Integrating artificial intelligence-based epitope prediction in a SARS-CoV-2 antibody discovery pipeline: caution is warranted.

Covid-19 Epitope mapping In silico prediction Neutralizing antibody SARS-CoV-2

Journal

EBioMedicine
ISSN: 2352-3964
Titre abrégé: EBioMedicine
Pays: Netherlands
ID NLM: 101647039

Informations de publication

Date de publication:
16 Jan 2024
Historique:
received: 01 05 2023
revised: 22 12 2023
accepted: 22 12 2023
medline: 18 1 2024
pubmed: 18 1 2024
entrez: 17 1 2024
Statut: aheadofprint

Résumé

SARS-CoV-2-neutralizing antibodies (nABs) showed great promise in the early phases of the COVID-19 pandemic. The emergence of resistant strains, however, quickly rendered the majority of clinically approved nABs ineffective. This underscored the imperative to develop nAB cocktails targeting non-overlapping epitopes. Undertaking a nAB discovery program, we employed a classical workflow, while integrating artificial intelligence (AI)-based prediction to select non-competing nABs very early in the pipeline. We identified and in vivo validated (in female Syrian hamsters) two highly potent nABs. Despite the promising results, in depth cryo-EM structural analysis demonstrated that the AI-based prediction employed with the intention to ensure non-overlapping epitopes was inaccurate. The two nABs in fact bound to the same receptor-binding epitope in a remarkably similar manner. Our findings indicate that, even in the Alphafold era, AI-based predictions of paratope-epitope interactions are rough and experimental validation of epitopes remains an essential cornerstone of a successful nAB lead selection. Full list of funders is provided at the end of the manuscript.

Sections du résumé

BACKGROUND BACKGROUND
SARS-CoV-2-neutralizing antibodies (nABs) showed great promise in the early phases of the COVID-19 pandemic. The emergence of resistant strains, however, quickly rendered the majority of clinically approved nABs ineffective. This underscored the imperative to develop nAB cocktails targeting non-overlapping epitopes.
METHODS METHODS
Undertaking a nAB discovery program, we employed a classical workflow, while integrating artificial intelligence (AI)-based prediction to select non-competing nABs very early in the pipeline. We identified and in vivo validated (in female Syrian hamsters) two highly potent nABs.
FINDINGS RESULTS
Despite the promising results, in depth cryo-EM structural analysis demonstrated that the AI-based prediction employed with the intention to ensure non-overlapping epitopes was inaccurate. The two nABs in fact bound to the same receptor-binding epitope in a remarkably similar manner.
INTERPRETATION CONCLUSIONS
Our findings indicate that, even in the Alphafold era, AI-based predictions of paratope-epitope interactions are rough and experimental validation of epitopes remains an essential cornerstone of a successful nAB lead selection.
FUNDING BACKGROUND
Full list of funders is provided at the end of the manuscript.

Identifiants

pubmed: 38232633
pii: S2352-3964(23)00526-1
doi: 10.1016/j.ebiom.2023.104960
pii:
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

104960

Informations de copyright

Copyright © 2023. Published by Elsevier B.V.

Déclaration de conflit d'intérêts

Declaration of interests Ghent University has filed for patent protection on the antibody sequences described herein, and D.D.A., M.W., R.W., W.W., S.G. and L.V. are named as co-inventors on this patent (European Patent Application: 21186206.5). A.P. is employee of the MAbSilico, H.R. holds a patent regarding neutralizing VHH antibodies binding the Spike RBD (PCT/EP2021/052885) and has filed a priority application for neutralizing VHH antibodies binding Spike S2 (EP 23160838.1). X.S. is a recipient of FWO research project COVID-19 (G0G4920N) and FWO-FNRS project VIREOS (EOS ID: 30981113) grants.

Auteurs

Delphine Diana Acar (DD)

HIV Cure Research Center, Department of Internal Medicine and Pediatrics, Ghent University Hospital, Ghent University, Ghent 9000, Belgium.

Wojciech Witkowski (W)

HIV Cure Research Center, Department of Internal Medicine and Pediatrics, Ghent University Hospital, Ghent University, Ghent 9000, Belgium.

Magdalena Wejda (M)

HIV Cure Research Center, Department of Internal Medicine and Pediatrics, Ghent University Hospital, Ghent University, Ghent 9000, Belgium.

