Neutralizing nanobodies against SARS-CoV-2 recognizing highly conserved epitopes at the Spike's S2 subunit

The formation of a six-helix bundle between the conserved heptad-repeat regions 1 and 2 (HR1 and HR2) in SARS-CoV-2 Spike's S2 subunit is essential for membrane fusion and represents a promising therapeutic target. Previously, we reported recombinant proteins named CoVS-HR1, which mimic the HR1...

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Autores: Polo-Megías, Daniel, Cano-Muñoz, Mario, Trolese, Philipp, Lestani, Sara, la Rocchia, Ilaria, Pierangelini, Andrea, Fongaro, Benedetta, de Laureto, P. P., Morales-Yánez, Francisco J., Vaneyck, Jonathan, Vanderplasschen, Alain F. C., Decoville, Thomas, Laumond, Géraldine, Salinas-García, M. C., Cámara-Artigas, Ana, Gavira Gallardo, J. A., Moog, Christiane, Dumoulin, Mireille, Conejero-Lara, Francisco
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2026
País:España
Institución:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/420254
Acceso en línea:http://hdl.handle.net/10261/420254
Access Level:acceso abierto
Palabra clave:Isothermal titration calorimetry
Single-domain antibodies (sdAbs)
X-ray crystallography
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network_acronym_str ES
network_name_str España
repository_id_str
dc.title.none.fl_str_mv Neutralizing nanobodies against SARS-CoV-2 recognizing highly conserved epitopes at the Spike's S2 subunit
title Neutralizing nanobodies against SARS-CoV-2 recognizing highly conserved epitopes at the Spike's S2 subunit
spellingShingle Neutralizing nanobodies against SARS-CoV-2 recognizing highly conserved epitopes at the Spike's S2 subunit
Polo-Megías, Daniel
Isothermal titration calorimetry
Single-domain antibodies (sdAbs)
X-ray crystallography
title_short Neutralizing nanobodies against SARS-CoV-2 recognizing highly conserved epitopes at the Spike's S2 subunit
title_full Neutralizing nanobodies against SARS-CoV-2 recognizing highly conserved epitopes at the Spike's S2 subunit
title_fullStr Neutralizing nanobodies against SARS-CoV-2 recognizing highly conserved epitopes at the Spike's S2 subunit
title_full_unstemmed Neutralizing nanobodies against SARS-CoV-2 recognizing highly conserved epitopes at the Spike's S2 subunit
title_sort Neutralizing nanobodies against SARS-CoV-2 recognizing highly conserved epitopes at the Spike's S2 subunit
dc.creator.none.fl_str_mv Polo-Megías, Daniel
Cano-Muñoz, Mario
Trolese, Philipp
Lestani, Sara
la Rocchia, Ilaria
Pierangelini, Andrea
Fongaro, Benedetta
de Laureto, P. P.
Morales-Yánez, Francisco J.
Vaneyck, Jonathan
Vanderplasschen, Alain F. C.
Decoville, Thomas
Laumond, Géraldine
Salinas-García, M. C.
Cámara-Artigas, Ana
Gavira Gallardo, J. A.
Moog, Christiane
Dumoulin, Mireille
Conejero-Lara, Francisco
author Polo-Megías, Daniel
author_facet Polo-Megías, Daniel
Cano-Muñoz, Mario
Trolese, Philipp
Lestani, Sara
la Rocchia, Ilaria
Pierangelini, Andrea
Fongaro, Benedetta
de Laureto, P. P.
Morales-Yánez, Francisco J.
Vaneyck, Jonathan
Vanderplasschen, Alain F. C.
Decoville, Thomas
Laumond, Géraldine
Salinas-García, M. C.
Cámara-Artigas, Ana
Gavira Gallardo, J. A.
Moog, Christiane
Dumoulin, Mireille
Conejero-Lara, Francisco
author_role author
author2 Cano-Muñoz, Mario
Trolese, Philipp
Lestani, Sara
la Rocchia, Ilaria
Pierangelini, Andrea
Fongaro, Benedetta
de Laureto, P. P.
