In vitro and in vivo functions of SARS-CoV-2 infection-enhancing and neutralizing antibodies

SARS-CoV-2-neutralizing antibodies (NAbs) protect against COVID-19. A concern regarding SARS-CoV-2 antibodies is whether they mediate disease enhancement. Here, we isolated NAbs against the receptor-binding domain (RBD) or the N-terminal domain (NTD) of SARS-CoV-2 spike from individuals with acute o...

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Vydáno v:Cell Ročník 184; číslo 16; s. 4203
Hlavní autoři: Li, Dapeng, Edwards, Robert J, Manne, Kartik, Martinez, David R, Schäfer, Alexandra, Alam, S Munir, Wiehe, Kevin, Lu, Xiaozhi, Parks, Robert, Sutherland, Laura L, Oguin, 3rd, Thomas H, McDanal, Charlene, Perez, Lautaro G, Mansouri, Katayoun, Gobeil, Sophie M C, Janowska, Katarzyna, Stalls, Victoria, Kopp, Megan, Cai, Fangping, Lee, Esther, Foulger, Andrew, Hernandez, Giovanna E, Sanzone, Aja, Tilahun, Kedamawit, Jiang, Chuancang, Tse, Longping V, Bock, Kevin W, Minai, Mahnaz, Nagata, Bianca M, Cronin, Kenneth, Gee-Lai, Victoria, Deyton, Margaret, Barr, Maggie, Von Holle, Tarra, Macintyre, Andrew N, Stover, Erica, Feldman, Jared, Hauser, Blake M, Caradonna, Timothy M, Scobey, Trevor D, Rountree, Wes, Wang, Yunfei, Moody, M Anthony, Cain, Derek W, DeMarco, C Todd, Denny, Thomas N, Woods, Christopher W, Petzold, Elizabeth W, Schmidt, Aaron G, Teng, I-Ting, Zhou, Tongqing, Kwong, Peter D, Mascola, John R, Graham, Barney S, Moore, Ian N, Seder, Robert, Andersen, Hanne, Lewis, Mark G, Montefiori, David C, Sempowski, Gregory D, Baric, Ralph S, Acharya, Priyamvada, Haynes, Barton F, Saunders, Kevin O
Médium: Journal Article
Jazyk:angličtina
Vydáno: United States 05.08.2021
Témata:
ISSN:1097-4172, 1097-4172
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Abstract SARS-CoV-2-neutralizing antibodies (NAbs) protect against COVID-19. A concern regarding SARS-CoV-2 antibodies is whether they mediate disease enhancement. Here, we isolated NAbs against the receptor-binding domain (RBD) or the N-terminal domain (NTD) of SARS-CoV-2 spike from individuals with acute or convalescent SARS-CoV-2 or a history of SARS-CoV infection. Cryo-electron microscopy of RBD and NTD antibodies demonstrated function-specific modes of binding. Select RBD NAbs also demonstrated Fc receptor-γ (FcγR)-mediated enhancement of virus infection in vitro, while five non-neutralizing NTD antibodies mediated FcγR-independent in vitro infection enhancement. However, both types of infection-enhancing antibodies protected from SARS-CoV-2 replication in monkeys and mice. Three of 46 monkeys infused with enhancing antibodies had higher lung inflammation scores compared to controls. One monkey had alveolar edema and elevated bronchoalveolar lavage inflammatory cytokines. Thus, while in vitro antibody-enhanced infection does not necessarily herald enhanced infection in vivo, increased lung inflammation can rarely occur in SARS-CoV-2 antibody-infused macaques.
