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• W4280517779 abstract "Neutralizing antibodies can block infection, clear pathogens, and are essential to provide long-term immunity. Since the onset of the pandemic, SARS-CoV-2 neutralizing antibodies have been comprehensively investigated and critical information on their development, function, and potential use to prevent and treat COVID-19 have been revealed. With the emergence of SARS-CoV-2 immune escape variants, humoral immunity is being challenged, and a detailed understanding of neutralizing antibodies is essential to guide vaccine design strategies as well as antibody-mediated therapies. In this review, we summarize some of the key findings on SARS-CoV-2 neutralizing antibodies, with a focus on their clinical application. Neutralizing antibodies can block infection, clear pathogens, and are essential to provide long-term immunity. Since the onset of the pandemic, SARS-CoV-2 neutralizing antibodies have been comprehensively investigated and critical information on their development, function, and potential use to prevent and treat COVID-19 have been revealed. With the emergence of SARS-CoV-2 immune escape variants, humoral immunity is being challenged, and a detailed understanding of neutralizing antibodies is essential to guide vaccine design strategies as well as antibody-mediated therapies. In this review, we summarize some of the key findings on SARS-CoV-2 neutralizing antibodies, with a focus on their clinical application. After emerging in December 2019, the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) rapidly spread across the globe (Singh et al., 2021Singh S. McNab C. Olson R.M. Bristol N. Nolan C. Bergstrøm E. Bartos M. Mabuchi S. Panjabi R. Karan A. et al.How an outbreak became a pandemic: a chronological analysis of crucial junctures and international obligations in the early months of the COVID-19 pandemic.The Lancet. 2021; 398: 2109-2124https://doi.org/10.1016/s0140-6736(21)01897-3Abstract Full Text Full Text PDF PubMed Google Scholar). While the virus encountered an immunologically naive human population, infections and expeditiously developed vaccines have shown to induce an adaptive immune response that can protect from SARS-CoV-2 infection and alleviate the severity of the SARS-CoV-2-associated coronavirus disease 2019 (COVID-19). Antibodies play a critical role in the adaptive immune response and are one of the most important correlates of protection in infectious diseases (Earle et al., 2021Earle K.A. Ambrosino D.M. Fiore-Gartland A. Goldblatt D. Gilbert P.B. Siber G.R. Dull P. Plotkin S.A. Evidence for antibody as a protective correlate for COVID-19 vaccines.Vaccine. 2021; 39: 4423-4428https://doi.org/10.1016/j.vaccine.2021.05.063Crossref PubMed Scopus (305) Google Scholar; Plotkin, 2010Plotkin S.A. Correlates of protection induced by vaccination.Clin. Vaccin. Immunol. 2010; 17: 1055-1065https://doi.org/10.1128/cvi.00131-10Crossref PubMed Scopus (0) Google Scholar). Secretion of monoclonal antibodies is accomplished by specialized immune cells (plasmablasts and plasma cells) that derive from activated B lymphocytes. To target a vast number of different pathogens, B cells undergo a sophisticated and strongly regulated process that includes the recombination of variable gene segments and introduction of somatic mutations (Imkeller and Wardemann, 2018Imkeller K. Wardemann H. Assessing human B cell repertoire diversity and convergence.Immunol. Rev. 2018; 284: 51-66https://doi.org/10.1111/imr.12670Crossref PubMed Scopus (23) Google Scholar; Victora and Nussenzweig, 2022Victora G.D. Nussenzweig M.C. Germinal centers.Annu. Rev. Immunol. 2022; 40: 413-442https://doi.org/10.1146/annurev-immunol-120419-022408Crossref PubMed Scopus (21) Google Scholar). As a result, a highly diverse antibody repertoire is encoded in the B lymphocyte and plasma cell compartments, enabling lasting production of pathogen-specific antibodies. A central feature of antibodies is their neutralizing function that blocks viral entry into target cells (Burton, 2002Burton D.R. Antibodies, viruses and vaccines.Nat. Rev. Immunol. 