker Hospital for Sick Children, Paris, France.
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- Tom Le Voyer
- Laboratory of Human Genetics of Infectious Diseases, Necker Branch, INSERM U1163, Necker Hospital for Sick Children, Paris, France.
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- Lucy Bizien
- Laboratory of Human Genetics of Infectious Diseases, Necker Branch, INSERM U1163, Necker Hospital for Sick Children, Paris, France.
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- Colin Zamecnik
- Weill Institute for Neurosciences, Department of Neurology, University of California, San Francisco, San Francisco, CA, USA.
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- Quentin Philippot
- Laboratory of Human Genetics of Infectious Diseases, Necker Branch, INSERM U1163, Necker Hospital for Sick Children, Paris, France.
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- Jérémie Rosain
- Laboratory of Human Genetics of Infectious Diseases, Necker Branch, INSERM U1163, Necker Hospital for Sick Children, Paris, France.
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- Emilie Catherinot
- Pneumology Department, Foch Hospital, Suresne, France.
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- Andrew Willmore
- Chan Zuckerberg Biohub, San Francisco, CA 94158, USA.
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- Anthea M. Mitchell
- Chan Zuckerberg Biohub, San Francisco, CA 94158, USA.
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- Rebecca Bair
- Weill Institute for Neurosciences, Department of Neurology, University of California, San Francisco, San Francisco, CA, USA.
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- Pierre Garçon
- Intensive Care Unit, Grand Hôpital de l'Est Francilien Site de Marne-la-Vallée, Jossigny, France.
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- Heather Kenney
- Laboratory of Clinical Immunology and Microbiology, Division of Intramural Research, NIAID, NIH, Bethesda, MD, USA.
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- Arnaud Fekkar
- Laboratory of Human Genetics of Infectious Diseases, Necker Branch, INSERM U1163, Necker Hospital for Sick Children, Paris, France.
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- Maria Salagianni
- Laboratory of Immunobiology, Center for Clinical, Experimental Surgery and Translational Research, Biomedical Research Foundation of the Academy of Athens, Athens, Greece.
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- Garyphallia Poulakou
- 3rd Department of Internal Medicine, National and Kapodistrian University of Athens, Medical School, “Sotiria” General Hospital of Chest Diseases, Athens, Greece.
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- Eleni Siouti
- Laboratory of Immunobiology, Center for Clinical, Experimental Surgery and Translational Research, Biomedical Research Foundation of the Academy of Athens, Athens, Greece.
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- Sabina Sahanic
- Department of Internal Medicine II, Medical University of Innsbruck, Innsbruck, Austria.
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- Ivan Tancevski
- Department of Internal Medicine II, Medical University of Innsbruck, Innsbruck, Austria.
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- Günter Weiss
- Department of Internal Medicine II, Medical University of Innsbruck, Innsbruck, Austria.
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- Laurenz Nagl
- Department of Internal Medicine V, Medical University of Innsbruck, Innsbruck, Austria.
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- Jérémy Manry
- Laboratory of Human Genetics of Infectious Diseases, Necker Branch, INSERM U1163, Necker Hospital for Sick Children, Paris, France.
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- Sotirija Duvlis
- Faculty of Medical Sciences, University “Goce Delchev”, Stip, Republic of North Macedonia.
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- Daniel Arroyo-Sánchez
- Department of Immunology, Instituto de Investigación Sanitaria Hospital 12 de Octubre (imas12) and Department of Immunology, Ophthalmology and ENT, Complutense University School of Medicine, CIBERINFEC, Madrid, Spain.
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- Estela Paz Artal
- Department of Immunology, Instituto de Investigación Sanitaria Hospital 12 de Octubre (imas12) and Department of Immunology, Ophthalmology and ENT, Complutense University School of Medicine, CIBERINFEC, Madrid, Spain.
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- Luis Rubio
- Department of Biochemistry and Biophysics, University of California, San Francisco, San Francisco, CA 94158, USA.
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- Cristiano Perani
- Emergency Room, ASST Spedali Civili di Brescia, Brescia, Italy.
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- Michela Bezzi
- Covid Unit, ASST Spedali Civili, Brescia, Italy.
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- Alessandra Sottini
- CREA Laboratory, Diagnostic Department, ASST Spedali Civili di Brescia, Brescia, Italy.
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- Virginia Quaresima
- CREA Laboratory, Diagnostic Department, ASST Spedali Civili di Brescia, Brescia, Italy.