AbstractList SARS-CoV-2-neutralizing antibodies (NAbs) protect against COVID-19. A concern regarding SARS-CoV-2 antibodies is whether they mediate disease enhancement. Here, we isolated NAbs against the receptor-binding domain (RBD) or the N-terminal domain (NTD) of SARS-CoV-2 spike from individuals with acute or convalescent SARS-CoV-2 or a history of SARS-CoV infection. Cryo-electron microscopy of RBD and NTD antibodies demonstrated function-specific modes of binding. Select RBD NAbs also demonstrated Fc receptor-γ (FcγR)-mediated enhancement of virus infection in vitro, while five non-neutralizing NTD antibodies mediated FcγR-independent in vitro infection enhancement. However, both types of infection-enhancing antibodies protected from SARS-CoV-2 replication in monkeys and mice. Three of 46 monkeys infused with enhancing antibodies had higher lung inflammation scores compared to controls. One monkey had alveolar edema and elevated bronchoalveolar lavage inflammatory cytokines. Thus, while in vitro antibody-enhanced infection does not necessarily herald enhanced infection in vivo, increased lung inflammation can rarely occur in SARS-CoV-2 antibody-infused macaques.
SARS-CoV-2-neutralizing antibodies (NAbs) protect against COVID-19. A concern regarding SARS-CoV-2 antibodies is whether they mediate disease enhancement. Here, we isolated NAbs against the receptor-binding domain (RBD) or the N-terminal domain (NTD) of SARS-CoV-2 spike from individuals with acute or convalescent SARS-CoV-2 or a history of SARS-CoV infection. Cryo-electron microscopy of RBD and NTD antibodies demonstrated function-specific modes of binding. Select RBD NAbs also demonstrated Fc receptor-γ (FcγR)-mediated enhancement of virus infection in vitro, while five non-neutralizing NTD antibodies mediated FcγR-independent in vitro infection enhancement. However, both types of infection-enhancing antibodies protected from SARS-CoV-2 replication in monkeys and mice. Three of 46 monkeys infused with enhancing antibodies had higher lung inflammation scores compared to controls. One monkey had alveolar edema and elevated bronchoalveolar lavage inflammatory cytokines. Thus, while in vitro antibody-enhanced infection does not necessarily herald enhanced infection in vivo, increased lung inflammation can rarely occur in SARS-CoV-2 antibody-infused macaques.SARS-CoV-2-neutralizing antibodies (NAbs) protect against COVID-19. A concern regarding SARS-CoV-2 antibodies is whether they mediate disease enhancement. Here, we isolated NAbs against the receptor-binding domain (RBD) or the N-terminal domain (NTD) of SARS-CoV-2 spike from individuals with acute or convalescent SARS-CoV-2 or a history of SARS-CoV infection. Cryo-electron microscopy of RBD and NTD antibodies demonstrated function-specific modes of binding. Select RBD NAbs also demonstrated Fc receptor-γ (FcγR)-mediated enhancement of virus infection in vitro, while five non-neutralizing NTD antibodies mediated FcγR-independent in vitro infection enhancement. However, both types of infection-enhancing antibodies protected from SARS-CoV-2 replication in monkeys and mice. Three of 46 monkeys infused with enhancing antibodies had higher lung inflammation scores compared to controls. One monkey had alveolar edema and elevated bronchoalveolar lavage inflammatory cytokines. Thus, while in vitro antibody-enhanced infection does not necessarily herald enhanced infection in vivo, increased lung inflammation can rarely occur in SARS-CoV-2 antibody-infused macaques.
