Nucleocapsid-specific antibody function is associated with therapeutic benefits from COVID-19 convalescent plasma therapy

Dong, 2020, An interactive web-based dashboard to track COVID-19 in real time, Lancet Infect. Dis., 20, 533, 10.1016/S1473-3099(20)30120-1 Casadevall, 2020, The convalescent sera option for containing COVID-19, J. Clin. Invest., 130, 1545, 10.1172/JCI138003 Libster, 2021, Early high-titer plasma therapy to prevent severe covid-19 in older adults, N. Engl. J. Med., 384, 610, 10.1056/NEJMoa2033700 Joyner, 2021, Convalescent plasma antibody levels and the risk of death from covid-19, N. Engl. J. Med., 384, 1015, 10.1056/NEJMoa2031893 O'Donnell, 2021, A randomized double-blind controlled trial of convalescent plasma in adults with severe COVID-19, J. Clin. Invest., 131, 150646, 10.1172/JCI150646 Yoon, 2021, Treatment of severe COVID-19 with convalescent plasma in bronx, NYC, JCI Insight, 6, e142270 Avendaño-Solá, 2021, A multicenter randomized open-label clinical trial for convalescent plasma in patients hospitalized with COVID-19 pneumonia, J. Clin. Invest., 131, e152740, 10.1172/JCI152740 Salazar, 2021, Significantly decreased mortality in a large cohort of coronavirus disease 2019 (COVID-19) patients transfused early with convalescent plasma containing high-titer anti–severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) spike protein IgG, Am. J. Pathol., 191, 90, 10.1016/j.ajpath.2020.10.008 Sullivan, 2021, Randomized controlled trial of early outpatient COVID-19 treatment with high-titer convalescent plasma, medRxiv The RECOVERY Collaborative Group; Horby, P.W., Estcourt, L., Peto, L., Emberson, J.R., Staplin, N., Spata, E., Pessoa-Amorim, G., Campbell, M., Roddick, A., et al. Convalescent Plasma in Patients Admitted to Hospital with COVID-19 (RECOVERY): A Randomised, Controlled, Open-Label, Platform Trial. Preprint at medRxiv. https://doi.org/10.1101/2021.03.09.21252736. Abdelhady, 2021, Effect of convalescent plasma on organ support–free days in critically ill patients with COVID-19, JAMA, 326, 1690, 10.1001/jama.2021.18178 Bégin, 2021, Convalescent plasma for hospitalized patients with COVID-19: an open-label, randomized controlled trial, Nat. Med., 27, 2012, 10.1038/s41591-021-01488-2 Herman, 2021, Functional convalescent plasma antibodies and pre-infusion titers shape the early severe COVID-19 immune response, Nat. Commun., 12, 6853, 10.1038/s41467-021-27201-y Bar, 2021, A randomized controlled study of convalescent plasma for individuals hospitalized with COVID-19 pneumonia, J. Clin. Invest., 131, e155114, 10.1172/JCI155114 Focosi, 2021, Comparative analysis of antibody responses from COVID-19 convalescents receiving various vaccines reveals consistent high neutralizing activity for SARS-CoV-2 variant of concern omicron, medRxiv Schmidt, 2022, Plasma neutralization of the SARS-CoV-2 omicron variant, N. Engl. J. Med., 386, 599, 10.1056/NEJMc2119641 O'Connell, 2021 Wang, 2020, Neutralizing antibodies responses to SARS-CoV-2 in COVID-19 inpatients and convalescent patients, Clin. Infect. Dis., 71, ciaa721 Natarajan, 2021, Markers of polyfunctional SARS-CoV-2 antibodies in convalescent plasma, mBio, 12, 007655, 10.1128/mBio.00765-21 Morgenlander, 2021, Antibody responses to endemic coronaviruses modulate COVID-19 convalescent plasma functionality, J. Clin. Invest., 131, 146927, 10.1172/JCI146927 Shaw, 2016, A rank test for bivariate time-to-event outcomes when one event is a surrogate, Stat. Med., 35, 3413, 10.1002/sim.6950 Chung, 2015, Dissecting polyclonal vaccine-induced humoral immunity against HIV using systems serology, Cell, 163, 988, 