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- Lucie Roussel
- Department of Medicine, Division of Infectious Diseases, McGill University Health Centre, Montréal, Québec, Canada.
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- Donald C. Vinh
- Department of Medicine, Division of Infectious Diseases, McGill University Health Centre, Montréal, Québec, Canada.
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- Luis Felipe Reyes
- Department of Microbiology, Universidad de La Sabana, Chía, Colombia.
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- Margaux Garzaro
- Department of Infectious Diseases, Necker Hospital for Sick Children, AP-HP, Paris, France.
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- Nevin Hatipoglu
- Pediatric Infectious Diseases Unit, Bakirkoy Dr. Sadi Konuk Training and Research Hospital, University of Health Sciences, Istanbul, Turkey.
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- David Boutboul
- Department of Immunology, Saint-Louis Hospital, AP-HP, Paris, France.
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- Yacine Tandjaoui-Lambiotte
- INSERM UMR 1137 IAME, Paris, France.
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- Alessandro Borghesi
- Neonatal Intensive Care Unit, Fondazione IRCCS Policlinico San Matteo, Pavia, Italy.
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- Anna Aliberti
- Anesthesia and Intensive Care, Rianimazione I, Fondazione IRCCS Policlinico San Matteo, Pavia, Italy.
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- Irene Cassaniti
- Microbiology and Virology Department, Fondazione IRCCS Policlinico San Matteo, Pavia, Italy.
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- Fabienne Venet
- Laboratoire d’Immunologie, Hospices Civils de Lyon, Hôpital Edouard Herriot, Lyon, France.
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- Guillaume Monneret
- Laboratoire d’Immunologie, Hospices Civils de Lyon, Hôpital Edouard Herriot, Lyon, France.
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- Rabih Halwani
- Sharjah Institute for Medical Research, College of Medicine, University of Sharjah, Sharjah, United Arab Emirates.
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- Narjes Saheb Sharif-Askari
- Sharjah Institute for Medical Research, College of Medicine, University of Sharjah, Sharjah, United Arab Emirates.
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- Jeffrey Danielson
- Laboratory of Clinical Immunology and Microbiology, Division of Intramural Research, NIAID, NIH, Bethesda, MD, USA.
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- Sonia Burrel
- Sorbonne Université, INSERM U1136, Institut Pierre Louis d'Epidémiologie et de Santé Publique (iPLESP), AP-HP, Hôpital Pitié Salpêtrière, Service de Virologie, Paris, France.
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- Caroline Morbieu
- Internal Medicine Department, Louis Mourier Hospital, AP-HP, Paris, France.
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- Yurii Stepanovskyy
- Shupyk National Healthcare University of Ukraine, Kyiv, Ukraine.
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- Anastasia Bondarenko
- Shupyk National Healthcare University of Ukraine, Kyiv, Ukraine.
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- Alla Volokha
- Shupyk National Healthcare University of Ukraine, Kyiv, Ukraine.
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- Oksana Boyarchuk
- Department of Children’s Diseases and Pediatric Surgery, I. Horbachevsky Ternopil National Medical University, Ternopil, Ukraine.
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- Alenka Gagro
- Department of Pediatrics, Children’s Hospital Zagreb, University of Zagreb School of Medicine, Zagreb, Josip Juraj Strossmayer University of Osijek, Medical Faculty Osijek, Osijek, Croatia.
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- Mathilde Neuville
- Intensive Care Unit, Foch Hospital, Suresnes, France.
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- Bénédicte Neven
- Department of Pediatrics Hematology Immunology and Rheumatology, Necker Hospital for Sick Children, AP-HP, Paris, France.
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- Sevgi Keles
- Meram Medical Faculty, Necmettin Erbakan University, Konya, Turkey.
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- Romain Hernu
- Service des Urgences, Groupement Hospitalier Nord, Hospices Civils de Lyon, Lyon, France.
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- Antonin Bal
- Laboratoire de virologie, Institut Agent Infectieux, Groupement Hospitalier Nord, Hospices Civils de Lyon, Lyon, France.
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- Antonio Novelli
- Laboratory of Medical Genetics, IRCCS Bambino Gesù Children’s Hospital, Rome, Italy.
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- Giuseppe Novelli
- Department of Biomedicine and Prevention, Tor Vergata University of Rome, Rome, Italy.
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- Kahina Saker
- Joint Research Unit, Hospices Civils de Lyon-bio Mérieux, Hospices Civils de Lyon, Lyon Sud Hospital, Pierre-Bénite, France; and International Center of Research in Infectiology, Lyon University, INSERM U1111, CNRS UMR 5308, ENS, UCBL, Lyon, France.
