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1. Broad SARS-CoV-2 neutralization by monoclonal and bispecific antibodies derived from a Gamma-infected individual

Author

Denise Guerra, Tim Beaumont, Laura Radić, Gius Kerster, Karlijn van der Straten, Meng Yuan, Jonathan L. Torres, Wen-Hsin Lee, Hejun Liu, Meliawati Poniman, Ilja Bontjer, Judith A. Burger, Mathieu Claireaux, Tom G. Caniels, Jonne L. Snitselaar, Tom P.L. Bijl, Sabine Kruijer, Gabriel Ozorowski, David Gideonse, Kwinten Sliepen, Andrew B. Ward, Dirk Eggink, Godelieve J. de Bree, Ian A. Wilson, Rogier W. Sanders, and Marit J. van Gils

Subjects
Immunology, Virology, Structural biology, Science
Abstract

Summary: The pandemic caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) has remained a medical threat due to the evolution of multiple variants that acquire resistance to vaccines and prior infection. Therefore, it is imperative to discover monoclonal antibodies (mAbs) that neutralize a broad range of SARS-CoV-2 variants. A stabilized spike glycoprotein was used to enrich antigen-specific B cells from an individual with a primary Gamma variant infection. Five mAbs selected from those B cells showed considerable neutralizing potency against multiple variants, with COVA309-35 being the most potent against the autologous virus, as well as Omicron BA.1 and BA.2, and COVA309-22 having binding and neutralization activity against Omicron BA.4/5, BQ.1.1, and XBB.1. When combining the COVA309 mAbs as cocktails or bispecific antibodies, the breadth and potency were improved. In addition, the mechanism of cross-neutralization of the COVA309 mAbs was elucidated by structural analysis. Altogether these data indicate that a Gamma-infected individual can develop broadly neutralizing antibodies.

Published
2023
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2. Lassa virus glycoprotein nanoparticles elicit neutralizing antibody responses and protection

Author

Philip J.M. Brouwer, Aleksandar Antanasijevic, Adam J. Ronk, Helena Müller-Kräuter, Yasunori Watanabe, Mathieu Claireaux, Hailee R. Perrett, Tom P.L. Bijl, Marloes Grobben, Jeffrey C. Umotoy, Angela I. Schriek, Judith A. Burger, Khadija Tejjani, Nicole M. Lloyd, Thijs H. Steijaert, Marlies M. van Haaren, Kwinten Sliepen, Steven W. de Taeye, Marit J. van Gils, Max Crispin, Thomas Strecker, Alexander Bukreyev, Andrew B. Ward, Rogier W. Sanders, Medical Microbiology and Infection Prevention, AII - Infectious diseases, Graduate School, and Experimental Immunology

Subjects
Virology, antibody, vaccine, cryo-EM, Parasitology, nanoparticles, Lassa virus, Microbiology, challenge study
Abstract

The Lassa virus is endemic in parts of West Africa, and it causes hemorrhagic fever with high mortality. The development of a recombinant protein vaccine has been hampered by the instability of soluble Lassa virus glycoprotein complex (GPC) trimers, which disassemble into monomeric subunits after expression. Here, we use two-component protein nanoparticles consisting of trimeric and pentameric subunits to stabilize GPC in a trimeric conformation. These GPC nanoparticles present twenty prefusion GPC trimers on the surface of an icosahedral particle. Cryo-EM studies of GPC nanoparticles demonstrated a well-ordered structure and yielded a high-resolution structure of an unliganded GPC. These nanoparticles induced potent humoral immune responses in rabbits and protective immunity against the lethal Lassa virus challenge in guinea pigs. Additionally, we isolated a neutralizing antibody that mapped to the putative receptor-binding site, revealing a previously undefined site of vulnerability. Collectively, these findings offer potential approaches to vaccine and therapeutic design for the Lassa virus.