10.1016/j.cell.2015.10.027 Zohar, 2020, Compromised humoral functional evolution tracks with SARS-CoV-2 mortality, Cell, 183, 1508, 10.1016/j.cell.2020.10.052 Zervou, 2021, SARS-CoV-2 antibodies: IgA correlates with severity of disease in early COVID-19 infection, J. Med. Virol., 93, 5409, 10.1002/jmv.27058 Bartsch, 2021, Humoral signatures of protective and pathological SARS-CoV-2 infection in children, Nat. Med., 27, 454, 10.1038/s41591-021-01263-3 Ma, 2020, Serum IgA, IgM, and IgG responses in COVID-19, Cell. Mol. Immunol., 17, 773, 10.1038/s41423-020-0474-z Yu, 2020, Distinct features of SARS-CoV-2-specific IgA response in COVID-19 patients, Eur. Respir. J., 56, 2001526, 10.1183/13993003.01526-2020 Frasca, 2017, Ageing and obesity similarly impair antibody responses, Clin. Exp. Immunol., 187, 64, 10.1111/cei.12824 Herman, 2021, Functional antibodies in COVID-19 convalescent plasma, medRxiv Weinreich, 2021, REGN-COV2, a neutralizing antibody cocktail, in outpatients with covid-19, N. Engl. J. Med., 384, 238, 10.1056/NEJMoa2035002 Peluso, 2021, SARS-CoV-2 antibody magnitude and detectability are driven by disease severity, timing, and assay, Sci. Adv., 7, eabh3409, 10.1126/sciadv.abh3409 Hansen, 2020, SARS-CoV-2 antibody responses are correlated to disease severity in COVID-19 convalescent individuals, J. Immunol., 206, 109, 10.4049/jimmunol.2000898 Garcia-Beltran, 2021, COVID-19-neutralizing antibodies predict disease severity and survival, Cell, 184, 476, 10.1016/j.cell.2020.12.015 Koleba, 2006, Pharmacokinetics of intravenous immunoglobulin: a systematic review, Pharmacotherapy, 26, 813, 10.1592/phco.26.6.813 Arnold, 2007, The impact of glycosylation on the biological function and structure of human immunoglobulins, Annu. Rev. Immunol., 25, 21, 10.1146/annurev.immunol.25.022106.141702 Raju, 2008, Terminal sugars of Fc glycans influence antibody effector functions of IgGs, Curr. Opin. Immunol., 20, 471, 10.1016/j.coi.2008.06.007 Jennewein, 2017, The immunoregulatory roles of antibody glycosylation, Trends Immunol., 38, 358, 10.1016/j.it.2017.02.004 Larsen, 2021, Afucosylated IgG characterizes enveloped viral responses and correlates with COVID-19 severity, Science, 371, eabc8378, 10.1126/science.abc8378 Chakraborty, 2020, Proinflammatory IgG Fc structures in patients with severe COVID-19, Nat. Immunol., 22, 67, 10.1038/s41590-020-00828-7 Kaneko, 2006, Anti-inflammatory activity of immunoglobulin G resulting from Fc sialylation, Science, 313, 670, 10.1126/science.1129594 Anthony, 2008, Recapitulation of IVIG anti-inflammatory activity with a recombinant IgG Fc, Science, 320, 373, 10.1126/science.1154315 Karsten, 2012, Anti-inflammatory activity of IgG1 mediated by Fc galactosylation and association of FcγRIIB and dectin-1, Nat. Med., 18, 1401, 10.1038/nm.2862 Hoepel, 2021, High titers and low fucosylation of early human anti–SARS-CoV-2 IgG promote inflammation by alveolar macrophages, Sci. Transl. Med., 13, eabf8654, 10.1126/scitranslmed.abf8654 Zhou, 2020, Pathogenic T-cells and inflammatory monocytes incite inflammatory storms in severe COVID-19 patients, Natl. Sci. Rev., 7, 998, 10.1093/nsr/nwaa041 Grace, 2021, Antibody subclass and glycosylation shift following effective TB treatment, Front. Immunol., 12, 679973, 10.3389/fimmu.2021.679973 Ho, 2015, Aberrant serum immunoglobulin G glycosylation in chronic hepatitis B is associated with histological liver damage and reversible by antiviral therapy, J. Infect. Dis., 211, 115, 10.1093/infdis/jiu388 Anthony, 2011, Intravenous gammaglobulin suppresses inflammation through a novel TH2 pathway, Nature, 475, 110, 10.1038/nature10134 Fiebiger, 