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- Oana Ailioaie
- Service de Génétique, Hôpital Raymond Poincaré, AP-HP, Garches, France.
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- Arnau Antolí
- Department of Internal Medicine, Hospital Universitari de Bellvitge, IDIBELL, Barcelona, Spain.
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- Eric Jeziorski
- General Pediatric Department, PCCEI, CeRéMAIA, University of Montpellier, CHU Montpellier, Montpellier, France.
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- Gemma Rocamora-Blanch
- Department of Internal Medicine, Hospital Universitari de Bellvitge, IDIBELL, Barcelona, Spain.
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- Carla Teixeira
- Unidade de Infeciologia e Imunodeficiências, Centro Materno-infantil do Norte, Centro Hospitalar Universitário do Porto, Porto, Portugal.
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- Clarisse Delaunay
- Department of Infectious Diseases, CHU Nantes, and INSERM UIC 1413, CHU, Nantes, France.
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- Marine Lhuillier
- Geriatric Department, CHU Nantes, Hopital Bellier, Nantes, France.
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- Paul Le Turnier
- Department of Infectious Diseases, CHU Nantes, and INSERM UIC 1413, CHU, Nantes, France.
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- Yu Zhang
- Laboratory of Clinical Immunology and Microbiology, Division of Intramural Research, NIAID, NIH, Bethesda, MD, USA.
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- Matthieu Mahevas
- Necker Enfants Malades Institute (INEM), INSERM U1151/CNRS UMR 8253, University of Paris Cité, Paris, France.
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- Qiang Pan-Hammarström
- Department of Biosciences and Nutrition, Karolinska Institutet, SE14183 Huddinge, Sweden.
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- Hassan Abolhassani
- Department of Biosciences and Nutrition, Karolinska Institutet, SE14183 Huddinge, Sweden.
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- Thierry Bompoil
- Biologie/Pathologie, CHU-Nantes–Hôtel Dieu, Institut de Biologie, Nantes, France.
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- Karim Dorgham
- Sorbonne Université, Inserm, Centre d’Immunologie et des Maladies Infectieuses, (CIMI-Paris), Paris, France.
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- Guy Gorochov
- Sorbonne Université, Inserm, Centre d’Immunologie et des Maladies Infectieuses, (CIMI-Paris), Paris, France.
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- Cédric Laouenan
- INSERM UMR 1137 IAME, Paris, France.
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- Carlos Rodríguez-Gallego
- Department of Clinical Sciences, University Fernando Pessoa Canarias, Las Palmas de Gran Canaria, Canary Islands, Spain.
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- Lisa F. P. Ng
- A*STAR Infectious Disease Labs, Agency for Science, Technology and Research, Singapore, Singapore.
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- Laurent Renia
- A*STAR Infectious Disease Labs, Agency for Science, Technology and Research, Singapore, Singapore.
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- Aurora Pujol
- Neurometabolic Diseases Laboratory, IDIBELL-Hospital Duran i Reynals, CIBERER U759, and Catalan Institution of Research and Advanced Studies (ICREA), Barcelona, Spain.
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- Alexandre Belot
- Joint Research Unit, Hospices Civils de Lyon-bio Mérieux, Hospices Civils de Lyon, Lyon Sud Hospital, Pierre-Bénite, France; and International Center of Research in Infectiology, Lyon University, INSERM U1111, CNRS UMR 5308, ENS, UCBL, Lyon, France.
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- François Raffi
- Department of Infectious Diseases, CHU Nantes, and INSERM UIC 1413, CHU, Nantes, France.
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- Luis M. Allende
- Department of Immunology, Instituto de Investigación Sanitaria Hospital 12 de Octubre (imas12) and Department of Immunology, Ophthalmology and ENT, Complutense University School of Medicine, CIBERINFEC, Madrid, Spain.
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- Javier Martinez-Picado
- IrsiCaixa AIDS Research Institute and Institute for Health Science Research Germans Trias i Pujol (IGTP), Badalona, Spain.
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- Tayfun Ozcelik
- Department of Molecular Biology and Genetics, Bilkent University, Ankara, Turkey.
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- Luisa Imberti
- CREA Laboratory, Diagnostic Department, ASST Spedali Civili di Brescia, Brescia, Italy.
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- Luigi D. Notarangelo
- Laboratory of Clinical Immunology and Microbiology, Division of Intramural Research, NIAID, NIH, Bethesda, MD, USA.
