Antibody Avidity Maturation Following Recovery From Infection or the Booster Vaccination Grants Breadth of SARS-CoV-2 Neutralizing Capacity.


Journal

The Journal of infectious diseases
ISSN: 1537-6613
Titre abrégé: J Infect Dis
Pays: United States
ID NLM: 0413675

Informations de publication

Date de publication:
28 03 2023
Historique:
received: 27 09 2022
accepted: 21 12 2022
medline: 29 3 2023
pubmed: 23 12 2022
entrez: 22 12 2022
Statut: ppublish

Résumé

Cross-neutralizing capacity of antibodies against severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) variants is important in mitigating (re-)exposures. Role of antibody maturation, the process whereby selection of higher affinity antibodies augments host immunity, to determine SARS-CoV-2 neutralizing capacity was investigated. Sera from SARS-CoV-2 convalescents at 2, 6, or 10 months postrecovery, and BNT162b2 vaccine recipients at 3 or 25 weeks postvaccination, were analyzed. Anti-spike IgG avidity was measured in urea-treated ELISAs. Neutralizing capacity was assessed by surrogate neutralization assays. Fold change between variant and wild-type neutralization inferred the breadth of neutralizing capacity. Compared with early-convalescent, avidity indices of late-convalescent sera were significantly higher (median, 37.7 [interquartile range 28.4-45.1] vs 64.9 [57.5-71.5], P < .0001). Urea-resistant, high-avidity IgG best predicted neutralizing capacity (Spearman r = 0.49 vs 0.67 [wild-type]; 0.18-0.52 vs 0.48-0.83 [variants]). Higher-avidity convalescent sera better cross-neutralized SARS-CoV-2 variants (P < .001 [Alpha]; P < .01 [Delta and Omicron]). Vaccinees only experienced meaningful avidity maturation following the booster dose, exhibiting rather limited cross-neutralizing capacity at week 25. Avidity maturation was progressive beyond acute recovery from infection, or became apparent after the booster vaccine dose, granting broader anti-SARS-CoV-2 neutralizing capacity. Understanding the maturation kinetics of the 2 building blocks of anti-SARS-CoV-2 humoral immunity is crucial.

Sections du résumé

BACKGROUND
Cross-neutralizing capacity of antibodies against severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) variants is important in mitigating (re-)exposures. Role of antibody maturation, the process whereby selection of higher affinity antibodies augments host immunity, to determine SARS-CoV-2 neutralizing capacity was investigated.
METHODS
Sera from SARS-CoV-2 convalescents at 2, 6, or 10 months postrecovery, and BNT162b2 vaccine recipients at 3 or 25 weeks postvaccination, were analyzed. Anti-spike IgG avidity was measured in urea-treated ELISAs. Neutralizing capacity was assessed by surrogate neutralization assays. Fold change between variant and wild-type neutralization inferred the breadth of neutralizing capacity.
RESULTS
Compared with early-convalescent, avidity indices of late-convalescent sera were significantly higher (median, 37.7 [interquartile range 28.4-45.1] vs 64.9 [57.5-71.5], P < .0001). Urea-resistant, high-avidity IgG best predicted neutralizing capacity (Spearman r = 0.49 vs 0.67 [wild-type]; 0.18-0.52 vs 0.48-0.83 [variants]). Higher-avidity convalescent sera better cross-neutralized SARS-CoV-2 variants (P < .001 [Alpha]; P < .01 [Delta and Omicron]). Vaccinees only experienced meaningful avidity maturation following the booster dose, exhibiting rather limited cross-neutralizing capacity at week 25.
CONCLUSIONS
Avidity maturation was progressive beyond acute recovery from infection, or became apparent after the booster vaccine dose, granting broader anti-SARS-CoV-2 neutralizing capacity. Understanding the maturation kinetics of the 2 building blocks of anti-SARS-CoV-2 humoral immunity is crucial.

Identifiants

pubmed: 36546706
pii: 6955885
doi: 10.1093/infdis/jiac492
pmc: PMC10044078
doi:

Substances chimiques

BNT162 Vaccine 0
Urea 8W8T17847W
Immunoglobulin G 0
Antibodies, Neutralizing 0
Antibodies, Viral 0
Spike Glycoprotein, Coronavirus 0
spike protein, SARS-CoV-2 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

780-787

Informations de copyright

© The Author(s) 2022. Published by Oxford University Press on behalf of Infectious Diseases Society of America.

Déclaration de conflit d'intérêts

Conflict of Interest. Y. N. and Y. K. report equity ownership of Quantum Molecular Diagnostics, an Osaka Metropolitan University spinout targeting infectious diseases to develop innovative diagnostics. Y. N. and Y. K. also report receiving financial support outside of this work from Abbott Japan LLC, Japan.

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Auteurs

Yu Nakagama (Y)

Department of Virology and Parasitology, Graduate School of Medicine, Osaka Metropolitan University, Osaka, Japan.
Research Center for Infectious Disease Sciences, Graduate School of Medicine, Osaka Metropolitan University, Osaka, Japan.