2002; 2: 706-713https://doi.org/10.1038/nri891Crossref PubMed Scopus (497) Google Scholar). Thereby, antibodies can prevent infection or limit viral burden through inhibition of viral propagation after infection. In addition, antibodies facilitate clearance of viruses and virus-infected cells via Fc-mediated effector functions, such as antibody-dependent cellular cytotoxicity exerted by natural killer (NK) cells (Bournazos and Ravetch, 2017Bournazos S. Ravetch J.V. Fcγ receptor function and the design of vaccination strategies.Immunity. 2017; 47: 224-233https://doi.org/10.1016/j.immuni.2017.07.009Abstract Full Text Full Text PDF PubMed Scopus (105) Google Scholar; Jost and Altfeld, 2013Jost S. Altfeld M. Control of human viral infections by natural killer cells.Annu. Rev. Immunol. 2013; 31: 163-194https://doi.org/10.1146/annurev-immunol-032712-100001Crossref PubMed Scopus (294) Google Scholar). Taking advantage of these powerful antiviral functions, transfer of neutralizing antibodies has been the leading principle behind the use of convalescent plasma or plasma-derived immunoglobulins for prevention and treatment of infectious diseases. While the concept of polyclonal antibody application dates back to the end of the 19th century, advanced B cell cloning methods have resulted in the isolation of highly potent and specific monoclonal antibodies targeting infectious pathogens (Corti et al., 2021Corti D. Purcell L.A. Snell G. Veesler D. Tackling COVID-19 with neutralizing monoclonal antibodies.Cell. 2021; 184: 3086-3108https://doi.org/10.1016/j.cell.2021.05.005Abstract Full Text Full Text PDF PubMed Scopus (122) Google Scholar, Gieselmann et al., 2021Gieselmann L. Kreer C. Ercanoglu M.S. Lehnen N. Zehner M. Schommers P. Potthoff J. Gruell H. Klein F. Effective high-throughput isolation of fully human antibodies targeting infectious pathogens.Nat. Protoc. 2021; 16: 3639-3671https://doi.org/10.1038/s41596-021-00554-wCrossref PubMed Scopus (6) Google Scholar, Klein et al., 2013Klein F. Mouquet H. Dosenovic P. Scheid J.F. Scharf L. Nussenzweig M.C. Antibodies in HIV-1 vaccine development and therapy.Science. 2013; 341: 1199-1204https://doi.org/10.1126/science.1241144Crossref PubMed Scopus (351) Google Scholar, Wardemann et al., 2003Wardemann H. Yurasov S. Schaefer A. Young J.W. Meffre E. Nussenzweig M.C. Predominant autoantibody production by early human B cell precursors.Science. 2003; 301: 1374-1377https://doi.org/10.1126/science.1086907Crossref PubMed Scopus (1495) Google Scholar). These include neutralizing antibodies that effectively prevent respiratory syncytial virus-associated disease or reduce mortality in Ebola-virus-infected individuals (Hammitt et al., 2022Hammitt L.L. Dagan R. Yuan Y. Baca Cots M. Bosheva M. Madhi S.A. Muller W.J. Zar H.J. Brooks D. Grenham A. et al.Nirsevimab for prevention of RSV in healthy late-preterm and term infants.N. Engl. J. Med. 2022; 386: 837-846https://doi.org/10.1056/nejmoa2110275Crossref PubMed Scopus (0) Google Scholar; Mulangu et al., 2019Mulangu S. Dodd L.E. Davey Jr., R.T. Tshiani Mbaya O. Proschan M. Mukadi D. Lusakibanza Manzo M. Nzolo D. Tshomba Oloma A. Ibanda A. et al.A randomized, controlled trial of ebola virus disease therapeutics.N. Engl. J. Med. 2019; 381: 2293-2303https://doi.org/10.1056/NEJMoa1910993Crossref PubMed Scopus (870) Google Scholar). While lifelong protective immunity induced by vaccination or infection has been demonstrated for viruses such as measles (Amanna et al., 2007Amanna I.J. Carlson N.E. Slifka M.K. Duration of humoral immunity to common viral and vaccine antigens.N. Engl. J. Med. 2007; 357: 1903-1915https://doi.org/10.1056/nejmoa066092Crossref PubMed Scopus (0) Google Scholar), immune-mediated protection from seasonal human coronaviruses (i.e., NL63, 229E, OC43, and HKU1) is known to be short-lived (Edridge et al., 2020Edridge A.W.D. Kaczorowska J. Hoste A.C.R. Bakker M. Klein