Recognition and inhibition of SARS-CoV-2 by humoral innate immunity pattern recognition molecules
The humoral arm of innate immunity includes diverse molecules with antibody-like functions, some of which serve as disease severity biomarkers in coronavirus disease 2019 (COVID-19). The present study was designed to conduct a systematic investigation of the interaction of human humoral fluid-phase...
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| Veröffentlicht in: | Nature immunology Jg. 23; H. 2; S. 275 - 286 |
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| Format: | Journal Article |
| Sprache: | Englisch |
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Nature Publishing Group
01.02.2022
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| ISSN: | 1529-2908, 1529-2916, 1529-2916 |
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| Abstract | The humoral arm of innate immunity includes diverse molecules with antibody-like functions, some of which serve as disease severity biomarkers in coronavirus disease 2019 (COVID-19). The present study was designed to conduct a systematic investigation of the interaction of human humoral fluid-phase pattern recognition molecules (PRMs) with severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2). Of 12 PRMs tested, the long pentraxin 3 (PTX3) and mannose-binding lectin (MBL) bound the viral nucleocapsid and spike proteins, respectively. MBL bound trimeric spike protein, including that of variants of concern (VoC), in a glycan-dependent manner and inhibited SARS-CoV-2 in three in vitro models. Moreover, after binding to spike protein, MBL activated the lectin pathway of complement activation. Based on retention of glycosylation sites and modeling, MBL was predicted to recognize the Omicron VoC. Genetic polymorphisms at the MBL2 locus were associated with disease severity. These results suggest that selected humoral fluid-phase PRMs can play an important role in resistance to, and pathogenesis of, COVID-19, a finding with translational implications. |
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| AbstractList | The humoral arm of innate immunity includes diverse molecules with antibody-like functions, some of which serve as disease severity biomarkers in coronavirus disease 2019 (COVID-19). The present study was designed to conduct a systematic investigation of the interaction of human humoral fluid-phase pattern recognition molecules (PRMs) with severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2). Of 12 PRMs tested, the long pentraxin 3 (PTX3) and mannose-binding lectin (MBL) bound the viral nucleocapsid and spike proteins, respectively. MBL bound trimeric spike protein, including that of variants of concern (VoC), in a glycan-dependent manner and inhibited SARS-CoV-2 in three in vitro models. Moreover, after binding to spike protein, MBL activated the lectin pathway of complement activation. Based on retention of glycosylation sites and modeling, MBL was predicted to recognize the Omicron VoC. Genetic polymorphisms at the MBL2 locus were associated with disease severity. These results suggest that selected humoral fluid-phase PRMs can play an important role in resistance to, and pathogenesis of, COVID-19, a finding with translational implications.The humoral arm of innate immunity includes diverse molecules with antibody-like functions, some of which serve as disease severity biomarkers in coronavirus disease 2019 (COVID-19). The present study was designed to conduct a systematic investigation of the interaction of human humoral fluid-phase pattern recognition molecules (PRMs) with severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2). Of 12 PRMs tested, the long pentraxin 3 (PTX3) and mannose-binding lectin (MBL) bound the viral nucleocapsid and spike proteins, respectively. MBL bound trimeric spike protein, including that of variants of concern (VoC), in a glycan-dependent manner and inhibited SARS-CoV-2 in three in vitro models. Moreover, after binding to spike protein, MBL activated the lectin pathway of complement activation. Based on retention of glycosylation sites and modeling, MBL was predicted to recognize the Omicron VoC. Genetic polymorphisms at the MBL2 locus were associated with disease severity. These results suggest that selected humoral fluid-phase PRMs can play an important role in resistance to, and pathogenesis of, COVID-19, a finding with translational implications. The humoral arm of innate immunity includes diverse molecules with antibody-like functions, some of which serve as disease severity biomarkers in coronavirus disease 2019 (COVID-19). The present study was designed to conduct a systematic investigation of the interaction of human humoral fluid-phase pattern recognition molecules (PRMs) with severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2). Of 12 PRMs tested, the long pentraxin 3 (PTX3) and mannose-binding lectin (MBL) bound the viral nucleocapsid and spike