Humoral signatures of protective and pathological SARS-CoV-2 infection in children
The severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) pandemic continues to spread relentlessly, associated with a high frequency of respiratory failure and mortality. Children experience largely asymptomatic disease, with rare reports of multisystem inflammatory syndrome in children (MIS...
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| Published in | Nature medicine Vol. 27; no. 3; pp. 454 - 462 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
New York
Nature Publishing Group US
01.03.2021
Nature Publishing Group |
| Subjects | |
| Online Access | Get full text |
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| Abstract | The severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) pandemic continues to spread relentlessly, associated with a high frequency of respiratory failure and mortality. Children experience largely asymptomatic disease, with rare reports of multisystem inflammatory syndrome in children (MIS-C). Identifying immune mechanisms that result in these disparate clinical phenotypes in children could provide critical insights into coronavirus disease 2019 (COVID-19) pathogenesis. Using systems serology, in this study we observed in 25 children with acute mild COVID-19 a functional phagocyte and complement-activating IgG response to SARS-CoV-2, similar to the acute responses generated in adults with mild disease. Conversely, IgA and neutrophil responses were significantly expanded in adults with severe disease. Moreover, weeks after the resolution of SARS-CoV-2 infection, children who develop MIS-C maintained highly inflammatory monocyte-activating SARS-CoV-2 IgG antibodies, distinguishable from acute disease in children but with antibody levels similar to those in convalescent adults. Collectively, these data provide unique insights into the potential mechanisms of IgG and IgA that might underlie differential disease severity as well as unexpected complications in children infected with SARS-CoV-2.
A study of multisystem inflammatory syndrome in children (MIS-C) shows maintenance of elevated levels of monocyte-activating pathogen-specific IgG not seen in children infected with SARS-CoV-2 who do not develop MIS-C. |
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| AbstractList | The severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) pandemic continues to spread relentlessly, associated with a high frequency of respiratory failure and mortality. Children experience largely asymptomatic disease, with rare reports of multisystem inflammatory syndrome in children (MIS-C). Identifying immune mechanisms that result in these disparate clinical phenotypes in children could provide critical insights into coronavirus disease 2019 (COVID-19) pathogenesis. Using systems serology, in this study we observed in 25 children with acute mild COVID-19 a functional phagocyte and complement-activating IgG response to SARS-CoV-2, similar to the acute responses generated in adults with mild disease. Conversely, IgA and neutrophil responses were significantly expanded in adults with severe disease. Moreover, weeks after the resolution of SARS-CoV-2 infection, children who develop MIS-C maintained highly inflammatory monocyte-activating SARS-CoV-2 IgG antibodies, distinguishable from acute disease in children but with antibody levels similar to those in convalescent adults. Collectively, these data provide unique insights into the potential mechanisms of IgG and IgA that might underlie differential disease severity as well as unexpected complications in children infected with SARS-CoV-2. A study of multisystem inflammatory syndrome in children (MIS-C) shows maintenance of elevated levels of monocyte-activating pathogen-specific IgG not seen in children infected with SARS-CoV-2 who do not develop MIS-C. The SARS-CoV-2 pandemic continues to spread relentlessly, associated with a high frequency of respiratory failure and mortality. Children experience largely asymptomatic disease, with rare reports of a Multisystem Inflammatory Syndrome in Children (MIS-C). Identifying immune mechanisms that result in these disparate clinical phenotypes in children could provide critical insights into COVID-19 pathogenesis. Using Systems Serology, here