2015, Protection in antibody- and T cell-mediated autoimmune diseases by antiinflammatory IgG Fcs requires type II FcRs, Proc. Natl. Acad. Sci. USA, 112, E2385, 10.1073/pnas.1505292112 Bournazos, 2020, Fc-optimized antibodies elicit CD8 immunity to viral respiratory infection, Nature, 588, 485, 10.1038/s41586-020-2838-z Lofano, 2018, Antigen-specific antibody Fc glycosylation enhances humoral immunity via the recruitment of complement, Sci. Immunol., 3, eaat7796, 10.1126/sciimmunol.aat7796 Gao, 2020, Highly pathogenic coronavirus N protein aggravates lung injury by MASP-2-mediated complement over-activation, medRxiv Kang, 2021, A SARS-CoV-2 antibody curbs viral nucleocapsid protein-induced complement hyperactivation, Nat. Commun., 12, 2697, 10.1038/s41467-021-23036-9 Ma, 2021, Increased complement activation is a distinctive feature of severe SARS-CoV-2 infection, Sci. Immunol., 6, eabh2259, 10.1126/sciimmunol.abh2259 Bernal, 2021, Molnupiravir for oral treatment of covid-19 in nonhospitalized patients, New Engl. J. Med. Agency, 2021 Raymond, 2011, Production of highly sialylated monoclonal antibodies Cameroni, 2021, Broadly neutralizing antibodies overcome SARS-CoV-2 Omicron antigenic shift, bioRxiv Aggarwal, 2021, SARS-CoV-2 Omicron: evasion of potent humoral responses and resistance to clinical immunotherapeutics relative to viral variants of concern, medRxiv Planas, 2021, Considerable escape of SARS-CoV-2 variant Omicron to antibody neutralization, bioRxiv Cao, 2021, Omicron escapes the majority of existing SARS-CoV-2 neutralizing antibodies, bioRxiv Ali, 2021, Hyperimmune anti-COVID-19 IVIG (C-IVIG) treatment in severe and critical COVID-19 patients: a phase I/II randomized control trial, Eclinicalmedicine, 36, 100926, 10.1016/j.eclinm.2021.100926 Liu, 2021, Human immunoglobulin from transchromosomic bovines hyperimmunized with SARS-CoV-2 spike antigen efficiently neutralizes viral variants, Hum. Vaccines Immunother., 18, 1940652, 10.1080/21645515.2021.1940652 Kunze, 2021, Mortality in individuals treated with COVID-19 convalescent plasma varies with the geographic provenance of donors, Nat. Commun., 12, 4864, 10.1038/s41467-021-25113-5 Boesch, 2014, Highly parallel characterization of IgG Fc binding interactions, mAbs, 6, 915, 10.4161/mabs.28808 Brown, 2017, Multiplexed Fc array for evaluation of antigen-specific antibody effector profiles, J. Immunol. Methods, 443, 33, 10.1016/j.jim.2017.01.010 Ackerman, 2011, A robust, high-throughput assay to determine the phagocytic activity of clinical antibody samples, J. Immunol. Methods, 366, 8, 10.1016/j.jim.2010.12.016 Ackerman, 2018, Route of immunization defines multiple mechanisms of vaccine-mediated protection against SIV, Nat. Med., 24, 1590, 10.1038/s41591-018-0161-0 Lu, 2016, A functional role for antibodies in tuberculosis, Cell, 167, 433, 10.1016/j.cell.2016.08.072 Fischinger, 2019, A high-throughput, bead-based, antigen-specific assay to assess the ability of antibodies to induce complement activation, J. Immunol. Methods, 1, 44 Karsten, 2019, A versatile high-throughput assay to characterize antibody-mediated neutrophil phagocytosis, J. Immunol. Methods, 471, 46, 10.1016/j.jim.2019.05.006 Alter, 2004, CD107a as a functional marker for the identification of natural killer cell activity, J. Immunol. Methods, 294, 15, 10.1016/j.jim.2004.08.008 Colucci, 2003, What does it take to make a natural killer?, Nat. Rev. Immunol., 3, 413, 10.1038/nri1088 Mahan, 2015, A method for high-throughput, sensitive analysis of IgG Fc and Fab glycosylation by capillary electrophoresis, J. Immunol. Methods, 417, 34, 10.1016/j.jim.2014.12.004