Morales-Yánez, Francisco J.
Vaneyck, Jonathan
Vanderplasschen, Alain F. C.
Decoville, Thomas
Laumond, Géraldine
Salinas-García, M. C.
Cámara-Artigas, Ana
Gavira Gallardo, J. A.
Moog, Christiane
Dumoulin, Mireille
Conejero-Lara, Francisco
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Agencia Estatal de Investigación (España)
European Commission
Ministerio de Ciencia e Innovación (España)
Ministerio de Ciencia, Innovación y Universidades (España)
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv Isothermal titration calorimetry
Single-domain antibodies (sdAbs)
X-ray crystallography
topic Isothermal titration calorimetry
Single-domain antibodies (sdAbs)
X-ray crystallography
description The formation of a six-helix bundle between the conserved heptad-repeat regions 1 and 2 (HR1 and HR2) in SARS-CoV-2 Spike's S2 subunit is essential for membrane fusion and represents a promising therapeutic target. Previously, we reported recombinant proteins named CoVS-HR1, which mimic the HR1 region and block its interaction with HR2, inhibiting viral fusion. Moreover, they are recognized by plasma antibodies from COVID-19 convalescent patients. In this work, we generated camelid heavy-chain-only antibody fragments (VHHs), also named nanobodies (NBs), against a CoVS-HR1 variant mimicking the full HR1 region. A first generation of selected NBs bound HR1 with high affinity and competed with HR2. Notably, this set of NBs exclusively recognized the C-terminal half of HR1, and two of them showed mild neutralizing activity in cell infection assays. Using a truncated CoVS-HR1 variant (N2C), we selected a second generation of NBs targeting specifically the N-terminal half of HR1. However, these NBs did not demonstrate neutralizing activity, possibly due to their low binding affinities. Several NB epitopes were delineated by hydrogen‑deuterium exchange and mass spectrometry analysis, and the crystal structure of a ternary complex between an HR1-mimetic protein and two NBs was determined, confirming competition with HR2. Intriguingly, we found cooperative binding effects between NBs targeting each half of HR1, but these did not result in detectable inhibitory synergy. These findings demonstrate the existence of neutralizing epitopes in the S2 HR1 region and provide a foundation for future development of enhanced neutralizing NBs focused on specific epitopes using HR1-mimetic proteins.
publishDate 2026
dc.date.none.fl_str_mv 2026
2026
2026
2026
dc.type.none.fl_str_mv info:eu-repo/semantics/article
http://purl.org/coar/resource_type/c_6501
Publisher's version
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/420254
url http://hdl.handle.net/10261/420254
dc.relation.none.fl_str_mv #PLACEHOLDER_PARENT_METADATA_VALUE#
#PLACEHOLDER_PARENT_METADATA_VALUE#
info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2019-107515RB-C21
info:eu-repo/grantAgreement/EC/H2020/681032
http://dx.doi.org/10.1016/j.ijbiomac.2025.150022

dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.publisher.none.fl_str_mv Elsevier BV
publisher.none.fl_str_mv Elsevier BV
dc.source.none.fl_str_mv reponame:DIGITAL.CSIC. Repositorio Institucional del CSIC
instname:Consejo Superior de Investigaciones Científicas (CSIC)
instname_str Consejo Superior de Investigaciones Científicas (CSIC)
reponame_str DIGITAL.CSIC. Repositorio Institucional del CSIC
collection DIGITAL.CSIC. Repositorio Institucional del CSIC