we observed in 25 children with acute mild COVID a functional phagocyte and complement activating IgG response to SARS-CoV-2, comparable to the acute responses generated in adults with mild disease. Conversely, IgA and neutrophil responses were significantly expanded in adults with severe disease. Moreover, weeks after the resolution of SARS-CoV-2 infection, children who develop MIS-C maintained highly inflammatory monocyte activating SARS-CoV-2 IgG antibodies distinguishable from acute disease in children but with antibody levels comparable to convalescent adults. Collectively, these data provide unique insights into the potential mechanisms of IgG and IgA that may underlie differential disease severity as well as unexpected complications in SARS-CoV-2 infected children. A study of Multisystem Inflammatory Syndrome in Children (MIS-C) shows maintenance of elevated levels of monocyte-activating pathogen-specific IgG, not seen in SARS-CoV-2-infected children who don’t develop MIS-C. The severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) pandemic continues to spread relentlessly, associated with a high frequency of respiratory failure and mortality. Children experience largely asymptomatic disease, with rare reports of multisystem inflammatory syndrome in children (MIS-C). Identifying immune mechanisms that result in these disparate clinical phenotypes in children could provide critical insights into coronavirus disease 2019 (COVID-19) pathogenesis. Using systems serology, in this study we observed in 25 children with acute mild COVID-19 a functional phagocyte and complement-activating IgG response to SARS-CoV-2, similar to the acute responses generated in adults with mild disease. Conversely, IgA and neutrophil responses were significantly expanded in adults with severe disease. Moreover, weeks after the resolution of SARS-CoV-2 infection, children who develop MIS-C maintained highly inflammatory monocyte-activating SARS-CoV-2 IgG antibodies, distinguishable from acute disease in children but with antibody levels similar to those in convalescent adults. Collectively, these data provide unique insights into the potential mechanisms of IgG and IgA that might underlie differential disease severity as well as unexpected complications in children infected with SARS-CoV-2. The severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) pandemic continues to spread relentlessly, associated with a high frequency of respiratory failure and mortality. Children experience largely asymptomatic disease, with rare reports of multisystem inflammatory syndrome in children (MIS-C). Identifying immune mechanisms that result in these disparate clinical phenotypes in children could provide critical insights into coronavirus disease 2019 (COVID-19) pathogenesis. Using systems serology, in this study we observed in 25 children with acute mild COVID-19 a functional phagocyte and complement-activating IgG response to SARS-CoV-2, similar to the acute responses generated in adults with mild disease. Conversely, IgA and neutrophil responses were significantly expanded in adults with severe disease. Moreover, weeks after the resolution of SARS-CoV-2 infection, children who develop MIS-C maintained highly inflammatory monocyte-activating SARS-CoV-2 IgG antibodies, distinguishable from acute disease in children but with antibody levels similar to those in convalescent adults. Collectively, these data provide unique insights into the potential mechanisms of IgG and IgA that might underlie differential disease severity as well as unexpected complications in children infected with SARS-CoV-2. A study of multisystem inflammatory syndrome in children (MIS-C) shows maintenance of elevated levels of monocyte-activating pathogen-specific IgG not seen in children infected with SARS-CoV-2 who do not develop MIS-C. The severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) pandemic continues to spread relentlessly, associated with a high frequency of respiratory failure and mortality. Children experience largely asymptomatic disease, with rare reports of multisystem inflammatory syndrome in children (MIS-C). Identifying immune mechanisms that result in these disparate clinical phenotypes in children could provide critical insights into coronavirus disease 2019 (COVID-19) pathogenesis. Using