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PIIS0092867421002245.Pdf Kent Academic Repository Full text document (pdf) Citation for published version Andreano, Emanuele and Nicastri, Emanuele and Paciello, Ida and Pileri, Piero and Manganaro, Noemi and Piccini, Giulia and Manenti, Alessandro and Pantano, Elisa and Kabanova, Anna and Troisi, Marco and Vacca, Fabiola and Cardamone, Dario and De Santi, Concetta and Torres, Jonathan L. and Ozorowski, Gabriel and Benincasa, Linda and Jang, Hyesun and Di Genova, Cecilia and DOI https://doi.org/10.1016/j.cell.2021.02.035 Link to record in KAR https://kar.kent.ac.uk/86752/ Document Version Publisher pdf Copyright & reuse Content in the Kent Academic Repository is made available for research purposes. Unless otherwise stated all content is protected by copyright and in the absence of an open licence (eg Creative Commons), permissions for further reuse of content should be sought from the publisher, author or other copyright holder. Versions of research The version in the Kent Academic Repository may differ from the final published version. Users are advised to check http://kar.kent.ac.uk for the status of the paper. Users should always cite the published version of record. Enquiries For any further enquiries regarding the licence status of this document, please contact: [email protected] If you believe this document infringes copyright then please contact the KAR admin team with the take-down information provided at http://kar.kent.ac.uk/contact.html Journal Pre-proof Extremely potent human monoclonal antibodies from COVID-19 convalescent patients Emanuele Andreano, Emanuele Nicastri, Ida Paciello, Piero Pileri, Noemi Manganaro, Giulia Piccini, Alessandro Manenti, Elisa Pantano, Anna Kabanova, Marco Troisi, Fabiola Vacca, Dario Cardamone, Concetta De Santi, Jonathan L. Torres, Gabriel Ozorowski, Linda Benincasa, Hyesun Jang, Cecilia Di Genova, Lorenzo Depau, Jlenia Brunetti, Chiara Agrati, Maria Rosaria Capobianchi, Concetta Castilletti, Arianna Emiliozzi, Massimiliano Fabbiani, Francesca Montagnani, Luisa Bracci, Giuseppe Sautto, Ted M. Ross, Emanuele Montomoli, Nigel Temperton, Andrew B. Ward, Claudia Sala, Giuseppe Ippolito, Rino Rappuoli PII: S0092-8674(21)00224-5 DOI: https://doi.org/10.1016/j.cell.2021.02.035 Reference: CELL 11898 To appear in: Cell Received Date: 24 November 2020 Revised Date: 25 January 2021 Accepted Date: 16 February 2021 Please cite this article as: Andreano, E., Nicastri, E., Paciello, I., Pileri, P., Manganaro, N., Piccini, G., Manenti, A., Pantano, E., Kabanova, A., Troisi, M., Vacca, F., Cardamone, D., De Santi, C., Torres, J.L., Ozorowski, G., Benincasa, L., Jang, H., Di Genova, C., Depau, L., Brunetti, J., Agrati, C., Capobianchi, M.R., Castilletti, C., Emiliozzi, A., Fabbiani, M., Montagnani, F., Bracci, L., Sautto, G., Ross, T.M., Montomoli, E., Temperton, N., Ward, A.B., Sala, C., Ippolito, G., Rappuoli, R., Extremely potent human monoclonal antibodies from COVID-19 convalescent patients, Cell (2021), doi: https://doi.org/10.1016/ j.cell.2021.02.035. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2021 Elsevier Inc. Journal Pre-proof 1 Extremely potent human monoclonal antibodies from CCOVIDOVIDOVID----1919 convalescent patients 2 3 Emanuele Andreano 1† , Emanuele Nicastri 4† , Ida Paciello 1, Piero Pileri 1, Noemi Manganaro 1, Giulia 4 Piccini 2, Alessandro Manenti 2,3 , Elisa Pantano 1, Anna Kabanova 1,11 , Marco Troisi 1,9 , Fabiola 5 Vacca 1,9 , Dario Cardamone 1,10 , Concetta De Santi 1, Jonathan L. Torres 16 , Gabriel Ozorowski 16 , 6 Linda Benincasa 3, Hyesun Jang 13 , Cecilia Di Genova 15 , Lorenzo Depau 12 , Jlenia Brunetti 12 , Chiara 7 Agrati 4, Maria Rosaria Capobianchi 4, Concetta Castilletti 4, Arianna Emiliozzi 5,6 , Massimiliano 8 Fabbiani 6, Francesca Montagnani 5,6 , Luisa Bracci 12 , Giuseppe Sautto 13 , Ted M. Ross 13,14 , 9 Emanuele Montomoli 2,3,7 , Nigel Temperton 15 , Andrew B. Ward 16 , Claudia Sala 1, Giuseppe Ippolito 4, 10 Rino Rappuoli 1,8,17, * 11 12 1Monoclonal Antibody Discovery (MAD) Lab, Fondazione Toscana Life Sciences, Siena, Italy 13 2VisMederi S.r.l, Siena, Italy 14 3VisMederi Research S.r.l., Siena, Italy 15 4National Institute for Infectious Diseases Lazzaro Spallanzani, IRCCS, Rome, Italy 16 5Department of Medical Biotechnologies, University of Siena, Siena, Italy 17 6Department of Medical Sciences, Infectious and Tropical Diseases Unit, University Hospital of 18 Siena, Siena, Italy 19 7Department of Molecular and Developmental Medicine, University of Siena, Siena, Italy 20 