In silico improvement of affinity for highly protective anti-malarial antibodies

Summary: The monoclonal antibody CIS43 preferentially binds the junctional region of Plasmodium falciparum circumsporozoite protein (PfCSP) and is highly protective in humans. Here, we develop an in silico pipeline to improve antigen-antibody interaction energies and apply it to CIS43 variants elici...

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Main Authors: Mateo Reveiz, Prabhanshu Tripathi, Lais Da Silva Pereira, Patience Kerubo Kiyuka, Tracy Liu, Yongping Yang, Baoshan Zhang, Dorra Benmohamed, Brian G. Bonilla, Carl W. Carruthers, Jr., Marlon Dillon, Daniel Gowetski, Sven Kratochvil, Gabriella Lagos, Mariah Lofgren, Ivan Loukinov, Shamika Mathis-Torres, Andrew J. Schaub, Elizabeth Scheideman, Arne Schön, Chen-Hsiang Shen, Yevel Flores-Garcia, Fidel Zavala, Facundo D. Batista, Azza H. Idris, Robert A. Seder, Peter D. Kwong, Reda Rawi
Format: Article
Language:English
Published: Elsevier 2025-07-01
Series:iScience
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Online Access:http://www.sciencedirect.com/science/article/pii/S2589004225011642
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author Mateo Reveiz
Prabhanshu Tripathi
Lais Da Silva Pereira
Patience Kerubo Kiyuka
Tracy Liu
Yongping Yang
Baoshan Zhang
Dorra Benmohamed
Brian G. Bonilla
Carl W. Carruthers, Jr.
Marlon Dillon
Daniel Gowetski
Sven Kratochvil
Gabriella Lagos
Mariah Lofgren
Ivan Loukinov
Shamika Mathis-Torres
Andrew J. Schaub
Elizabeth Scheideman
Arne Schön
Chen-Hsiang Shen
Yevel Flores-Garcia
Fidel Zavala
Facundo D. Batista
Azza H. Idris
Robert A. Seder
Peter D. Kwong
Reda Rawi
author_facet Mateo Reveiz
Prabhanshu Tripathi
Lais Da Silva Pereira
Patience Kerubo Kiyuka
Tracy Liu
Yongping Yang
Baoshan Zhang
Dorra Benmohamed
Brian G. Bonilla
Carl W. Carruthers, Jr.
Marlon Dillon
Daniel Gowetski
Sven Kratochvil
Gabriella Lagos
Mariah Lofgren
Ivan Loukinov
Shamika Mathis-Torres
Andrew J. Schaub
Elizabeth Scheideman
Arne Schön
Chen-Hsiang Shen
Yevel Flores-Garcia
Fidel Zavala
Facundo D. Batista
Azza H. Idris
Robert A. Seder
Peter D. Kwong
Reda Rawi
author_sort Mateo Reveiz
collection DOAJ
description Summary: The monoclonal antibody CIS43 preferentially binds the junctional region of Plasmodium falciparum circumsporozoite protein (PfCSP) and is highly protective in humans. Here, we develop an in silico pipeline to improve antigen-antibody interaction energies and apply it to CIS43 variants elicited in CIS43-germline knock-in mice. Improved binding of CIS43 variants to the CIS43 junctional epitope (PfCSP peptide 21) was achieved by introducing single and double amino acid substitutions in the peptide 21-proximal heavy- and light-chain-variable regions. The best in silico designed variant, antibody P3-43-LS, was 2- to 3-fold more protective than antibody CIS43-LS, the clinical version of CIS43 with half-life extending leucine-serine (LS) mutations, and had comparable protection to the current best-in-class antibody (iGL-CIS43.D3-LS) to this region. Crystal structures of the improved antibodies revealed atomic-level interactions accounting for gains in binding affinity. This in silico approach to improve antibody affinity can thus be used to enhance potency of PfCSP monoclonal antibodies.