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spelling Neutralizing nanobodies against SARS-CoV-2 recognizing highly conserved epitopes at the Spike's S2 subunitPolo-Megías, DanielCano-Muñoz, MarioTrolese, PhilippLestani, Sarala Rocchia, IlariaPierangelini, AndreaFongaro, Benedettade Laureto, P. P.Morales-Yánez, Francisco J.Vaneyck, JonathanVanderplasschen, Alain F. C.Decoville, ThomasLaumond, GéraldineSalinas-García, M. C.Cámara-Artigas, AnaGavira Gallardo, J. A.Moog, ChristianeDumoulin, MireilleConejero-Lara, FranciscoIsothermal titration calorimetrySingle-domain antibodies (sdAbs)X-ray crystallographyThe formation of a six-helix bundle between the conserved heptad-repeat regions 1 and 2 (HR1 and HR2) in SARS-CoV-2 Spike's S2 subunit is essential for membrane fusion and represents a promising therapeutic target. Previously, we reported recombinant proteins named CoVS-HR1, which mimic the HR1 region and block its interaction with HR2, inhibiting viral fusion. Moreover, they are recognized by plasma antibodies from COVID-19 convalescent patients. In this work, we generated camelid heavy-chain-only antibody fragments (VHHs), also named nanobodies (NBs), against a CoVS-HR1 variant mimicking the full HR1 region. A first generation of selected NBs bound HR1 with high affinity and competed with HR2. Notably, this set of NBs exclusively recognized the C-terminal half of HR1, and two of them showed mild neutralizing activity in cell infection assays. Using a truncated CoVS-HR1 variant (N2C), we selected a second generation of NBs targeting specifically the N-terminal half of HR1. However, these NBs did not demonstrate neutralizing activity, possibly due to their low binding affinities. Several NB epitopes were delineated by hydrogen‑deuterium exchange and mass spectrometry analysis, and the crystal structure of a ternary complex between an HR1-mimetic protein and two NBs was determined, confirming competition with HR2. Intriguingly, we found cooperative binding effects between NBs targeting each half of HR1, but these did not result in detectable inhibitory synergy. These findings demonstrate the existence of neutralizing epitopes in the S2 HR1 region and provide a foundation for future development of enhanced neutralizing NBs focused on specific epitopes using HR1-mimetic proteins.This research was funded by grant PID2019.107515RB.C21 from the Spanish State Research Agency (SRA/10.13039/501100011033). Additional support was provided by ANRS (Agence Nationale de Recherches sur le SIDA et les hépatites virales), the Investissements d'Avenir program administered by the ANR (grant ANR-10-LABX-77), and EHVA (Grant No. 681032, Horizon 2020), with co-funding from the ERDF/ESF under the initiatives “A way to make Europe” and “Investing in your future.” We are also grateful to the Andalusian Regional Government for the predoctoral fellowship awarded to Daniel Polo-Megías. Mario Cano-Muñoz was supported by a Postdoctoral Research Program from the Spanish Research Agency: Juan de la Cierva (JDC2022-049681-I). Francisco Morales-Yáñez was supported by a COS-R funding from the University of Liège. Jonathan Vaneyck was supported by CIP funding. Mireille Dumoulin is a research associate from the FRS-FNRS. We are grateful to the Spanish Radiation Synchrotron Source (ALBA), Barcelona, Spain, and the European Synchrotron Radiation Facility (ESRF), Grenoble, France, for the provision of beamtime and staff assistance at XALOC (ALBA, BAG number 2023087670) and ID30B and ID23-2 (ESRF, BAG number MX2650) beamlines during diffraction data collection. We also acknowledge the Robotein® platform of the BE Instruct-ERIC Centre for providing access to the EasyPick Microlab STARlet Hamilton workstation (https://www.robotein.uliege.be/cms/c_14301428/en/robotein). Funding for open access charge: Universidad de Granada/CBUA.Elsevier BVAgencia Estatal de Investigación (España)European CommissionMinisterio de Ciencia e Innovación (España)Ministerio de Ciencia, Innovación y Universidades (España)Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]2026202620262026info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionhttp://hdl.handle.net/10261/420254reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)#PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE#info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2019-107515RB-C21info:eu-repo/grantAgreement/EC/H2020/681032http://dx.doi.org/10.1016/j.ijbiomac.2025.150022Síinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/4202542026-05-22T06:33:51Z
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