systems serology, in this study we observed in 25 children with acute mild COVID-19 a functional phagocyte and complement-activating IgG response to SARS-CoV-2, similar to the acute responses generated in adults with mild disease. Conversely, IgA and neutrophil responses were significantly expanded in adults with severe disease. Moreover, weeks after the resolution of SARS-CoV-2 infection, children who develop MIS-C maintained highly inflammatory monocyte-activating SARS-CoV-2 IgG antibodies, distinguishable from acute disease in children but with antibody levels similar to those in convalescent adults. Collectively, these data provide unique insights into the potential mechanisms of IgG and IgA that might underlie differential disease severity as well as unexpected complications in children infected with SARS-CoV-2.The severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) pandemic continues to spread relentlessly, associated with a high frequency of respiratory failure and mortality. Children experience largely asymptomatic disease, with rare reports of multisystem inflammatory syndrome in children (MIS-C). Identifying immune mechanisms that result in these disparate clinical phenotypes in children could provide critical insights into coronavirus disease 2019 (COVID-19) pathogenesis. Using systems serology, in this study we observed in 25 children with acute mild COVID-19 a functional phagocyte and complement-activating IgG response to SARS-CoV-2, similar to the acute responses generated in adults with mild disease. Conversely, IgA and neutrophil responses were significantly expanded in adults with severe disease. Moreover, weeks after the resolution of SARS-CoV-2 infection, children who develop MIS-C maintained highly inflammatory monocyte-activating SARS-CoV-2 IgG antibodies, distinguishable from acute disease in children but with antibody levels similar to those in convalescent adults. Collectively, these data provide unique insights into the potential mechanisms of IgG and IgA that might underlie differential disease severity as well as unexpected complications in children infected with SARS-CoV-2. |
| Audience | Academic |
| Author | Atyeo, Caroline Fischer, Eric S. Burke, John S. Yonker, Lael M. Irimia, Daniel Wang, Chuangqi Edlow, Andrea G. Ryan, Edward T. Zohar, Tomer Baden, Lindsey R. Hopke, Alex R. Charles, Richelle C. Julg, Boris D. Alter, Galit Woolley, Ann E. Karlson, Elizabeth W. Fischinger, Stephanie Nilles, Eric J. Kang, Jaewon Bartsch, Yannic C. Fasano, Alessio Lauffenburger, Douglas A. |
| AuthorAffiliation | 8 Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Boston, MA 7 Department of Cancer Biology, Dana Farber Cancer Institute, Boston MA 1 Ragon Institute of MGH, MIT and Harvard, Cambridge, MA, USA 3 Massachusetts General Hospital Department of Obstetrics and Gynecology, Division of Maternal-Fetal Medicine, Boston, MA 6 Massachusetts General Hospital, BioMEMS Resource Center, Boston, MA 2 Department of Biological Engineering, Massachusetts Institute of Technology, Cambridge, MA, USA 4 Massachusetts General Hospital, Mucosal Immunology and Biology Research Center, Boston, MA Massachusetts General Hospital, Department of Pediatrics, Boston, MA 5 Brigham and Women’s Hospital, Boston, MA |
| AuthorAffiliation_xml | – name: 1 Ragon Institute of MGH, MIT and Harvard, Cambridge, MA, USA – name: 5 Brigham and Women’s Hospital, Boston, MA – name: 6 Massachusetts General Hospital, BioMEMS Resource Center, Boston, MA – name: 3 Massachusetts General Hospital Department of Obstetrics and Gynecology, Division of Maternal-Fetal Medicine, Boston, MA – name: 2 Department of Biological Engineering, Massachusetts Institute of Technology, Cambridge, MA, USA – name: 7 Department of Cancer Biology, Dana Farber Cancer Institute, Boston MA – name: 8 Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Boston, MA – name: 4 Massachusetts General Hospital, Mucosal Immunology and Biology Research Center, Boston, MA Massachusetts General Hospital, Department of Pediatrics, Boston, MA |