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spelling doaj-art-7b8ee6ed1dcb41929c3ccbc650ea5a792025-08-20T02:37:38ZengElsevieriScience2589-00422025-07-0128711290310.1016/j.isci.2025.112903In silico improvement of affinity for highly protective anti-malarial antibodiesMateo Reveiz0Prabhanshu Tripathi1Lais Da Silva Pereira2Patience Kerubo Kiyuka3Tracy Liu4Yongping Yang5Baoshan Zhang6Dorra Benmohamed7Brian G. Bonilla8Carl W. Carruthers, Jr.9Marlon Dillon10Daniel Gowetski11Sven Kratochvil12Gabriella Lagos13Mariah Lofgren14Ivan Loukinov15Shamika Mathis-Torres16Andrew J. Schaub17Elizabeth Scheideman18Arne Schön19Chen-Hsiang Shen20Yevel Flores-Garcia21Fidel Zavala22Facundo D. Batista23Azza H. Idris24Robert A. Seder25Peter D. Kwong26Reda Rawi27Vaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, USAVaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, USAVaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, USAVaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, USA; Kenya Medical Research Institute, Centre for Geographic Medicine Research Coast, P.O. Box 230-80108, Kilifi, KenyaVaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, USAVaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, USAVaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, USAVaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, USAVaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, USAVaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, USAVaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, USAVaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, USAThe Ragon Institute of Massachusetts General Hospital, Massachusetts Institute of Technology and Harvard University, Cambridge, MA, USAVaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, USAVaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, USAVaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, USAMalaria Research Institute, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD 21205, USAVaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, USAVaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, USADepartment of Biology, Johns Hopkins University, Baltimore, MD, USAVaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, USAMalaria Research Institute, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD 21205, USAMalaria Research Institute, Johns Hopkins Bloomberg School of Public Health, Baltimore, MD 21205, USAThe Ragon Institute of Massachusetts General Hospital, Massachusetts Institute of Technology and Harvard University, Cambridge, MA, USA; Department of Immunology, Harvard Medical School, Boston, MA, USA; Department of Microbiology, Harvard Medical School, Boston, MA, USA; Department of Biology, Massachusetts Institute of Technology, Cambridge, MA, USAVaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, USA; The Ragon Institute of Massachusetts General Hospital, Massachusetts Institute of Technology and Harvard University, Cambridge, MA, USAVaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, USA; Corresponding authorVaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, USA; Aaron Diamond AIDS Research Center, Columbia University Vagelos College of Physicians and Surgeons, New York, NY 10032, USA; Department of Biochemistry and Molecular Biophysics, Columbia University, New York, NY 10032, USA; Corresponding authorVaccine Research Center, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, USA; Corresponding authorSummary: The monoclonal antibody CIS43 preferentially binds the junctional region of Plasmodium falciparum circumsporozoite protein (PfCSP) and is highly protective in humans. Here, we develop an in silico pipeline to improve antigen-antibody interaction energies and apply it to CIS43 variants elicited in CIS43-germline knock-in mice. Improved binding of CIS43 variants to the CIS43 junctional epitope (PfCSP peptide 21) was achieved by introducing single and double amino acid substitutions in the peptide 21-proximal heavy- and light-chain-variable regions. The best in silico designed variant, antibody P3-43-LS, was 2- to 3-fold more protective than antibody CIS43-LS, the clinical version of CIS43 with half-life extending leucine-serine (LS) mutations, and had comparable protection to the current best-in-class antibody (iGL-CIS43.D3-LS) to this region. Crystal structures of the improved antibodies revealed atomic-level interactions accounting for gains in binding affinity. This in silico approach to improve antibody affinity can thus be used to enhance potency of PfCSP monoclonal antibodies.http://www.sciencedirect.com/science/article/pii/S2589004225011642Biological sciencesImmunologyNatural sciencesStructural biology
spellingShingle Mateo Reveiz
Prabhanshu Tripathi
Lais Da Silva Pereira
Patience Kerubo Kiyuka
Tracy Liu
Yongping Yang
Baoshan Zhang
Dorra Benmohamed
Brian G. Bonilla
Carl W. Carruthers, Jr.
Marlon Dillon
Daniel Gowetski
Sven Kratochvil
Gabriella Lagos
Mariah Lofgren
Ivan Loukinov
Shamika Mathis-Torres
Andrew J. Schaub
Elizabeth Scheideman
Arne Schön
Chen-Hsiang Shen
Yevel Flores-Garcia
Fidel Zavala
Facundo D. Batista
Azza H. Idris
Robert A. Seder
Peter D. Kwong
Reda Rawi
In silico improvement of affinity for highly protective anti-malarial antibodies
iScience
Biological sciences
Immunology
Natural sciences
Structural biology
title In silico improvement of affinity for highly protective anti-malarial antibodies
title_full In silico improvement of affinity for highly protective anti-malarial antibodies
title_fullStr In silico improvement of affinity for highly protective anti-malarial antibodies
title_full_unstemmed In silico improvement of affinity for highly protective anti-malarial antibodies
title_short In silico improvement of affinity for highly protective anti-malarial antibodies
title_sort in silico improvement of affinity for highly protective anti malarial antibodies
topic Biological sciences
Immunology
Natural sciences
Structural biology
url http://www.sciencedirect.com/science/article/pii/S2589004225011642
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