Published
2022

3. Influenza a virus hemagglutinin trimer, head and stem proteins identify and quantify different hemagglutinin-specific b cell subsets in humans

Author

Marit J. van Gils, Mathieu Claireaux, Willy M. J. M. Bogers, Rogier W. Sanders, Sarah van Leeuwen, Petra Mooij, Aafke Aartse, Gerrit Koopman, Dirk Eggink, Medical Microbiology and Infection Prevention, and AII - Infectious diseases

Subjects
0301 basic medicine, medicine.drug_class, Immunology, Hemagglutinin (influenza), Stem, medicine.disease_cause, Monoclonal antibody, Article, Neutralization, Epitope, Virus, 03 medical and health sciences, 0302 clinical medicine, Drug Discovery, Influenza A virus, medicine, Pharmacology (medical), Hemagglutinin, B cell, Pharmacology, biology, Virology, 030104 developmental biology, Infectious Diseases, medicine.anatomical_structure, Trimer specific, biology.protein, Medicine, Antibody responses, Antibody, Head, 030217 neurology & neurosurgery
Abstract

Antibody responses against the influenza A virus hemagglutinin (HA)-protein are studied intensively because they can protect against (re)infection. Previous studies have focused on antibodies targeting the head or stem domains, while other possible specificities are often not taken into account. To study such specificities, we developed a diverse set of HA-domain proteins based on an H1N1pdm2009-like influenza virus strain, including monomeric head and trimeric stem domain, as well as the full HA-trimer. These proteins were used to study the B cell and antibody responses in six healthy human donors. A large proportion of HA-trimer B cells bound exclusively to HA-trimer probe (54–77%), while only 8–18% and 9–23% were able to recognize the stem or head probe, respectively. Monoclonal antibodies (mAbs) were isolated and three of these mAbs, targeting the different domains, were characterized in-depth to confirm the binding profile observed in flow cytometry. The head-directed mAb, targeting an epitope distinct from known head-specific mAbs, showed relatively broad H1N1 neutralization and the stem-directed mAb was able to broadly neutralize diverse H1N1 viruses. Moreover, we identified a trimer-directed mAb that did not compete with known head or stem domain specific mAbs, suggesting that it targets an unknown epitope or conformation of influenza virus’ HA. These observations indicate that the described method can characterize the diverse antibody response to HA and might be able to identify HA-specific B cells and antibodies with previously unknown specificities that could be relevant for vaccine design.

Published
2021

4. Two-component spike nanoparticle vaccine protects macaques from SARS-CoV-2 infection

Author

Anna Z Mykytyn, Max Crispin, Mathieu Claireaux, Karlijn van der Straten, Tom G. Caniels, Rashmi Ravichandran, Raphael Ho Tsong Fang, Kwinten Sliepen, Nisreen M.A. Okba, Mitch Brinkkemper, Nidhal Kahlaoui, Marlon de Gast, Rogier W. Sanders, Ilja Bontjer, Hannah L. Turner, Romain Marlin, Jelle van Schooten, Sylvie van der Werf, Meliawati Poniman, Godelieve J. de Bree, Yoann Aldon, Julien Lemaitre, Thibaut Naninck, Yasunori Watanabe, Roger Le Grand, Eric Ginoux, Ségolène Diry, Pauline Maisonnasse, Julien Villaudy, Edith E. Schermer, Julia M. Giezen, Vanessa Contreras, Bart L. Haagmans, Catherine Chapon, Gius Kerster, Philip J. M. Brouwer, Cynthia A. van der Linden, Yme U. van der Velden, Judith A. Burger, Andrew B. Ward, Virginie Chesnais, Mariëlle J. van Breemen, Marit J. van Gils, Marloes Grobben, Nathalie Dereuddre-Bosquet, Neil P. King, Joel D. Allen, Department of Medical Microbiology and Infection Prevention [Amsterdam], University of Amsterdam [Amsterdam] (UvA), Immunologie des maladies virales, auto-immunes, hématologiques et bactériennes (IMVA-HB), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Paris-Saclay, Life and Soft, University of Southampton, University of Oxford, The Scripps Research Institute [La Jolla, San Diego], Imperial College London, Amsterdam UMC - Amsterdam University Medical Center, Erasmus University Medical Center [Rotterdam] (Erasmus MC), University of Washington [Seattle], AIMM Therapeutics [Amsterdam, the Netherlands], Génétique Moléculaire des Virus à ARN - Molecular Genetics of RNA Viruses (GMV-ARN (UMR_3569 / U-Pasteur_2)), Institut Pasteur [Paris] (IP)-Centre National de la Recherche Scientifique (CNRS)-Université Paris Cité (UPCité), Centre National de Référence des virus des infections respiratoires (dont la grippe) - National Reference Center Virus Influenzae [Paris] (CNR - laboratoire coordonnateur), Institut Pasteur [Paris] (IP)-Université Paris Cité (UPCité), This work was supported by a Netherlands Organisation for Scientific Research (NWO) Vici grant (to R.W.S.), the Bill & Melinda Gates Foundation through the Collaboration for AIDS Vaccine Discovery (CAVD) grants OPP1111923, OPP1132237, and INV-002022 (to R.W.S. and/or N.P.K.), INV-008352/OPP1153692 and OPP1196345/INV-008813 (to M.C.), and OPP1170236 (to A.B.W.), the Fondation Dormeur, Vaduz (R.W.S. and to M.J.v.G.) and Health-Holland PPS-allowance LSHM20040 (to M.J.v.G.), the University of Southampton Coronavirus Response Fund (M.C.), and the Netherlands Organisation for Health Research and Development ZONMW (B.L.H). M.J.v.G. is a recipient of an AMC Fellowship from Amsterdam UMC and a COVID-19 grant from the Amsterdam Institute for Infection and Immunity. R.W.S. and M.J.v.G. are recipients of support from the University of Amsterdam Proof of Concept fund (contract 200421) as managed by Innovation Exchange Amsterdam (IXA). The Infectious Disease Models and Innovative Therapies (IDMIT) research infrastructure is supported by the Programme Investissements d’Avenir, managed by the National Research Agency (ANR) under reference ANR-11-INBS-0008. The Fondation Bettencourt Schueller and the Region Ile-de-France contributed to the implementation of IDMIT’s facilities and imaging technologies. The non-human primate study received financial support from REACTing, the ANR (AM-CoV-Path), and the European Infrastructure TRANSVAC2 (730964)., ANR-11-INBS-0008,IDMIT,Infrastructure nationale pour la modélisation des maladies infectieuses humaines(2011), ANR-20-COVI-0021,AM-Cov-Path,Pathogénèse de l'infection SARS-Cov-2 dans un modèle de primates non humains : un modèle pour les traitements et la prévention(2020), European Project: 730964, H2020, RIA,H2020-INFRAIA-2016-1,TRANSVAC2(2017), Graduate School, AII - Infectious diseases, Medical Microbiology and Infection Prevention, Experimental Immunology, Infectious diseases, APH - Aging & Later Life, APH - Global Health, and Virology

