SARS-CoV-2 induces human plasmacytoid predendritic cell diversification via UNC93B and IRAK4
Several studies have analyzed antiviral immune pathways in late-stage severe COVID-19. However, the initial steps of SARS-CoV-2 antiviral immunity are poorly understood. Here we have isolated primary SARS-CoV-2 viral strains and studied their interaction with human plasmacytoid predendritic cells (p...
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| Published in | The Journal of experimental medicine Vol. 218; no. 4 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Rockefeller University Press
05.04.2021
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| Subjects | |
| Online Access | Get full text |
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| Abstract | Several studies have analyzed antiviral immune pathways in late-stage severe COVID-19. However, the initial steps of SARS-CoV-2 antiviral immunity are poorly understood. Here we have isolated primary SARS-CoV-2 viral strains and studied their interaction with human plasmacytoid predendritic cells (pDCs), a key player in antiviral immunity. We show that pDCs are not productively infected by SARS-CoV-2. However, they efficiently diversified into activated P1-, P2-, and P3-pDC effector subsets in response to viral stimulation. They expressed CD80, CD86, CCR7, and OX40 ligand at levels similar to influenza virus–induced activation. They rapidly produced high levels of interferon-α, interferon-λ1, IL-6, IP-10, and IL-8. All major aspects of SARS-CoV-2–induced pDC activation were inhibited by hydroxychloroquine. Mechanistically, SARS-CoV-2–induced pDC activation critically depended on IRAK4 and UNC93B1, as established using pDC from genetically deficient patients. Overall, our data indicate that human pDC are efficiently activated by SARS-CoV-2 particles and may thus contribute to type I IFN–dependent immunity against SARS-CoV-2 infection. |
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| AbstractList | Several studies have analyzed antiviral immune pathways in late-stage severe COVID-19. However, the initial steps of SARS-CoV-2 antiviral immunity are poorly understood. Here we have isolated primary SARS-CoV-2 viral strains and studied their interaction with human plasmacytoid predendritic cells (pDCs), a key player in antiviral immunity. We show that pDCs are not productively infected by SARS-CoV-2. However, they efficiently diversified into activated P1-, P2-, and P3-pDC effector subsets in response to viral stimulation. They expressed CD80, CD86, CCR7, and OX40 ligand at levels similar to influenza virus-induced activation. They rapidly produced high levels of interferon-α, interferon-λ1, IL-6, IP-10, and IL-8. All major aspects of SARS-CoV-2-induced pDC activation were inhibited by hydroxychloroquine. Mechanistically, SARS-CoV-2-induced pDC activation critically depended on IRAK4 and UNC93B1, as established using pDC from genetically deficient patients. Overall, our data indicate that human pDC are efficiently activated by SARS-CoV-2 particles and may thus contribute to type I IFN-dependent immunity against SARS-CoV-2 infection.Several studies have analyzed antiviral immune pathways in late-stage severe COVID-19. However, the initial steps of SARS-CoV-2 antiviral immunity are poorly understood. Here we have isolated primary SARS-CoV-2 viral strains and studied their interaction with human plasmacytoid predendritic cells (pDCs), a key player in antiviral immunity. We show that pDCs are not productively infected by SARS-CoV-2. However, they efficiently diversified into activated P1-, P2-, and P3-pDC effector subsets in response to viral stimulation. They expressed CD80, CD86, CCR7, and OX40 ligand at levels similar to influenza virus-induced activation. They rapidly produced high levels of interferon-α, interferon-λ1, IL-6, IP-10, and IL-8. All major aspects of SARS-CoV-2-induced pDC activation were inhibited by hydroxychloroquine. Mechanistically, SARS-CoV-2-induced pDC activation critically depended on IRAK4 and UNC93B1, as established using pDC from