A high-throughput, fully automated competition assay to evaluate SARS-CoV-2 neutralizing responses and epitope specificity in clinical samples

Abstract Coronavirus disease-2019 (COVID-19) remains a critical global health concern. We developed a fully automated, high-throughput competition immunoassay to elucidate how epitope recognition on the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) spike receptor-binding domain (RBD)...

Full description

Saved in:
Bibliographic Details
Main Authors: Yusuke Atarashi, Jeeeun Kim, Yasuhiro Irino, Masayuki Amano, Kiyoto Tsuchiya, Kenji Maeda, Mari Terada, Noriko Iwamoto, Shinya Shimada, Hiroaki Mitsuya, Masatoshi Yanagida, Yuki Takamatsu
Format: Article
Language:English
Published: Nature Portfolio 2025-04-01
Series:Scientific Reports
Subjects:
Online Access:https://doi.org/10.1038/s41598-025-94317-2
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849735010326675456
author Yusuke Atarashi
Jeeeun Kim
Yasuhiro Irino
Masayuki Amano
Kiyoto Tsuchiya
Kenji Maeda
Mari Terada
Noriko Iwamoto
Shinya Shimada
Hiroaki Mitsuya
Masatoshi Yanagida
Yuki Takamatsu
author_facet Yusuke Atarashi
Jeeeun Kim
Yasuhiro Irino
Masayuki Amano
Kiyoto Tsuchiya
Kenji Maeda
Mari Terada
Noriko Iwamoto
Shinya Shimada
Hiroaki Mitsuya
Masatoshi Yanagida
Yuki Takamatsu
author_sort Yusuke Atarashi
collection DOAJ
description Abstract Coronavirus disease-2019 (COVID-19) remains a critical global health concern. We developed a fully automated, high-throughput competition immunoassay to elucidate how epitope recognition on the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) spike receptor-binding domain (RBD) correlates with neutralizing activity. Analysis of clinical samples from both SARS-CoV-2-infected and vaccinated individuals revealed that vaccination elicits significantly higher antibody titers across multiple S1 subunit epitopes compared to natural infection. Notably, median antibody levels against the receptor-binding motif (RBM) exceeded 50% in both cohorts, highlighting the RBM as a key target for antibody induction irrespective of immune origin. Furthermore, the strongest correlation with neutralizing activity was observed for antibodies directed against the broader S1 subunit, indicating that epitopes outside the RBM also contribute to neutralization. These findings underscore the importance of both RBM- and non-RBM-directed antibodies in effective immune defense against SARS-CoV-2. Our assay enables large-scale, reliable quantification of neutralizing antibodies and provides critical insights for developing improved diagnostic antigens and vaccine strategies aimed at eliciting robust, multi-epitope immune responses.
format Article
id doaj-art-1deb9dfa172c4ea088d48ecd837223e5
institution DOAJ
issn 2045-2322
language English
publishDate 2025-04-01
publisher Nature Portfolio
record_format Article
series Scientific Reports
spelling doaj-art-1deb9dfa172c4ea088d48ecd837223e52025-08-20T03:07:40ZengNature PortfolioScientific Reports2045-23222025-04-011511710.1038/s41598-025-94317-2A high-throughput, fully automated competition assay to evaluate SARS-CoV-2 neutralizing responses and epitope specificity in clinical samplesYusuke Atarashi0Jeeeun Kim1Yasuhiro Irino2Masayuki Amano3Kiyoto Tsuchiya4Kenji Maeda5Mari Terada6Noriko Iwamoto7Shinya Shimada8Hiroaki Mitsuya9Masatoshi Yanagida10Yuki Takamatsu11Central Research Laboratories, Sysmex CorporationCentral Research Laboratories, Sysmex CorporationCentral Research Laboratories, Sysmex CorporationDepartment of Clinical Retrovirology, Joint Research Center for Human Retrovirus Infection, Kumamoto UniversityAIDS Clinical Center, Center hospital of the National Center for Global Health and MedicineRefractory Viral Diseases, National Center for Global Health and Medicine Research InstituteDepartment of Disease Control Center, Center Hospital of the National Center for Global Health and MedicineDepartment of Disease Control Center, Center Hospital of the National Center for Global Health and MedicineJapan Community Healthcare Organization, Kumamoto General HospitalRefractory Viral Diseases, National Center for Global Health and Medicine Research InstituteCentral Research Laboratories, Sysmex CorporationRefractory Viral Diseases, National Center for Global Health and Medicine Research InstituteAbstract Coronavirus disease-2019 (COVID-19) remains a critical global health concern. We developed a fully automated, high-throughput competition immunoassay to elucidate how epitope recognition on the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) spike receptor-binding domain (RBD) correlates with neutralizing activity. Analysis of clinical samples from both SARS-CoV-2-infected and vaccinated individuals revealed that vaccination elicits significantly higher antibody titers across multiple S1 subunit epitopes compared to natural infection. Notably, median antibody levels against the receptor-binding motif (RBM) exceeded 50% in both cohorts, highlighting the RBM as a key target for antibody induction irrespective of immune origin. Furthermore, the strongest correlation with neutralizing activity was observed for antibodies directed against the broader S1 subunit, indicating that epitopes outside the RBM also contribute to neutralization. These findings underscore the importance of both RBM- and non-RBM-directed antibodies in effective immune defense against SARS-CoV-2. Our assay enables large-scale, reliable quantification of neutralizing antibodies and provides critical insights for developing improved diagnostic antigens and vaccine strategies aimed at eliciting robust, multi-epitope immune responses.https://doi.org/10.1038/s41598-025-94317-2SARS-CoV-2High throughput testingAntibody testNeutralizing activity