proteins, respectively. MBL bound trimeric spike protein, including that of variants of concern (VoC), in a glycan-dependent manner and inhibited SARS-CoV-2 in three in vitro models. Moreover, after binding to spike protein, MBL activated the lectin pathway of complement activation. Based on retention of glycosylation sites and modeling, MBL was predicted to recognize the Omicron VoC. Genetic polymorphisms at the MBL2 locus were associated with disease severity. These results suggest that selected humoral fluid-phase PRMs can play an important role in resistance to, and pathogenesis of, COVID-19, a finding with translational implications.Stravalaci et al. examined recognition of SARS-CoV-2 by human soluble innate pattern recognition receptor. They report that pentraxin 3 and mannose-binding protein recognize viral nucleoprotein and spike, respectively. Mannose-binding lectin has antiviral activity, and human genetic polymorphisms of MBL2 are associated with more severe COVID-19. The humoral arm of innate immunity includes diverse molecules with antibody-like functions, some of which serve as disease severity biomarkers in coronavirus disease 2019 (COVID-19). The present study was designed to conduct a systematic investigation of the interaction of human humoral fluid-phase pattern recognition molecules (PRMs) with severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2). Of 12 PRMs tested, the long pentraxin 3 (PTX3) and mannose-binding lectin (MBL) bound the viral nucleocapsid and spike proteins, respectively. MBL bound trimeric spike protein, including that of variants of concern (VoC), in a glycan-dependent manner and inhibited SARS-CoV-2 in three in vitro models. Moreover, after binding to spike protein, MBL activated the lectin pathway of complement activation. Based on retention of glycosylation sites and modeling, MBL was predicted to recognize the Omicron VoC. Genetic polymorphisms at the MBL2 locus were associated with disease severity. These results suggest that selected humoral fluid-phase PRMs can play an important role in resistance to, and pathogenesis of, COVID-19, a finding with translational implications. |
| Author | Bayarri-Olmos, Rafael Paraboschi, Elvezia Maria Mancini, Nicasio Doni, Andrea Varani, Luca Garred, Peter Mapelli, Sarah N Matkovic, Milos Uguccioni, Mariagrazia Cavalli, Andrea Scavello, Francesco Invernizzi, Pietro Pedotti, Mattia Bottazzi, Barbara Pagani, Isabel Capurro, Valeria Mantovani, Alberto Asselta, Rosanna Cesana, Daniela Gallina, Pierangela Rappuoli, Rino Perucchini, Chiara Stravalaci, Matteo Duga, Stefano Vicenzi, Elisa Pedemonte, Nicoletta Sironi, Marina Clementi, Nicola Garlanda, Cecilia |
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Humanitas Research Hospital, Milan, Italy – sequence: 7 givenname: Sarah N orcidid: 0000-0002-0129-2055 surname: Mapelli fullname: Mapelli, Sarah N organization: IRCCS Humanitas Research Hospital, Milan, Italy – sequence: 8 givenname: Marina surname: Sironi fullname: Sironi, Marina organization: IRCCS Humanitas Research Hospital, Milan, Italy – sequence: 9 givenname: Chiara surname: Perucchini fullname: Perucchini, Chiara organization: IRCCS Humanitas Research Hospital, Milan, Italy – sequence: 10 givenname: Luca surname: Varani fullname: Varani, Luca organization: Institute for Research in Biomedicine, Università della Svizzera italiana (USI), Bellinzona, Switzerland – sequence: 11 givenname: Milos surname: Matkovic fullname: Matkovic, Milos organization: Institute for Research in Biomedicine, Università della Svizzera italiana (USI), Bellinzona, Switzerland – sequence: 12 givenname: Andrea surname: Cavalli fullname: Cavalli, Andrea organization: Swiss Institute of Bioinformatics, Lausanne, Switzerland – sequence: 13 givenname: Daniela orcidid: 0000-0001-6366-4224 surname: Cesana fullname: Cesana, Daniela organization: San Raffaele Telethon Institute for Gene Therapy (SR-Tiget), IRCCS, San Raffaele Scientific Institute, Milan, Italy – sequence: 14 givenname: Pierangela surname: Gallina fullname: Gallina, Pierangela organization: San Raffaele Telethon Institute for Gene Therapy (SR-Tiget), IRCCS, San Raffaele Scientific Institute, Milan, Italy – sequence: 15 givenname: Nicoletta orcidid: 0000-0002-5161-1720 surname: Pedemonte fullname: Pedemonte, Nicoletta organization: UOC Genetica Medica, IRCCS Istituto Giannina Gaslini, Genova, Italy – sequence: 16 givenname: Valeria surname: Capurro fullname: Capurro, Valeria organization: UOC Genetica Medica, IRCCS Istituto Giannina Gaslini, Genova, Italy – sequence: 17 givenname: Nicola orcidid: 0000-0002-1822-9861 surname: Clementi fullname: Clementi, Nicola organization: Laboratory of Microbiology and Virology, IRCCS Scientific Institute and Vita-Salute San Raffaele University, Milan, Italy – sequence: 18 givenname: Nicasio surname: Mancini fullname: Mancini, Nicasio organization: Laboratory of Microbiology and Virology, IRCCS Scientific Institute and Vita-Salute San Raffaele