| Author_xml | – sequence: 1 givenname: Yannic C. orcidid: 0000-0002-3844-3056 surname: Bartsch fullname: Bartsch, Yannic C. organization: Ragon Institute of MGH, MIT and Harvard – sequence: 2 givenname: Chuangqi surname: Wang fullname: Wang, Chuangqi organization: Department of Biological Engineering, Massachusetts Institute of Technology – sequence: 3 givenname: Tomer surname: Zohar fullname: Zohar, Tomer organization: Ragon Institute of MGH, MIT and Harvard, Department of Biological Engineering, Massachusetts Institute of Technology – sequence: 4 givenname: Stephanie orcidid: 0000-0003-2307-3379 surname: Fischinger fullname: Fischinger, Stephanie organization: Ragon Institute of MGH, MIT and Harvard – sequence: 5 givenname: Caroline orcidid: 0000-0002-7489-0232 surname: Atyeo fullname: Atyeo, Caroline organization: Ragon Institute of MGH, MIT and Harvard – sequence: 6 givenname: John S. orcidid: 0000-0003-1282-8211 surname: Burke fullname: Burke, John S. organization: Ragon Institute of MGH, MIT and Harvard – sequence: 7 givenname: Jaewon orcidid: 0000-0003-0846-4611 surname: Kang fullname: Kang, Jaewon organization: Ragon Institute of MGH, MIT and Harvard – sequence: 8 givenname: Andrea G. surname: Edlow fullname: Edlow, Andrea G. organization: Massachusetts General Hospital Department of Obstetrics and Gynecology, Division of Maternal-Fetal Medicine – sequence: 9 givenname: Alessio orcidid: 0000-0002-2134-0261 surname: Fasano fullname: Fasano, Alessio organization: Massachusetts General Hospital, Mucosal Immunology and Biology Research Center, Massachusetts General Hospital, Department of Pediatrics – sequence: 10 givenname: Lindsey R. surname: Baden fullname: Baden, Lindsey R. organization: Brigham and Women’s Hospital – sequence: 11 givenname: Eric J. orcidid: 0000-0001-7044-5257 surname: Nilles fullname: Nilles, Eric J. organization: Brigham and Women’s Hospital – sequence: 12 givenname: Ann E. surname: Woolley fullname: Woolley, Ann E. organization: Brigham and Women’s Hospital – sequence: 13 givenname: Elizabeth W. surname: Karlson fullname: Karlson, Elizabeth W. organization: Brigham and Women’s Hospital – sequence: 14 givenname: Alex R. orcidid: 0000-0003-4860-4121 surname: Hopke fullname: Hopke, Alex R. organization: Massachusetts General Hospital, BioMEMS Resource Center – sequence: 15 givenname: Daniel orcidid: 0000-0001-7347-2082 surname: Irimia fullname: Irimia, Daniel organization: Massachusetts General Hospital, BioMEMS Resource Center – sequence: 16 givenname: Eric S. orcidid: 0000-0001-7337-6306 surname: Fischer fullname: Fischer, Eric S. organization: Department of Cancer Biology, Dana Farber Cancer Institute, Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School – sequence: 17 givenname: Edward T. surname: Ryan fullname: Ryan, Edward T. organization: Massachusetts General Hospital, BioMEMS Resource Center – sequence: 18 givenname: Richelle C. orcidid: 0000-0002-8881-1849 surname: Charles fullname: Charles, Richelle C. organization: Massachusetts General Hospital, BioMEMS Resource Center – sequence: 19 givenname: Boris D. surname: Julg fullname: Julg, Boris D. organization: Ragon Institute of MGH, MIT and Harvard – sequence: 20 givenname: Douglas A. orcidid: 0000-0002-0050-989X surname: Lauffenburger fullname: Lauffenburger, Douglas A. organization: Department of Biological Engineering, Massachusetts Institute of Technology – sequence: 21 givenname: Lael M. surname: Yonker fullname: Yonker, Lael M. email: lyonker@mgh.harvard.edu organization: Massachusetts General Hospital, Mucosal Immunology and Biology Research Center, Massachusetts General Hospital, Department of Pediatrics – sequence: 22 givenname: Galit orcidid: 0000-0002-7680-9215 surname: Alter fullname: Alter, Galit email: galter@mgh.harvard.edu organization: Ragon Institute of MGH, MIT and Harvard |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/33589825$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article |
| Copyright | The Author(s), under exclusive licence to Springer Nature America, Inc. 2021 COPYRIGHT 2021 Nature Publishing Group The Author(s), under exclusive licence to Springer Nature America, Inc. 2021. |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Author contribution YCB, LMY and GA analyzed and interpreted the data. YCB, TZ, SF CA, JB, JK, ARH and DI performed experiments. CW and DAL performed the computational analysis. AGE, AF, LRB, EJN, LRB, AEW, EWB, ETR, RC, BDJ and LMY collected the samples and supervised and managed the clinical data. ESF produced SARS-CoV-2 and human coronavirus antigens. LMY and GA supervised the project. YCB and GA drafted the manuscript. All authors critically reviewed the manuscript. |