spellingShingle Yusuke Atarashi
Jeeeun Kim
Yasuhiro Irino
Masayuki Amano
Kiyoto Tsuchiya
Kenji Maeda
Mari Terada
Noriko Iwamoto
Shinya Shimada
Hiroaki Mitsuya
Masatoshi Yanagida
Yuki Takamatsu
A high-throughput, fully automated competition assay to evaluate SARS-CoV-2 neutralizing responses and epitope specificity in clinical samples
Scientific Reports
SARS-CoV-2
High throughput testing
Antibody test
Neutralizing activity
title A high-throughput, fully automated competition assay to evaluate SARS-CoV-2 neutralizing responses and epitope specificity in clinical samples
title_full A high-throughput, fully automated competition assay to evaluate SARS-CoV-2 neutralizing responses and epitope specificity in clinical samples
title_fullStr A high-throughput, fully automated competition assay to evaluate SARS-CoV-2 neutralizing responses and epitope specificity in clinical samples
title_full_unstemmed A high-throughput, fully automated competition assay to evaluate SARS-CoV-2 neutralizing responses and epitope specificity in clinical samples
title_short A high-throughput, fully automated competition assay to evaluate SARS-CoV-2 neutralizing responses and epitope specificity in clinical samples
title_sort high throughput fully automated competition assay to evaluate sars cov 2 neutralizing responses and epitope specificity in clinical samples
topic SARS-CoV-2
High throughput testing
Antibody test
Neutralizing activity
url https://doi.org/10.1038/s41598-025-94317-2
work_keys_str_mv AT yusukeatarashi ahighthroughputfullyautomatedcompetitionassaytoevaluatesarscov2neutralizingresponsesandepitopespecificityinclinicalsamples
AT jeeeunkim ahighthroughputfullyautomatedcompetitionassaytoevaluatesarscov2neutralizingresponsesandepitopespecificityinclinicalsamples
AT yasuhiroirino ahighthroughputfullyautomatedcompetitionassaytoevaluatesarscov2neutralizingresponsesandepitopespecificityinclinicalsamples
AT masayukiamano ahighthroughputfullyautomatedcompetitionassaytoevaluatesarscov2neutralizingresponsesandepitopespecificityinclinicalsamples
AT kiyototsuchiya ahighthroughputfullyautomatedcompetitionassaytoevaluatesarscov2neutralizingresponsesandepitopespecificityinclinicalsamples
AT kenjimaeda ahighthroughputfullyautomatedcompetitionassaytoevaluatesarscov2neutralizingresponsesandepitopespecificityinclinicalsamples
AT mariterada ahighthroughputfullyautomatedcompetitionassaytoevaluatesarscov2neutralizingresponsesandepitopespecificityinclinicalsamples
AT norikoiwamoto ahighthroughputfullyautomatedcompetitionassaytoevaluatesarscov2neutralizingresponsesandepitopespecificityinclinicalsamples
AT shinyashimada ahighthroughputfullyautomatedcompetitionassaytoevaluatesarscov2neutralizingresponsesandepitopespecificityinclinicalsamples
AT hiroakimitsuya ahighthroughputfullyautomatedcompetitionassaytoevaluatesarscov2neutralizingresponsesandepitopespecificityinclinicalsamples
AT masatoshiyanagida ahighthroughputfullyautomatedcompetitionassaytoevaluatesarscov2neutralizingresponsesandepitopespecificityinclinicalsamples
AT yukitakamatsu ahighthroughputfullyautomatedcompetitionassaytoevaluatesarscov2neutralizingresponsesandepitopespecificityinclinicalsamples
AT yusukeatarashi highthroughputfullyautomatedcompetitionassaytoevaluatesarscov2neutralizingresponsesandepitopespecificityinclinicalsamples
AT jeeeunkim highthroughputfullyautomatedcompetitionassaytoevaluatesarscov2neutralizingresponsesandepitopespecificityinclinicalsamples
AT yasuhiroirino highthroughputfullyautomatedcompetitionassaytoevaluatesarscov2neutralizingresponsesandepitopespecificityinclinicalsamples
AT masayukiamano highthroughputfullyautomatedcompetitionassaytoevaluatesarscov2neutralizingresponsesandepitopespecificityinclinicalsamples
AT kiyototsuchiya highthroughputfullyautomatedcompetitionassaytoevaluatesarscov2neutralizingresponsesandepitopespecificityinclinicalsamples
AT kenjimaeda highthroughputfullyautomatedcompetitionassaytoevaluatesarscov2neutralizingresponsesandepitopespecificityinclinicalsamples
AT mariterada highthroughputfullyautomatedcompetitionassaytoevaluatesarscov2neutralizingresponsesandepitopespecificityinclinicalsamples
AT norikoiwamoto highthroughputfullyautomatedcompetitionassaytoevaluatesarscov2neutralizingresponsesandepitopespecificityinclinicalsamples
AT shinyashimada highthroughputfullyautomatedcompetitionassaytoevaluatesarscov2neutralizingresponsesandepitopespecificityinclinicalsamples
AT hiroakimitsuya highthroughputfullyautomatedcompetitionassaytoevaluatesarscov2neutralizingresponsesandepitopespecificityinclinicalsamples
AT masatoshiyanagida highthroughputfullyautomatedcompetitionassaytoevaluatesarscov2neutralizingresponsesandepitopespecificityinclinicalsamples
AT yukitakamatsu highthroughputfullyautomatedcompetitionassaytoevaluatesarscov2neutralizingresponsesandepitopespecificityinclinicalsamples