Author Schmidt, Aaron G
Gee-Lai, Victoria
Foulger, Andrew
Parks, Robert
Hernandez, Giovanna E
Macintyre, Andrew N
Haynes, Barton F
Sanzone, Aja
Caradonna, Timothy M
Mascola, John R
Barr, Maggie
Denny, Thomas N
Graham, Barney S
Cronin, Kenneth
Hauser, Blake M
DeMarco, C Todd
Minai, Mahnaz
Stalls, Victoria
Schäfer, Alexandra
Saunders, Kevin O
Oguin, 3rd, Thomas H
Acharya, Priyamvada
Feldman, Jared
Lu, Xiaozhi
Martinez, David R
Sutherland, Laura L
Moore, Ian N
Manne, Kartik
Jiang, Chuancang
Wang, Yunfei
Petzold, Elizabeth W
Zhou, Tongqing
Alam, S Munir
Bock, Kevin W
Tse, Longping V
Wiehe, Kevin
Montefiori, David C
Edwards, Robert J
Cain, Derek W
Kwong, Peter D
Kopp, Megan
Stover, Erica
Scobey, Trevor D
Mansouri, Katayoun
Janowska, Katarzyna
Deyton, Margaret
McDanal, Charlene
Woods, Christopher W
Moody, M Anthony
Teng, I-Ting
Cai, Fangping
Sempowski, Gregory D
Nagata, Bianca M
Lewis, Mark G
Tilahun, Kedamawit
Lee, Esther
Andersen, Hanne
Perez, Lautaro G
Von Holle, Tarra
Baric, Ralph S
Li, Dapeng
Gobeil, Sophie M C
Seder, Robert
Rountree, Wes
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  surname: Andersen
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  organization: BIOQUAL, Rockville, MD 20850, USA
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  surname: Montefiori
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  givenname: Gregory D
  surname: Sempowski
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  organization: Duke Human Vaccine Institute, Duke University School of Medicine, Durham, NC 27710, USA; Department of Medicine, Duke University School of Medicine, Durham, NC 27710, USA
– sequence: 61
  givenname: Ralph S
  surname: Baric
  fullname: Baric, Ralph S
  organization: Department of Epidemiology, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599, USA
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  givenname: Priyamvada
  surname: Acharya
  fullname: Acharya, Priyamvada
  organization: Duke Human Vaccine Institute, Duke University School of Medicine, Durham, NC 27710, USA; Department of Surgery, Duke University, Durham, NC 27710, USA
– sequence: 63
  givenname: Barton F
  surname: Haynes
  fullname: Haynes, Barton F
  email: barton.haynes@duke.edu
  organization: Duke Human Vaccine Institute, Duke University School of Medicine, Durham, NC 27710, USA; Department of Medicine, Duke University School of Medicine, Durham, NC 27710, USA; Department of Immunology, Duke University School of Medicine, Durham, NC 27710, USA. Electronic address: barton.haynes@duke.edu
– sequence: 64
  givenname: Kevin O
  surname: Saunders
  fullname: Saunders, Kevin O
  email: kevin.saunders@duke.edu
  organization: Duke Human Vaccine Institute, Duke University School of Medicine, Durham, NC 27710, USA; Department of Surgery, Duke University, Durham, NC 27710, USA; Department of Immunology, Duke University School of Medicine, Durham, NC 27710, USA; Department of Molecular Genetics and Microbiology, Duke University School of Medicine, Durham, NC 27710, USA. Electronic address: kevin.saunders@duke.edu
BackLink https://www.ncbi.nlm.nih.gov/pubmed/34242577$$D View this record in MEDLINE/PubMed
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Keywords COVID-19
electron micrograph
SARS-CoV-2
cross-neutralization
receptor-binding domain
neutralizing antibody
N-terminal domain
antibody-dependent enhancement
infection enhancement
in vivo protection
Language English
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PublicationTitle Cell
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Snippet SARS-CoV-2-neutralizing antibodies (NAbs) protect against COVID-19. A concern regarding SARS-CoV-2 antibodies is whether they mediate disease enhancement....
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StartPage 4203
SubjectTerms Animals
Antibodies, Neutralizing - immunology
Antibodies, Viral - immunology
Bronchoalveolar Lavage Fluid - chemistry
COVID-19 - pathology
COVID-19 - virology
Cytokines - metabolism
Female
Haplorhini
Humans
Lung - pathology
Lung - virology
Male
Mice
Mice, Inbred BALB C
Protein Domains
Receptors, IgG - metabolism
SARS-CoV-2 - isolation & purification
SARS-CoV-2 - physiology
Spike Glycoprotein, Coronavirus - chemistry
Spike Glycoprotein, Coronavirus - immunology
Viral Load
Virus Replication
Title In vitro and in vivo functions of SARS-CoV-2 infection-enhancing and neutralizing antibodies
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