Subjects
T-Lymphocytes, viruses, [SDV]Life Sciences [q-bio], Disease, Public administration, Mice, 0302 clinical medicine, vaccine, Pandemic, antibodies, Spike (database), Neutralizing antibody, 0303 health sciences, B-Lymphocytes, Mice, Inbred BALB C, biology, Transmission (medicine), Viral Load, protection, Models, Animal, Spike Glycoprotein, Coronavirus, Christian ministry, Rabbits, Antibody, Viral load, Healthcare system, COVID-19 Vaccines, Coronavirus disease 2019 (COVID-19), macaques, Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), Article, General Biochemistry, Genetics and Molecular Biology, 03 medical and health sciences, SDG 3 - Good Health and Well-being, Acquired immunodeficiency syndrome (AIDS), Immunity, Political science, medicine, Animals, 030304 developmental biology, B cells, SARS-CoV-2, Conflict of interest, Spike Protein, COVID-19, medicine.disease, Antibodies, Neutralizing, Virology, immunity, Macaca fascicularis, Immunization, Infectious disease (medical specialty), biology.protein, nanoparticles, 030217 neurology & neurosurgery
Abstract

The severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) pandemic is continuing to disrupt personal lives, global healthcare systems, and economies. Hence, there is an urgent need for a vaccine that prevents viral infection, transmission, and disease. Here, we present a two-component protein-based nanoparticle vaccine that displays multiple copies of the SARS-CoV-2 spike protein. Immunization studies show that this vaccine induces potent neutralizing antibody responses in mice, rabbits, and cynomolgus macaques. The vaccine-induced immunity protects macaques against a high-dose challenge, resulting in strongly reduced viral infection and replication in the upper and lower airways. These nanoparticles are a promising vaccine candidate to curtail the SARS-CoV-2 pandemic., Graphical Abstract, Brouwer et al. present preclinical evidence in support of a COVID-19 vaccine candidate, designed as a self-assembling two-component protein nanoparticle displaying multiple copies of the SARS-CoV-2 spike protein, which induces strong neutralizing antibody responses and protects from high-dose SARS-CoV-2 challenge.