M. Loens K. Jebbink M.F. Matser A. Kinsella C.M. Rueda P. et al.Seasonal coronavirus protective immunity is short-lasting.Nat. Med. 2020; 26: 1691-1693https://doi.org/10.1038/s41591-020-1083-1Crossref PubMed Scopus (372) Google Scholar). In addition to these differences in the dynamics of the immune and antibody response to different pathogens, viral evolution and the development of immune escape variants pose a significant challenge to antibody-mediated immunity. This became particularly apparent with the recent emergence of the SARS-CoV-2 Omicron variants that carry numerous spike mutations and evade a broad spectrum of neutralizing antibodies (Viana et al., 2022Viana R. Moyo S. Amoako D.G. Tegally H. Scheepers C. Althaus C.L. Anyaneji U.J. Bester P.A. Boni M.F. Chand M. et al.Rapid epidemic expansion of the SARS-CoV-2 Omicron variant in southern Africa.Nature. 2022; 603: 679-686https://doi.org/10.1038/s41586-022-04411-yCrossref PubMed Scopus (326) Google Scholar). This complex interaction of virus evolution and the virus-specific antibody response requires a detailed understanding of the development and function of SARS-CoV-2 neutralizing antibodies informing on successful future vaccine strategies as well as on the effective use of monoclonal antibodies in clinical applications. In this review, we aim to summarize the remarkable body of knowledge on SARS-CoV-2 neutralizing antibodies, ranging from their development in infected and vaccinated individuals to their mechanisms and demonstrated efficacy in prevention and treatment of COVID-19. B cell activation and differentiation into an antibody-secreting cell are initiated by the B cell receptor interaction with its cognate antigen (Figure 1). Given the high prevalence of immunity to endemic betacoronaviruses (e.g., HCoV-OC43), it was speculated whether B cell reactivity to SARS-CoV-2 may preexist in naive individuals and shape immunological outcomes of infection. Although SARS-CoV-2 binding antibodies could be observed in rare cases (Anderson et al., 2021Anderson E.M. Goodwin E.C. Verma A. Arevalo C.P. Bolton M.J. Weirick M.E. Gouma S. McAllister C.M. Christensen S.R. Weaver J. et al.Seasonal human coronavirus antibodies are boosted upon SARS-CoV-2 infection but not associated with protection.Cell. 2021; 184: 1858-1864.e10https://doi.org/10.1016/j.cell.2021.02.010Abstract Full Text Full Text PDF PubMed Scopus (160) Google Scholar; Ng et al., 2020Ng K.W. Faulkner N. Cornish G.H. Rosa A. Harvey R. Hussain S. Ulferts R. Earl C. Wrobel A.G. Benton D.J. et al.Preexisting and de novo humoral immunity to SARS-CoV-2 in humans.Science. 2020; 370: 1339-1343https://doi.org/10.1126/science.abe1107Crossref PubMed Scopus (391) Google Scholar) and monoclonal antibodies with low neutralizing activity have been reported in seronegative individuals (Feldman et al., 2021Feldman J. Bals J. Altomare C.G. St Denis K. Lam E.C. Hauser B.M. Ronsard L. Sangesland M. Moreno T.B. Okonkwo V. et al.Naive human B cells engage the receptor binding domain of SARS-CoV-2, variants of concern, and related sarbecoviruses.Sci. Immunol. 2021; 6: eabl5842https://doi.org/10.1126/sciimmunol.abl5842Crossref PubMed Scopus (9) Google Scholar), SARS-CoV-2 neutralizing activity was mostly undetectable in prepandemic samples (Ercanoglu et al., 2022Ercanoglu M.S. Gieselmann L. Dahling S. Poopalasingam N. Detmer S. Koch M. Korenkov M. Halwe S. Kluver M. Di Cristanziano V. et al.No substantial preexisting B cell immunity against SARS-CoV-2 in healthy adults.iScience. 