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K Takahashi (1263_CR28) 2010; 3 L Verdoni (1263_CR6) 2020; 395 T Zohar (1263_CR10) 2020; 20 AE Mahan (1263_CR45) 2015; 417 V Roy (1263_CR41) 2020; 484-485 CC Khor (1263_CR31) 2011; 43 1263_CR17 1263_CR39 S Fagarasan (1263_CR20) 2003; 3 1263_CR37 1263_CR16 1263_CR38 1263_CR13 1263_CR35 1263_CR11 E Aleyd (1263_CR22) 2014; 192 CB Karsten (1263_CR44) 2019; 471 M Laforge (1263_CR14) 2020; 20 J Abe (1263_CR33) 2005; 174 R Hamre (1263_CR12) 2003; 57 C Weemaes (1263_CR26) 2003; 58 QX Long (1263_CR36) 2020; 26 S Wold (1263_CR47) 1987; 2 1263_CR19 Y Liu (1263_CR24) 2020; 81 S Menikou (1263_CR18) 2019; 10 JM Woof (1263_CR21) 2004; 113 1263_CR40 LR Feldstein (1263_CR8) 2020; 383 JO Richards (1263_CR30) 2008; 7 S Fischinger (1263_CR42) 2019; 473 1263_CR1 S Riphagen (1263_CR7) 2020; 395 1263_CR3 1263_CR2 1263_CR27 SQ Nagelkerke (1263_CR32) 2014; 124 1263_CR46 1263_CR4 1263_CR25 S Godfred-Cato (1263_CR34) 2020; 69 ME Ackerman (1263_CR43) 2011; 366 1263_CR23 1263_CR9 V Witko-Sarsat (1263_CR15) 2000; 80 WH Mason (1263_CR29) 1985; 4 R Tibshirani (1263_CR48) 2011; 73 JT Ladner (1263_CR5) 2021; 2 |
| References_xml | – reference: Gruber, C. N. et al. Mapping systemic inflammation and antibody responses in multisystem inflammatory syndrome in children (MIS-C). Cell183, 982–995 (2020). – reference: KarstenCBA versatile high-throughput assay to characterize antibody-mediated neutrophil phagocytosisJ. Immunol. Methods201947146561:CAS:528:DC%2BC1MXhtFOku77E10.1016/j.jim.2019.05.006 – reference: VerdoniLAn outbreak of severe Kawasaki-like disease at the Italian epicentre of the SARS-CoV-2 epidemic: an observational cohort studyLancet2020395177117781:CAS:528:DC%2BB3cXptlKmsL8%3D10.1016/S0140-6736(20)31103-X – reference: Zuo, Y. et al. Neutrophil extracellular traps in COVID-19. JCI Insight5, e138999 (2020). – reference: MasonWHJordanSCSakaiRTakahashiMBernsteinBCirculating immune complexes in Kawasaki syndromePediatr. Infect. Dis.1985448511:STN:280:DyaL2M7ht1yktA%3D%3D10.1097/00006454-198501000-00012 – reference: ZoharTAlterGDissecting antibody-mediated protection against SARS-CoV-2Nat. Rev. Immunol.2020203923941:CAS:528:DC%2BB3cXhtFWltLvP10.1038/s41577-020-0359-5 – reference: Veras, F. P. et al. SARS-CoV-2-triggered neutrophil extracellular traps mediate COVID-19 pathology. J. Exp. Med.217, e20201129 (2020). – reference: WeemaesCDevelopment of immunoglobulin A in infancy and childhoodScand. J. Immunol.2003586426481:CAS:528:DC%2BD2cXht1ekuw%3D%3D10.1111/j.1365-3083.2003.01344.x – reference: RichardsJOOptimization of antibody binding to FcγRIIa enhances macrophage phagocytosis of tumor cellsMol. Cancer Ther.20087251725271:CAS:528:DC%2BD1cXhtVWksLzJ10.1158/1535-7163.MCT-08-0201 – reference: FeldsteinLRMultisystem inflammatory syndrome in U.S. children and adolescentsN. Engl. J. Med.20203833343461:CAS:528:DC%2BB3cXhsFWrs7jI10.1056/NEJMoa2021680 – reference: MahanAEA method for high-throughput, sensitive analysis of IgG Fc and Fab glycosylation by capillary electrophoresisJ. Immunol. Methods201541734441:CAS:528:DC%2BC2cXitFygt73E10.1016/j.jim.2014.12.004 – reference: Weisberg, S. P. et al. Distinct antibody responses to SARS-CoV-2 in children and adults across the COVID-19 clinical spectrum. Nat. Immunol. 22, 25–31 (2020). – reference: Belhadjer, Z. et al. Acute heart failure in multisystem inflammatory syndrome in children (MIS-C) in the context of global SARS-CoV-2 pandemic. Circulation142, 429–436 (2020). – reference: Bi, Q. et al. Epidemiology and transmission of COVID-19 in 391 cases and 1286 of their close contacts in Shenzhen, China: a retrospective cohort study. Lancet Infect. Dis.20, 911–919 (2020). – reference: WoofJMKerrMAIgA function—variations on a themeImmunology20041131751771:CAS:528:DC%2BD2cXot1Khsr8%3D10.1111/j.1365-2567.2004.01958.x – reference: Godfred-CatoSCOVID-19-associated multisystem inflammatory syndrome in children—United States, March-July 2020MMWR Morb. Mortal. Wkly. 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| Title | Humoral signatures of protective and pathological SARS-CoV-2 infection in children |
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