Ruifang Wei (R)

HIV Cure Research Center, Department of Internal Medicine and Pediatrics, Ghent University Hospital, Ghent University, Ghent 9000, Belgium.

Tim Desmet (T)

Department of Basic and Applied Medical Sciences, Ghent University, Ghent 9000, Belgium.

Bert Schepens (B)

VIB-UGent Center for Medical Biotechnology, VIB, Ghent 9052, Belgium; Department of Biochemistry and Microbiology, Ghent University, Ghent 9052, Belgium.

Sieglinde De Cae (S)

VIB-UGent Center for Medical Biotechnology, VIB, Ghent 9052, Belgium; Department of Biochemistry and Microbiology, Ghent University, Ghent 9052, Belgium.

Koen Sedeyn (K)

VIB-UGent Center for Medical Biotechnology, VIB, Ghent 9052, Belgium; Department of Biochemistry and Microbiology, Ghent University, Ghent 9052, Belgium.

Hannah Eeckhaut (H)

VIB-UGent Center for Medical Biotechnology, VIB, Ghent 9052, Belgium; Department of Biochemistry and Microbiology, Ghent University, Ghent 9052, Belgium.

Daria Fijalkowska (D)

VIB-UGent Center for Medical Biotechnology, VIB, Ghent 9052, Belgium; Department of Biochemistry and Microbiology, Ghent University, Ghent 9052, Belgium.

Kenny Roose (K)

VIB-UGent Center for Medical Biotechnology, VIB, Ghent 9052, Belgium; Department of Biochemistry and Microbiology, Ghent University, Ghent 9052, Belgium.

Sandrine Vanmarcke (S)

VIB-UGent Center for Medical Biotechnology, VIB, Ghent 9052, Belgium; Department of Biochemistry and Microbiology, Ghent University, Ghent 9052, Belgium.

Anne Poupon (A)

MAbSilico, Tours 37000, France.

Dirk Jochmans (D)

Laboratory of Virology and Chemotherapy, Department of Microbiology, Immunology and Transplantation, Rega Institute for Medical Research, KU Leuven, Leuven 3000, Belgium.

Xin Zhang (X)

Laboratory of Virology and Chemotherapy, Department of Microbiology, Immunology and Transplantation, Rega Institute for Medical Research, KU Leuven, Leuven 3000, Belgium.

Rana Abdelnabi (R)

Laboratory of Virology and Chemotherapy, Department of Microbiology, Immunology and Transplantation, Rega Institute for Medical Research, KU Leuven, Leuven 3000, Belgium.

Caroline S Foo (CS)

Laboratory of Virology and Chemotherapy, Department of Microbiology, Immunology and Transplantation, Rega Institute for Medical Research, KU Leuven, Leuven 3000, Belgium.

Birgit Weynand (B)

Department of Imaging and Pathology, Translational Cell and Tissue Research, KU Leuven, Leuven 3000, Belgium.

Dirk Reiter (D)

Department of Bioengineering Sciences, Vrije Universiteit Brussel, Brussels 1050, Belgium.

Nico Callewaert (N)

VIB-UGent Center for Medical Biotechnology, VIB, Ghent 9052, Belgium; Department of Biochemistry and Microbiology, Ghent University, Ghent 9052, Belgium.

Han Remaut (H)

Department of Bioengineering Sciences, Vrije Universiteit Brussel, Brussels 1050, Belgium; VIB-VUB Center for Structural Biology, VIB, Brussels 1050, Belgium.

Johan Neyts (J)

Laboratory of Virology and Chemotherapy, Department of Microbiology, Immunology and Transplantation, Rega Institute for Medical Research, KU Leuven, Leuven 3000, Belgium.

Xavier Saelens (X)

VIB-UGent Center for Medical Biotechnology, VIB, Ghent 9052, Belgium; Department of Biochemistry and Microbiology, Ghent University, Ghent 9052, Belgium.

Sarah Gerlo (S)

HIV Cure Research Center, Department of Internal Medicine and Pediatrics, Ghent University Hospital, Ghent University, Ghent 9000, Belgium; Department of Biomolecular Medicine, Ghent University, Ghent 9000, Belgium.

Linos Vandekerckhove (L)

HIV Cure Research Center, Department of Internal Medicine and Pediatrics, Ghent University Hospital, Ghent University, Ghent 9000, Belgium. Electronic address: linos.vandekerckhove@ugent.be.

Classifications MeSH