2022; 25: 103951https://doi.org/10.1016/j.isci.2022.103951Abstract Full Text Full Text PDF PubMed Scopus (1) Google Scholar; Poston et al., 2021Poston D. Weisblum Y. Wise H. Templeton K. Jenks S. Hatziioannou T. Bieniasz P. Absence of severe acute respiratory syndrome coronavirus 2 neutralizing activity in prepandemic sera from individuals with recent seasonal coronavirus infection.Clin. Infect Dis. 2021; 73: e1208-e1211https://doi.org/10.1093/cid/ciaa1803Crossref PubMed Scopus (27) Google Scholar). However, upon exposure to SARS-CoV-2 antigen, activation of preexisting betacoronavirus-reactive B cells could be detected but was not associated with protection from SARS-CoV-2 infection (Anderson et al., 2021Anderson E.M. Goodwin E.C. Verma A. Arevalo C.P. Bolton M.J. Weirick M.E. Gouma S. McAllister C.M. Christensen S.R. Weaver J. et al.Seasonal human coronavirus antibodies are boosted upon SARS-CoV-2 infection but not associated with protection.Cell. 2021; 184: 1858-1864.e10https://doi.org/10.1016/j.cell.2021.02.010Abstract Full Text Full Text PDF PubMed Scopus (160) Google Scholar; Sokal et al., 2021Sokal A. Chappert P. Barba-Spaeth G. Roeser A. Fourati S. Azzaoui I. Vandenberghe A. Fernandez I. Meola A. Bouvier-Alias M. et al.Maturation and persistence of the anti-SARS-CoV-2 memory B cell response.Cell. 2021; 184: 1201-1213.e14https://doi.org/10.1016/j.cell.2021.01.050Abstract Full Text Full Text PDF PubMed Scopus (129) Google Scholar; Song et al., 2021Song G. He W.T. Callaghan S. Anzanello F. Huang D. Ricketts J. Torres J.L. Beutler N. Peng L. Vargas S. et al.Cross-reactive serum and memory B-cell responses to spike protein in SARS-CoV-2 and endemic coronavirus infection.Nat. Commun. 2021; 12: 2938https://doi.org/10.1038/s41467-021-23074-3Crossref PubMed Scopus (92) Google Scholar; Turner et al., 2021bTurner J.S. O'Halloran J.A. Kalaidina E. Kim W. Schmitz A.J. Zhou J.Q. Lei T. Thapa M. Chen R.E. Case J.B. et al.SARS-CoV-2 mRNA vaccines induce persistent human germinal centre responses.Nature. 2021; 596: 109-113https://doi.org/10.1038/s41586-021-03738-2Crossref PubMed Scopus (250) Google Scholar). Thus, rarely observed preexisting B cell cross-reactivity is unlikely to result in the development of a potent SARS-CoV-2 neutralizing response, although Fc-mediated functions of non-neutralizing antibodies might contribute to mitigate the course of the infection (Kaplonek et al., 2021Kaplonek P. Wang C. Bartsch Y. Fischinger S. Gorman M.J. Bowman K. Kang J. Dayal D. Martin P. Nowak R.P. et al.Early cross-coronavirus reactive signatures of humoral immunity against COVID-19.Sci. Immunol. 2021; 6: eabj2901https://doi.org/10.1126/sciimmunol.abj2901Crossref PubMed Scopus (23) Google Scholar). Following antigen contact, B cells are typically recruited into germinal centers in the B cell follicles of secondary lymphoid organs (e.g., lymph nodes or spleen). Within the germinal center, activated B cells proliferate, mutate, and compete for antigen and T cell help. This multifaceted process results in the development of affinity-matured and class-switched memory B cells as well as long-lived plasma cells (Akkaya et al., 2020Akkaya M. Kwak K. Pierce S.K. B cell memory: building two walls of protection against pathogens.Nat. Rev. Immunol. 2020; 20: 229-238https://doi.org/10.1038/s41577-019-0244-2Crossref PubMed Scopus (141) Google Scholar; Dorner and Radbruch, 2007Dorner T. Radbruch A. Antibodies and B cell memory in viral immunity.Immunity. 2007; 27: 384-392https://doi.org/10.1016/j.immuni.2007.09.002Abstract Full Text Full Text PDF PubMed Scopus (181) Google Scholar; Victora and Nussenzweig, 2022Victora G.D. Nussenzweig M.C. Germinal centers.Annu. Rev. Immunol. 2022; 40: 413-442https://doi.org/10.1146/annurev-immunol-120419-022408Crossref PubMed Scopus (21) Google Scholar). The human germinal center response to SARS-CoV-2 has been studied in some detail in vaccinated individuals through aspirates of draining lymph nodes, in which vaccine mRNA and spike antigen could be identified up to >8 weeks post-immunization (Röltgen et al., 2022Röltgen K. Nielsen S.C.A. Silva O. Younes S.F. Zaslavsky M. Costales C. Yang F. Wirz O.F. Solis D. Hoh R.A. et al.Immune imprinting, breadth of variant recognition, and germinal center response in human SARS-CoV-2 infection and vaccination.Cell. 2022; 185: 1025-1040.e14https://doi.org/10.1016/j.cell.2022.01.018Abstract Full Text Full Text PDF PubMed Scopus (46) Google Scholar). SARS-CoV-2-reactive germinal center B and T follicular helper cells became