genetically deficient patients. Overall, our data indicate that human pDC are efficiently activated by SARS-CoV-2 particles and may thus contribute to type I IFN-dependent immunity against SARS-CoV-2 infection. Plasmacytoid dendritic cells (pDCs) are not permissive to SARS-CoV-2 infection but, upon viral exposure, differentiate into subsets and rapidly produce type I and III interferons. Mechanistically, pDC activation depends on IRAK4 and UNC93B1 expression. Several studies have analyzed antiviral immune pathways in late-stage severe COVID-19. However, the initial steps of SARS-CoV-2 antiviral immunity are poorly understood. Here we have isolated primary SARS-CoV-2 viral strains and studied their interaction with human plasmacytoid predendritic cells (pDCs), a key player in antiviral immunity. We show that pDCs are not productively infected by SARS-CoV-2. However, they efficiently diversified into activated P1-, P2-, and P3-pDC effector subsets in response to viral stimulation. They expressed CD80, CD86, CCR7, and OX40 ligand at levels similar to influenza virus–induced activation. They rapidly produced high levels of interferon-α, interferon-λ1, IL-6, IP-10, and IL-8. All major aspects of SARS-CoV-2–induced pDC activation were inhibited by hydroxychloroquine. Mechanistically, SARS-CoV-2–induced pDC activation critically depended on IRAK4 and UNC93B1, as established using pDC from genetically deficient patients. Overall, our data indicate that human pDC are efficiently activated by SARS-CoV-2 particles and may thus contribute to type I IFN–dependent immunity against SARS-CoV-2 infection. Several studies have analyzed antiviral immune pathways in late-stage severe COVID-19. However, the initial steps of SARS-CoV-2 antiviral immunity are poorly understood. Here we have isolated primary SARS-CoV-2 viral strains and studied their interaction with human plasmacytoid predendritic cells (pDCs), a key player in antiviral immunity. We show that pDCs are not productively infected by SARS-CoV-2. However, they efficiently diversified into activated P1-, P2-, and P3-pDC effector subsets in response to viral stimulation. They expressed CD80, CD86, CCR7, and OX40 ligand at levels similar to influenza virus-induced activation. They rapidly produced high levels of interferon-α, interferon-λ1, IL-6, IP-10, and IL-8. All major aspects of SARS-CoV-2-induced pDC activation were inhibited by hydroxychloroquine. Mechanistically, SARS-CoV-2-induced pDC activation critically depended on IRAK4 and UNC93B1, as established using pDC from genetically deficient patients. Overall, our data indicate that human pDC are efficiently activated by SARS-CoV-2 particles and may thus contribute to type I IFN-dependent immunity against SARS-CoV-2 infection. |
| Author | Karpf, Léa Bonnet-Madin, Lucie Amara, Ali Molina, Jean-Michel Zhang, Shen-Ying Zhang, Qian Delaugerre, Constance Soumelis, Vassili Puel, Anne Onodi, Fanny Jouanguy, Emmanuelle Meertens, Laurent Casanova, Jean-Laurent Picard, Capucine Le Goff, Jérôme Poirot, Justine |
| AuthorAffiliation | 1 Université de Paris, Institut de Recherche Saint-Louis, Institut National de la Santé et de la Recherche Médicale U976, Hôpital Saint-Louis, Paris, France 2 Université de Paris, Institut de Recherche Saint-Louis, Institut National de la Santé et de la Recherche Médicale U944, Centre National de la Recherche Scientifique 7212, Hôpital Saint-Louis, Paris, France 3 Laboratory of Human Genetics of Infectious Diseases, Necker Branch, Institut National de la Santé et de la Recherche Médicale, Necker Hospital for Sick Children, Paris, France 5 St. Giles Laboratory of Human Genetics of Infectious Diseases, Rockefeller Branch, The Rockefeller University, New York, NY 4 Université de Paris, Institut National de la Santé et de la Recherche Médicale Unite Mixte de Recherche 1163, Institut Imagine, Paris, France 7 Laboratoire de Virologie et Département des Maladies Infectieuses, Hôpital Saint-Louis, Assistance Publique–Hôpitaux de Paris, Paris, France 8 Howard Hughes Medical Institute, New York, NY 9 A |