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- Jesus Troya
- Department of Internal Medicine, Infanta Leonor University Hospital, Madrid, Spain.
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- Xavier Solanich
- Department of Internal Medicine, Hospital Universitari de Bellvitge, IDIBELL, Barcelona, Spain.
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- Shen-Ying Zhang
- Laboratory of Human Genetics of Infectious Diseases, Necker Branch, INSERM U1163, Necker Hospital for Sick Children, Paris, France.
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- Anne Puel
- Laboratory of Human Genetics of Infectious Diseases, Necker Branch, INSERM U1163, Necker Hospital for Sick Children, Paris, France.
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- Michael R. Wilson
- Weill Institute for Neurosciences, Department of Neurology, University of California, San Francisco, San Francisco, CA, USA.
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- Sophie Trouillet-Assant
- Hospices Civils de Lyon, Lyon, France; and International Center of Research in Infectiology, Lyon University, INSERM U1111, CNRS UMR 5308, ENS, UCBL, Lyon, France.
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- Laurent Abel
- Laboratory of Human Genetics of Infectious Diseases, Necker Branch, INSERM U1163, Necker Hospital for Sick Children, Paris, France.
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- Emmanuelle Jouanguy
- Laboratory of Human Genetics of Infectious Diseases, Necker Branch, INSERM U1163, Necker Hospital for Sick Children, Paris, France.
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- Chun Jimmie Ye
- Chan Zuckerberg Biohub, San Francisco, CA 94158, USA.
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- Aurélie Cobat
- Laboratory of Human Genetics of Infectious Diseases, Necker Branch, INSERM U1163, Necker Hospital for Sick Children, Paris, France.
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- Leslie M. Thompson
- Departments of Psychiatry and Human Behavior and Neurobiology and Behavior, University of California, Irvine, Irvine, CA, USA.
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- Evangelos Andreakos
- Laboratory of Immunobiology, Center for Clinical, Experimental Surgery and Translational Research, Biomedical Research Foundation of the Academy of Athens, Athens, Greece.
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- Qian Zhang
- Laboratory of Human Genetics of Infectious Diseases, Necker Branch, INSERM U1163, Necker Hospital for Sick Children, Paris, France.
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- Mark S. Anderson
- Diabetes Center, University of California, San Francisco, San Francisco, CA 94143, USA.
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- Jean-Laurent Casanova
- Laboratory of Human Genetics of Infectious Diseases, Necker Branch, INSERM U1163, Necker Hospital for Sick Children, Paris, France.
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- Joseph L. DeRisi
- Department of Biochemistry and Biophysics, University of California, San Francisco, San Francisco, CA 94158, USA.
抄録
<jats:p>Life-threatening “breakthrough” cases of critical COVID-19 are attributed to poor or waning antibody (Ab) response to SARS-CoV-2 vaccines in individuals already at risk. Preexisting auto-Abs neutralizing type I IFNs underlie at least 15% of critical COVID-19 pneumonia cases in unvaccinated individuals; their contribution to hypoxemic breakthrough cases in vaccinated people is unknown. We studied a cohort of 48 individuals (aged 20 to 86 years) who received two doses of a messenger RNA (mRNA) vaccine and developed a breakthrough infection with hypoxemic COVID-19 pneumonia 2 weeks to 4 months later. Ab levels to the vaccine, neutralization of the virus, and auto-Abs to type I IFNs were measured in the plasma. Forty-two individuals had no known deficiency of B cell immunity and a normal Ab response to the vaccine. Among them, 10 (24%) had auto-Abs neutralizing type I IFNs (aged 43 to 86 years). Eight of these 10 patients had auto-Abs neutralizing both IFN-α2 and IFN-ω, whereas two neutralized IFN-ω only. No patient neutralized IFN-β. Seven neutralized type I IFNs at 10 ng/ml and three at 100 pg/ml only. Seven patients neutralized SARS-CoV-2 D614G and Delta efficiently, whereas one patient neutralized Delta slightly less efficiently. Two of the three patients neutralizing only type I IFNs at 100 pg/ml neutralized both D614G and Delta less efficiently. Despite two mRNA vaccine inoculations and the presence of circulating Abs capable of neutralizing SARS-CoV-2, auto-Abs neutralizing type I IFNs may underlie a notable proportion of hypoxemic COVID-19 pneumonia cases, highlighting the importance of this particularly vulnerable population.</jats:p>
収録刊行物
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- Science Immunology
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Science Immunology 8 (90), 2023-12-22
American Association for the Advancement of Science (AAAS)