detectable within 2–3 weeks of immunization and were associated with the development of neutralizing antibodies (Lederer et al., 2022Lederer K. Bettini E. Parvathaneni K. Painter M.M. Agarwal D. Lundgreen K.A. Weirick M. Muralidharan K. Castano D. Goel R.R. et al.Germinal center responses to SARS-CoV-2 mRNA vaccines in healthy and immunocompromised individuals.Cell. 2022; 185: 1008-1024.e15https://doi.org/10.1016/j.cell.2022.01.027Abstract Full Text Full Text PDF PubMed Scopus (28) Google Scholar; Mudd et al., 2022Mudd P.A. Minervina A.A. Pogorelyy M.V. Turner J.S. Kim W. Kalaidina E. Petersen J. Schmitz A.J. Lei T. Haile A. et al.SJTRC Study TeamSARS-CoV-2 mRNA vaccination elicits a robust and persistent T follicular helper cell response in humans.Cell. 2022; 185: 603-613.e15https://doi.org/10.1016/j.cell.2021.12.026Abstract Full Text Full Text PDF PubMed Scopus (44) Google Scholar; Schmitz et al., 2021Schmitz A.J. Turner J.S. Liu Z. Zhou J.Q. Aziati I.D. Chen R.E. Joshi A. Bricker T.L. Darling T.L. Adelsberg D.C. et al.A vaccine-induced public antibody protects against SARS-CoV-2 and emerging variants.Immunity. 2021; 54: 2159-2166.e6https://doi.org/10.1016/j.immuni.2021.08.013Abstract Full Text Full Text PDF PubMed Scopus (23) Google Scholar; Turner et al., 2021bTurner J.S. O'Halloran J.A. Kalaidina E. Kim W. Schmitz A.J. Zhou J.Q. Lei T. Thapa M. Chen R.E. Case J.B. et al.SARS-CoV-2 mRNA vaccines induce persistent human germinal centre responses.Nature. 2021; 596: 109-113https://doi.org/10.1038/s41586-021-03738-2Crossref PubMed Scopus (250) Google Scholar). Indicating the persistence of this response, SARS-CoV-2-reactive germinal center cells and bone marrow plasma cells could be detected >6 months after the first immunization (Kim et al., 2022Kim W. Zhou J.Q. Horvath S.C. Schmitz A.J. Sturtz A.J. Lei T. Liu Z. Kalaidina E. Thapa M. Alsoussi W.B. et al.Germinal centre-driven maturation of B cell response to mRNA vaccination.Nature. 2022; 604: 141-145https://doi.org/10.1038/s41586-022-04527-1Crossref PubMed Scopus (39) Google Scholar; Mudd et al., 2022Mudd P.A. Minervina A.A. Pogorelyy M.V. Turner J.S. Kim W. Kalaidina E. Petersen J. Schmitz A.J. Lei T. Haile A. et al.SJTRC Study TeamSARS-CoV-2 mRNA vaccination elicits a robust and persistent T follicular helper cell response in humans.Cell. 2022; 185: 603-613.e15https://doi.org/10.1016/j.cell.2021.12.026Abstract Full Text Full Text PDF PubMed Scopus (44) Google Scholar). In contrast to longitudinal observations after vaccination, lymphoid follicle analyses after infection have largely been limited to post-mortem studies. In such fatal cases of COVID-19, disruptions and loss of germinal centers were repeatedly demonstrated (Kaneko et al., 2020Kaneko N. Kuo H.H. Boucau J. Farmer J.R. Allard-Chamard H. Mahajan V.S. Piechocka-Trocha A. Lefteri K. Osborn M. Bals J. et al.Massachusetts Consortium on Pathogen Readiness Specimen Working GroupLoss of Bcl-6-expressing T follicular helper cells and germinal centers in COVID-19.Cell. 2020; 183: 143-157.e13https://doi.org/10.1016/j.cell.2020.08.025Abstract Full Text Full Text PDF PubMed Scopus (332) Google Scholar; Röltgen et al., 2022Röltgen K. Nielsen S.C.A. Silva O. Younes S.F. Zaslavsky M. Costales C. Yang F. Wirz O.F. Solis D. Hoh R.A. et al.Immune imprinting, breadth of variant recognition, and germinal center response in human SARS-CoV-2 infection and vaccination.Cell. 2022; 185: 1025-1040.e14https://doi.org/10.1016/j.cell.2022.01.018Abstract Full Text Full Text PDF PubMed Scopus (46) Google Scholar). Moreover, severe COVID-19 was associated with extrafollicular germinal center-independent B cell responses that can result in short-lived plasma cells with low or no affinity maturation (Woodruff et al., 2020Woodruff M.C. Ramonell R.P. Nguyen D.C. Cashman K.S. Saini A.S. Haddad N.S. Ley A.M. 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• W4280517779 title "Antibody-mediated neutralization of SARS-CoV-2" @default.
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