| AuthorAffiliation_xml | – name: 2 Université de Paris, Institut de Recherche Saint-Louis, Institut National de la Santé et de la Recherche Médicale U944, Centre National de la Recherche Scientifique 7212, Hôpital Saint-Louis, Paris, France – name: 3 Laboratory of Human Genetics of Infectious Diseases, Necker Branch, Institut National de la Santé et de la Recherche Médicale, Necker Hospital for Sick Children, Paris, France – name: 6 Study Center for Primary Immunodeficiencies, Necker Hospital for Sick Children, Assistance Publique–Hôpitaux de Paris, Paris, France – name: 7 Laboratoire de Virologie et Département des Maladies Infectieuses, Hôpital Saint-Louis, Assistance Publique–Hôpitaux de Paris, Paris, France – name: 4 Université de Paris, Institut National de la Santé et de la Recherche Médicale Unite Mixte de Recherche 1163, Institut Imagine, Paris, France – name: 1 Université de Paris, Institut de Recherche Saint-Louis, Institut National de la Santé et de la Recherche Médicale U976, Hôpital Saint-Louis, Paris, France – name: 5 St. Giles Laboratory of Human Genetics of Infectious Diseases, Rockefeller Branch, The Rockefeller University, New York, NY – name: 8 Howard Hughes Medical Institute, New York, NY – name: 9 Assistance Publique-Hôpitaux de Paris, Hôpital Saint-Louis, Laboratoire d'Immunologie, Paris, France |
| Author_xml | – sequence: 1 givenname: Fanny orcidid: 0000-0002-8429-4821 surname: Onodi fullname: Onodi, Fanny – sequence: 2 givenname: Lucie orcidid: 0000-0002-9848-3287 surname: Bonnet-Madin fullname: Bonnet-Madin, Lucie – sequence: 3 givenname: Laurent orcidid: 0000-0003-2811-3675 surname: Meertens fullname: Meertens, Laurent – sequence: 4 givenname: Léa orcidid: 0000-0001-6959-7528 surname: Karpf fullname: Karpf, Léa – sequence: 5 givenname: Justine orcidid: 0000-0002-6694-7796 surname: Poirot fullname: Poirot, Justine – sequence: 6 givenname: Shen-Ying orcidid: 0000-0002-9449-3672 surname: Zhang fullname: Zhang, Shen-Ying – sequence: 7 givenname: Capucine orcidid: 0000-0001-8788-5056 surname: Picard fullname: Picard, Capucine – sequence: 8 givenname: Anne orcidid: 0000-0003-2603-0323 surname: Puel fullname: Puel, Anne – sequence: 9 givenname: Emmanuelle orcidid: 0000-0002-7358-9157 surname: Jouanguy fullname: Jouanguy, Emmanuelle – sequence: 10 givenname: Qian orcidid: 0000-0002-9040-3289 surname: Zhang fullname: Zhang, Qian – sequence: 11 givenname: Jérôme orcidid: 0000-0001-7111-1865 surname: Le Goff fullname: Le Goff, Jérôme – sequence: 12 givenname: Jean-Michel orcidid: 0000-0001-8684-2214 surname: Molina fullname: Molina, Jean-Michel – sequence: 13 givenname: Constance orcidid: 0000-0001-6081-7993 surname: Delaugerre fullname: Delaugerre, Constance – sequence: 14 givenname: Jean-Laurent orcidid: 0000-0002-7782-4169 surname: Casanova fullname: Casanova, Jean-Laurent – sequence: 15 givenname: Ali orcidid: 0000-0002-0283-1815 surname: Amara fullname: Amara, Ali – sequence: 16 givenname: Vassili orcidid: 0000-0003-1849-9834 surname: Soumelis fullname: Soumelis, Vassili |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/33533916$$D View this record in MEDLINE/PubMed |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Disclosures: J.-M. Molina reported grants from Gilead and personal fees from Merck, ViiV, and Janssen outside the submitted work. V. Soumelis reported grants from Sanofi and Roche, and personal fees from Leo Pharma, Gilead, Merck, and Sanofi outside the submitted work. No other disclosures were reported. |
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| Snippet | Several studies have analyzed antiviral immune pathways in late-stage severe COVID-19. However, the initial steps of SARS-CoV-2 antiviral immunity are poorly... Plasmacytoid dendritic cells (pDCs) are not permissive to SARS-CoV-2 infection but, upon viral exposure, differentiate into subsets and rapidly produce type I... |
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| Title | SARS-CoV-2 induces human plasmacytoid predendritic cell diversification via UNC93B and IRAK4 |
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