Katherine Candray (K)

Department of Virology and Parasitology, Graduate School of Medicine, Osaka Metropolitan University, Osaka, Japan.
Research Center for Infectious Disease Sciences, Graduate School of Medicine, Osaka Metropolitan University, Osaka, Japan.
Centro Nacional de Investigaciones Científicas de El Salvador, San Salvador, El Salvador.

Natsuko Kaku (N)

Department of Virology and Parasitology, Graduate School of Medicine, Osaka Metropolitan University, Osaka, Japan.
Research Center for Infectious Disease Sciences, Graduate School of Medicine, Osaka Metropolitan University, Osaka, Japan.

Yuko Komase (Y)

Department of Respiratory Internal Medicine, St Marianna University, Yokohama Seibu Hospital, Yokohama, Japan.

Maria-Virginia Rodriguez-Funes (MV)

National Rosales Hospital, San Salvador, El Salvador.

Rhina Dominguez (R)

El Salvador National Institute of Health, San Salvador, El Salvador.

Tomoya Tsuchida (T)

Division of General Internal Medicine, St Marianna University School of Medicine, Kawasaki, Japan.

Hiroyuki Kunishima (H)

Department of Infectious Diseases, St Marianna University School of Medicine, Kawasaki, Japan.

Etsuko Nagai (E)

Department of Infectious Diseases and Applied Immunology, Institute of Medical Science, The University of Tokyo, Tokyo, Japan.

Eisuke Adachi (E)

Department of Infectious Diseases and Applied Immunology, Institute of Medical Science, The University of Tokyo, Tokyo, Japan.

Dieudonné Mumba Ngoyi (DM)

Institut National de Recherche Biomedicale, Kinshasa, Democratic Republic of the Congo.

Mari Yamasue (M)

Department of Respiratory Medicine and Infectious Diseases, Oita University Faculty of Medicine, Oita, Japan.

Kosaku Komiya (K)

Department of Respiratory Medicine and Infectious Diseases, Oita University Faculty of Medicine, Oita, Japan.

Kazufumi Hiramatsu (K)

Department of Respiratory Medicine and Infectious Diseases, Oita University Faculty of Medicine, Oita, Japan.

Naoto Uemura (N)

Department of Respiratory Medicine and Infectious Diseases, Oita University Faculty of Medicine, Oita, Japan.

Yuki Sugiura (Y)

Center for Cancer Immunotherapy and Immunobiology, Kyoto University Graduate School of Medicine, Kyoto, Japan.

Mayo Yasugi (M)

Graduate School of Veterinary Science, Osaka Metropolitan University, Osaka, Japan.
Asian Health Science Research Institute, Osaka Metropolitan University, Osaka, Japan.
Osaka International Research Center for Infectious Diseases, Osaka Metropolitan University, Osaka, Japan.

Yuka Yamagishi (Y)

Department of Clinical Infectious Diseases, Aichi Medical University, Aichi, Japan.

Hiroshige Mikamo (H)

Department of Clinical Infectious Diseases, Aichi Medical University, Aichi, Japan.

Satoshi Shiraishi (S)

Department of Respiratory Medicine, Osaka City Juso Hospital, Osaka, Japan.

Takehiro Izumo (T)

Department of Respiratory Medicine, Japanese Red Cross Medical Center, Tokyo, Japan.

Sachie Nakagama (S)

Department of Virology and Parasitology, Graduate School of Medicine, Osaka Metropolitan University, Osaka, Japan.
Research Center for Infectious Disease Sciences, Graduate School of Medicine, Osaka Metropolitan University, Osaka, Japan.

Chihiro Watanabe (C)

Department of Virology and Parasitology, Graduate School of Medicine, Osaka Metropolitan University, Osaka, Japan.
Research Center for Infectious Disease Sciences, Graduate School of Medicine, Osaka Metropolitan University, Osaka, Japan.

Yuko Nitahara (Y)

Department of Virology and Parasitology, Graduate School of Medicine, Osaka Metropolitan University, Osaka, Japan.
Research Center for Infectious Disease Sciences, Graduate School of Medicine, Osaka Metropolitan University, Osaka, Japan.

Evariste Tshibangu-Kabamba (E)

Department of Virology and Parasitology, Graduate School of Medicine, Osaka Metropolitan University, Osaka, Japan.
Research Center for Infectious Disease Sciences, Graduate School of Medicine, Osaka Metropolitan University, Osaka, Japan.

Hiroshi Kakeya (H)

Department of Virology and Parasitology, Graduate School of Medicine, Osaka Metropolitan University, Osaka, Japan.
Department of Infection Control Science, Graduate School of Medicine, Osaka Metropolitan University, Osaka, Japan.

Yasutoshi Kido (Y)

Department of Virology and Parasitology, Graduate School of Medicine, Osaka Metropolitan University, Osaka, Japan.
Research Center for Infectious Disease Sciences, Graduate School of Medicine, Osaka Metropolitan University, Osaka, Japan.

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