Published
2021

5. Potent neutralizing antibodies from COVID-19 patients define multiple targets of vulnerability

Author

Gestur Vidarsson, Mathieu Claireaux, Ilja Bontjer, Marlies M. van Haaren, Alex van der Kooi, Philip J. M. Brouwer, Jelle van Schooten, Niels van der Velde, Ronald Derking, Karlijn van der Straten, Denise Guerra, Gius Kerster, Andrew B. Ward, Jonathan L. Torres, W. Joost Wiersinga, Neeltje A. Kootstra, Sandhya Bangaru, Tom P. L. Bijl, Aafke Aartse, Edith E. Schermer, Judith A. Burger, Kirsten D. Verheul, Bart L. Haagmans, Mariëlle J. van Breemen, Tom G. Caniels, Marit J. van Gils, Yoann Aldon, Nisreen M.A. Okba, Godelieve J. de Bree, Kwinten Sliepen, Jonne L. Snitselaar, Rogier W. Sanders, Arthur E. H. Bentlage, Virology, AII - Infectious diseases, Graduate School, Medical Microbiology and Infection Prevention, APH - Aging & Later Life, Experimental Immunology, Infectious diseases, Center of Experimental and Molecular Medicine, AII - Inflammatory diseases, AII - Cancer immunology, Landsteiner Laboratory, and APH - Global Health

Subjects
Male, 0301 basic medicine, Vulnerability, Antibody Affinity, Antibodies, Viral, medicine.disease_cause, Epitope, Epitopes, 0302 clinical medicine, Immunophenotyping, skin and connective tissue diseases, Antigens, Viral, Research Articles, Coronavirus, Multidisciplinary, biology, Antibodies, Monoclonal, Microbio, Middle Aged, 030220 oncology & carcinogenesis, Spike Glycoprotein, Coronavirus, Receptors, Virus, Female, Antibody, Coronavirus Infections, Research Article, Adult, Coronavirus disease 2019 (COVID-19), medicine.drug_class, Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), Immunology, Pneumonia, Viral, Protein domain, B-Lymphocyte Subsets, Somatic hypermutation, Monoclonal antibody, Betacoronavirus, 03 medical and health sciences, Protein Domains, Antigen, Cell Line, Tumor, medicine, Humans, Protein Interaction Domains and Motifs, Pandemics, Aged, SARS-CoV-2, R-Articles, Spike Protein, COVID-19, Antibodies, Neutralizing, Virology, 030104 developmental biology, biology.protein, Immunologic Memory, Broadly Neutralizing Antibodies, Receptors, Coronavirus
Abstract

Sites of vulnerability in SARS-CoV-2 Antibodies that neutralize severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) could be an important tool in treating coronavirus disease 2019 (COVID-19). Brouwer et al. isolated 403 monoclonal antibodies from three convalescent COVID-19 patients. They show that the patients had strong immune responses against the viral spike protein, a complex that binds to receptors on the host cell. A subset of antibodies was able to neutralize the virus. Competition and electron microscopy studies showed that these antibodies target diverse epitopes on the spike, with the two most potent targeting the domain that binds the host receptor. Science , this issue p. 643

Published
2020
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6. Public T cell receptors confer high-avidity CD4 responses to HIV controllers