University, Milan, Italy – sequence: 19 givenname: Pietro orcidid: 0000-0003-3262-1998 surname: Invernizzi fullname: Invernizzi, Pietro organization: European Reference Network on Hepatological Diseases (ERN RARE-LIVER), San Gerardo Hospital, Monza, Italy – sequence: 20 givenname: Rafael orcidid: 0000-0003-3202-9679 surname: Bayarri-Olmos fullname: Bayarri-Olmos, Rafael organization: Laboratory of Molecular Medicine, Department of Clinical Immunology, Section 7631, Rigshospitalet, Copenhagen University Hospital, København, Denmark – sequence: 21 givenname: Peter orcidid: 0000-0002-2876-8586 surname: Garred fullname: Garred, Peter organization: Laboratory of Molecular Medicine, Department of Clinical Immunology, Section 7631, Rigshospitalet, Copenhagen University Hospital, København, Denmark – sequence: 22 givenname: Rino orcidid: 0000-0002-8827-254X surname: Rappuoli fullname: Rappuoli, Rino organization: Faculty of Medicine, Imperial College London, London, UK – sequence: 23 givenname: Stefano orcidid: 0000-0003-3457-1410 surname: Duga fullname: Duga, Stefano organization: Department of Biomedical Sciences, Humanitas University, Milan, Italy – sequence: 24 givenname: Barbara orcidid: 0000-0002-1930-9257 surname: Bottazzi fullname: Bottazzi, Barbara organization: IRCCS Humanitas Research Hospital, Milan, Italy – sequence: 25 givenname: Mariagrazia surname: Uguccioni fullname: Uguccioni, Mariagrazia organization: Institute for Research in Biomedicine, Università della Svizzera italiana (USI), Bellinzona, Switzerland – sequence: 26 givenname: Rosanna orcidid: 0000-0001-5351-0619 surname: Asselta fullname: Asselta, Rosanna organization: Department of Biomedical Sciences, Humanitas University, Milan, Italy – sequence: 27 givenname: Elisa orcidid: 0000-0003-0051-3968 surname: Vicenzi fullname: Vicenzi, Elisa email: vicenzi.elisa@hsr.it organization: Viral Pathogenesis and Biosafety Unit, IRCCS San Raffaele Scientific Institute, Milan, Italy. vicenzi.elisa@hsr.it – sequence: 28 givenname: Alberto orcidid: 0000-0001-5578-236X surname: Mantovani fullname: Mantovani, Alberto email: alberto.mantovani@humanitasresearch.it, alberto.mantovani@humanitasresearch.it, alberto.mantovani@humanitasresearch.it organization: The William Harvey Research Institute, Queen Mary University of London, Charterhouse Square, London, UK. alberto.mantovani@humanitasresearch.it – sequence: 29 givenname: Cecilia orcidid: 0000-0002-1510-7703 surname: Garlanda fullname: Garlanda, Cecilia email: cecilia.garlanda@humanitasresearch.it, cecilia.garlanda@humanitasresearch.it organization: Department of Biomedical Sciences, Humanitas University, Milan, Italy. cecilia.garlanda@humanitasresearch.it |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/35102342$$D View this record in MEDLINE/PubMed |
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| PublicationDate_xml | – month: 02 year: 2022 text: 2022-02-01 day: 01 |
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| PublicationTitle | Nature immunology |
| PublicationTitleAlternate | Nat Immunol |
| PublicationYear | 2022 |
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| Snippet | The humoral arm of innate immunity includes diverse molecules with antibody-like functions, some of which serve as disease severity biomarkers in coronavirus... |
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| SubjectTerms | Animals Antiviral activity Antiviral drugs C-Reactive Protein - immunology C-Reactive Protein - metabolism Case-Control Studies Chlorocebus aethiops Complement Activation Coronavirus Nucleocapsid Proteins - genetics Coronavirus Nucleocapsid Proteins - immunology Coronavirus Nucleocapsid Proteins - metabolism Coronaviruses COVID-19 COVID-19 - immunology COVID-19 - metabolism COVID-19 - virology Female Gene polymorphism Glycosylation HEK293 Cells Host-Pathogen Interactions Humans Humoral immunity Immunity, Humoral Innate immunity Lectins Male Mannose Mannose-binding lectin Mannose-Binding Lectin - genetics Mannose-Binding Lectin - immunology Mannose-Binding Lectin - metabolism Nucleocapsids Pattern recognition Pattern recognition receptors Pentraxins Phosphoproteins - genetics Phosphoproteins - immunology Phosphoproteins - metabolism Polymorphism, Genetic Protein Binding Proteins Receptors, Pattern Recognition - genetics Receptors, Pattern Recognition - immunology Receptors, Pattern Recognition - metabolism Respiration SARS-CoV-2 - genetics SARS-CoV-2 - immunology SARS-CoV-2 - metabolism SARS-CoV-2 - pathogenicity Serum Amyloid P-Component - immunology Serum Amyloid P-Component - metabolism Severe acute respiratory syndrome coronavirus 2 Signal Transduction Spike Glycoprotein, Coronavirus - genetics Spike Glycoprotein, Coronavirus - immunology Spike Glycoprotein, Coronavirus - metabolism Spike protein Vero Cells |
| Title | Recognition and inhibition of SARS-CoV-2 by humoral innate immunity pattern recognition molecules |
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