8Faculty of Medicine, Imperial College, London, United Kingdom 21 9Department of Biotechnology, Chemistry and Pharmacy, University of Siena, Siena, Italy 22 10 University of Turin, Turin, Italy 23 11 Tumour Immunology Unit, Fondazione Toscana Life Sciences, Siena, Italy 24 12 MedBiotech Hub and Competence Center, Department of Medical Biotechnologies, University of 25 Siena 26 13 Center for Vaccines and Immunology, University of Georgia, Athens, GA 30602, USA. 27 14 Department of InfectiousJournal Diseases, University of Pre-proofGeorgia, Athens, GA 30602, USA. 28 15 Viral Pseudotype Unit, Medway School of Pharmacy, University of Kent, Chatham, UK 29 16 Department of Integrative Structural and Computational Biology, The Scripps Research Institute, 30 La Jolla, CA 92037 31 17 Lead contact 32 33 †These authors contributed equally in sample processing and patient enrolment respectively. 34 *To whom correspondence should be addressed: Dr. Rino Rappuoli [email protected] (R.R.) 1 35 SUMMARY 36 Human monoclonal antibodies are safe, preventive and therapeutic tools, that can be rapidly 37 developed to help restore the massive health and economic disruption caused by the coronavirus 38 disease 2019 (COVID-19) pandemic. By single cell sorting 4,277 SARS-CoV-2 spike protein 39 specific memory B cells from 14 COVID-19 survivors, 453 neutralizing antibodies were identified. 40 The most potent neutralizing antibodies recognized the spike protein receptor binding domain, 41 followed in potency by antibodies that recognize the S1 domain, the spike protein trimer and the S2 42 subunit. Only 1.4% of them neutralized the authentic virus with a potency of 1-10 ng/mL.. The most 43 potent monoclonal antibody, engineered to reduce the risk of antibody dependent enhancement 44 and prolong half-life, neutralized the authentic wild type virus and emerging variants containing 45 D614G, E484K and N501Y substitutions. Prophylactic and therapeutic efficacy in the hamster 46 model was observed at 0.25 and 4 mg/kg respectively in absence of Fc-functions. Journal Pre-proof 2 47 INTRODUCTION 48 The impact of the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) pandemic, with 49 more than 100 million cases, over 2 million deaths, an estimated cost of 16 trillion US dollars to the 50 USA economy (Cutler and Summers, 2020) and 45 million people filing unemployment in the 51 United States alone, is unprecedented (Aratani, 2020). 52 Vaccines and drugs against SARS-CoV-2 have recently received emergency use authorization 53 (EUA) by the Food and Drug Administration (FDA) for prevention and treatment of coronavirus 54 disease 2019 (COVID-19) (FDA, 2021, FDA, 2020). 55 In spite of this, it is predictable that waves of infection will continue to spread globally and it is likely 56 to be followed by additional waves over the next few years. This is supported by the emergence of 57 new SARS-CoV-2 variants in the United Kingdom, South Africa, Brazil and Japan (CDC, 2021). 58 It is therefore imperative to quickly develop, in parallel to vaccines, therapeutic tools against SARS- 59 CoV-2 and its variants. Among the many therapeutic options available, human monoclonal 60 antibodies (mAbs) can be developed in the shortest time frame. In fact, the extensive clinical 61 experience with the safety of more than 50 commercially available mAbs approved to treat cancer, 62 inflammatory and autoimmune disorders, provides high confidence of their safety (Wellcome, 63 2020). These advantages, combined with the urgency of the SARS-CoV-2 pandemic, support and 64 justify an accelerated regulatory pathway. In addition, the long industrial experience in developing 65 and manufacturing mAbs decreases risks usually associated with technical development of 66 investigational products. JournalFinally, the incredible t echnicalPre-proof progress in this field allows shortening of 67 conventional timelines and enables a path from discovery to proof of concept trials within 5-6 68 months (Kelley, 2020). A key example is the Ebola case, where mAbs were developed faster than 69 vaccines or other drugs (Kupferschmidt, 2019) becoming the first therapeutic intervention 70 recommended by the World Health Organization (WHO) and approved by the Food and Drug 71 Administration (FDA) (Mullard, 2020). 72 During the first months of this pandemic many groups have been active in isolating and 73 characterizing human monoclonal antibodies from COVID-19 convalescent patients or from 74 humanized mice and some of them have been progressing
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