Author

Pierre de Truchis, Mathieu Claireaux, Alexandre Nouël, Lisa A. Chakrabarti, Moran Galperin, Samia Hendou, Daniela Benati, Pierre Lechat, Brigitte Lemercier, Annick Lim, Fernando Arenzana-Seisdedos, Olivier Lambotte, Jean-François Delfraissy, Kristy-Anne Campbell, Jamie Rossjohn, Stephanie Gras, Faroudy Boufassa, Madhura Mukhopadhyay, Pathogénie Virale - Viral Pathogenesis, Institut Pasteur [Paris] (IP)-Institut National de la Santé et de la Recherche Médicale (INSERM), Immunologie des Maladies Virales et Autoimmunes (IMVA - U1184), Université Paris-Sud - Paris 11 (UP11)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Institut National de la Santé et de la Recherche Médicale (INSERM), Infection and Immunity Program and Department of Biochemistry and Molecular Biology, Biomedicine Discovery Institute, Australian Research Council Centre of Excellence for Advanced Molecular Imaging, Monash University [Clayton], Département d'Immunologie - Department of Immunology, Institut Pasteur [Paris] (IP), Centre de recherche en épidémiologie et santé des populations (CESP), Université de Versailles Saint-Quentin-en-Yvelines (UVSQ)-Université Paris-Sud - Paris 11 (UP11)-Assistance publique - Hôpitaux de Paris (AP-HP) (AP-HP)-Hôpital Paul Brousse-Institut National de la Santé et de la Recherche Médicale (INSERM), Hub Bioinformatique et Biostatistique - Bioinformatics and Biostatistics HUB, Institut Pasteur [Paris] (IP)-Centre National de la Recherche Scientifique (CNRS), Institute of Infection and Immunity, Cardiff University, This work was supported by ANRS, Sidaction, the Pasteur Institute, the Australian Research Council (ARC), and the National Health and Medical Research Council of Australia (NHMRC). L.A. Chakrabarti is supported by grants grants from ANRS (EP36-8) and Agence Nationale de la Recherche (ANR PD1VAX), S. Gras is supported by an ARC Future Fellowship (FF120100416), and J. Rossjohn by an NHMRC Australia Fellowship (AF50). D. Benati was the recipient of postdoctoral fellowships from ANRS, the Fondation pour la Recher- che Médicale, and the Institut Servier. M. Galperin is the recipient of an ANRS doctoral fellowship. M. Mukhopadhyay is a scholar in the Pasteur - Paris University (PPU) International PhD program., ANR-14-CE16-0029,PD1VAX,Une nouvelle stratégie de vaccination par vecteur ADN PD1 pour mimer les réponses spécifiques de Gag trouvées chez les contrôleurs spontanés du VIH(2014), Pathogénie Virale, Institut Pasteur [Paris]-Institut National de la Santé et de la Recherche Médicale (INSERM), Institut Pasteur [Paris], Assistance publique - Hôpitaux de Paris (AP-HP) (AP-HP)-Université Paris-Sud - Paris 11 (UP11)-Hôpital Paul Brousse-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université de Versailles Saint-Quentin-en-Yvelines (UVSQ), Institut Pasteur [Paris]-Centre National de la Recherche Scientifique (CNRS), Pham, Cécile, and Appel à projets générique - Une nouvelle stratégie de vaccination par vecteur ADN PD1 pour mimer les réponses spécifiques de Gag trouvées chez les contrôleurs spontanés du VIH - - PD1VAX2014 - ANR-14-CE16-0029 - Appel à projets générique - VALID

Subjects
0301 basic medicine, Adult, CD4-Positive T-Lymphocytes, Adoptive cell transfer, CD4 antigen, Receptors, Antigen, T-Cell, chemical and pharmacologic phenomena, HIV Infections, Biology, gag Gene Products, Human Immunodeficiency Virus, Epitope, HIV Long-Term Survivors, 03 medical and health sciences, chemistry.chemical_compound, Mice, 0302 clinical medicine, Immune system, L Cells, Antigen, Antiretroviral Therapy, Highly Active, Animals, Humans, HLA-DR Antigen, [SDV.MP.VIR] Life Sciences [q-bio]/Microbiology and Parasitology/Virology, Immunity, Cellular, T-cell receptor, HIV, Adoptive Transfer, CD4 Antigens, Genes, T-Cell Receptor alpha, Genes, T-Cell Receptor beta, HLA-DR Antigens, L Cells (Cell Line), Middle Aged, HIV-1, Medicine (all), hemic and immune systems, General Medicine, Virology, 3. Good health, 030104 developmental biology, chemistry, Immunology, [SDV.MP.VIR]Life Sciences [q-bio]/Microbiology and Parasitology/Virology, CD8, 030215 immunology, Research Article
Abstract

International audience; The rare patients who are able to spontaneously control HIV replication in the absence of therapy show signs of a particularly efficient cellular immune response. To identify the molecular determinants that underlie this response, we characterized the T cell receptor (TCR) repertoire directed at Gag293, the most immunoprevalent CD4 epitope in the HIV-1 capsid. HIV controllers from the ANRS CODEX cohort showed a highly skewed TCR repertoire that was characterized by a predominance of TRAV24 and TRBV2 variable genes, shared CDR3 motifs, and a high frequency of public clonotypes. The most prevalent public clonotypes generated TCRs with affinities at the higher end of values reported for naturally occurring TCRs. The high-affinity Gag293-specific TCRs were cross-restricted by up to 5 distinct HLA-DR alleles, accounting for the expression of these TCRs in HIV controllers of diverse genetic backgrounds. Transfer of these TCRs to healthy donor CD4+ T cells conferred high antigen sensitivity and polyfunctionality, thus recapitulating key features of the controller CD4 response. Transfer of a high-affinity Gag293-specific TCR also redirected CD8+ T cells to target HIV-1 capsid via nonconventional MHC II restriction. Together, these findings indicate that TCR clonotypes with superior functions are associated with HIV control. Amplification or transfer of such clonotypes may contribute to immunotherapeutic approaches aiming at a functional HIV cure.

Published
2016

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