Longitudinal Analysis of the Human B Cell Response to Ebola Virus Infection
Ebola virus (EBOV) remains a public health threat. We performed a longitudinal study of B cell responses to EBOV in four survivors of the 2014 West African outbreak. Infection induced lasting EBOV-specific immunoglobulin G (IgG) antibodies, but their subclass composition changed over time, with IgG1...
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| Published in | Cell Vol. 177; no. 6; pp. 1566 - 1582.e17 |
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| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
30.05.2019
Cell Press |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Ebola virus (EBOV) remains a public health threat. We performed a longitudinal study of B cell responses to EBOV in four survivors of the 2014 West African outbreak. Infection induced lasting EBOV-specific immunoglobulin G (IgG) antibodies, but their subclass composition changed over time, with IgG1 persisting, IgG3 rapidly declining, and IgG4 appearing late. Striking changes occurred in the immunoglobulin repertoire, with massive recruitment of naive B cells that subsequently underwent hypermutation. We characterized a large panel of EBOV glycoprotein-specific monoclonal antibodies (mAbs). Only a small subset of mAbs that bound glycoprotein by ELISA recognized cell-surface glycoprotein. However, this subset contained all neutralizing mAbs. Several mAbs protected against EBOV disease in animals, including one mAb that targeted an epitope under evolutionary selection during the 2014 outbreak. Convergent antibody evolution was seen across multiple donors, particularly among VH3-13 neutralizing antibodies specific for the GP1 core. Our study provides a benchmark for assessing EBOV vaccine-induced immunity.
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•Ebola virus infection causes massive recruitment of naive B cells•Virus-specific antibodies continue to class-switch and mutate for months after acute infection•Protective antibodies can be neutralizing or non-neutralizing and can appear early•Convergent, protective antibody rearrangements are seen in multiple donors
A longitudinal study of Ebola virus infection survivors maps out the antibody features that confer protection, with potential implications for vaccination. |
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| AbstractList | Ebola virus (EBOV) remains a public health threat. We performed a longitudinal study of B cell responses to EBOV in four survivors of the 2014 West African outbreak. Infection induced lasting EBOV-specific immunoglobulin G (IgG) antibodies, but their subclass composition changed over time, with IgG1 persisting, IgG3 rapidly declining, and IgG4 appearing late. Striking changes occurred in the immunoglobulin repertoire, with massive recruitment of naive B cells that subsequently underwent hypermutation. We characterized a large panel of EBOV glycoprotein-specific monoclonal antibodies (mAbs). Only a small subset of mAbs that bound glycoprotein by ELISA recognized cell-surface glycoprotein. However, this subset contained all neutralizing mAbs. Several mAbs protected against EBOV disease in animals, including one mAb that targeted an epitope under evolutionary selection during the 2014 outbreak. Convergent antibody evolution was seen across multiple donors, particularly among VH3-13 neutralizing antibodies specific for the GP1 core. Our study provides a benchmark for assessing EBOV vaccine-induced immunity. Ebola virus (EBOV) remains a public health threat. We performed a longitudinal study of B cell responses to EBOV in four survivors of the 2014 West African outbreak. Infection induced lasting EBOV-specific immunoglobulin G (IgG) antibodies, but their subclass composition changed over time, with IgG1 persisting, IgG3 rapidly declining, and IgG4 appearing late. Striking changes occurred in the immunoglobulin repertoire, with massive recruitment of naive B cells that subsequently underwent hypermutation. We characterized a large panel of EBOV glycoprotein-specific monoclonal antibodies (mAbs). Only a small subset of mAbs that bound glycoprotein by ELISA recognized cell-surface glycoprotein. However, this subset contained all neutralizing mAbs. Several mAbs protected against EBOV disease in animals, including one mAb that targeted an epitope under evolutionary selection during the 2014 outbreak. Convergent antibody evolution was seen across multiple donors, particularly among VH3-13 neutralizing antibodies specific for the GP1 core. Our study provides a benchmark for assessing EBOV vaccine-induced immunity. • Ebola virus infection causes massive recruitment of naive B cells • Virus-specific antibodies continue to class-switch and mutate for months after acute infection • Protective antibodies can be neutralizing or non-neutralizing and can appear early • Convergent, protective antibody rearrangements are seen in multiple donors A longitudinal study of Ebola virus infection survivors maps out the antibody features that confer protection, with potential implications for vaccination. Ebola virus (EBOV) remains a public health threat. We performed a longitudinal study of B cell responses to EBOV in four survivors of the 2014 West African outbreak. Infection induced lasting EBOV-specific immunoglobulin G (IgG) antibodies, but their subclass composition changed over time, with IgG1 persisting, IgG3 rapidly declining, and IgG4 appearing late. Striking changes occurred in the immunoglobulin repertoire, with massive recruitment of naive B cells that subsequently underwent hypermutation. We characterized a large panel of EBOV glycoprotein-specific monoclonal antibodies (mAbs). Only a small subset of mAbs that bound glycoprotein by ELISA recognized cell-surface glycoprotein. However, this subset contained all neutralizing mAbs. Several mAbs protected against EBOV disease in animals, including one mAb that targeted an epitope under evolutionary selection during the 2014 outbreak. Convergent antibody evolution was seen across multiple donors, particularly among VH3-13 neutralizing antibodies specific for the GP1 core. Our study provides a benchmark for assessing EBOV vaccine-induced immunity. [Display omitted] •Ebola virus infection causes massive recruitment of naive B cells•Virus-specific antibodies continue to class-switch and mutate for months after acute infection•Protective antibodies can be neutralizing or non-neutralizing and can appear early•Convergent, protective antibody rearrangements are seen in multiple donors A longitudinal study of Ebola virus infection survivors maps out the antibody features that confer protection, with potential implications for vaccination. |
| Author | Piper, Ashley E. Chennareddy, Chakravarthy Cavet, Guy Ahmed, Rafi Ellebedy, Ali H. Spiropoulou, Christina F. Sette, Alessandro Davis, Carl W. Sidney, John Goff, Arthur J. Jackson, Katherine J.L. Kawaoka, Yoshihiro Boyd, Scott D. Huang, Jessica Yu, Tianwei Crozier, Ian Leung, Yvonne Albariño, César G. Mehta, Aneesh K. Nielsen, Sandra C.A. McElroy, Anita K. Saphire, Erica Ollman Halfmann, Peter Glass, Pamela J. |
| AuthorAffiliation | 14 Department of Medicine, University of California San Diego, La Jolla, CA, USA 13 Division of Vaccine Discovery, La Jolla Institute for Allergy and Immunology, La Jolla, CA, USA 10 Department of Immunology and Microbial Science, The Scripps Research Institute, La Jolla, CA, USA 16 La Jolla Institute for Immunology, La Jolla, CA, USA 17 Division of Virology, Department of Microbiology and Immunology, International Research Center for Infectious Diseases, Institute of Medical Science, University of Tokyo, Tokyo, Japan 8 Virology Division, United States Army Medical Research Institute for Infectious Diseases, Fort Detrick, MD, USA 4 Viral Special Pathogens Branch, US Centers for Disease Control and Prevention, Atlanta, GA, USA 15 Department of Biostatistics and Bioinformatics, Emory University, Atlanta, GA, USA 1 Emory Vaccine Center and Department of Microbiology and Immunology, Emory University, Atlanta, GA, USA 7 Department of Pathobiological Sciences, School of Veterinary Medicine, Universit |
| AuthorAffiliation_xml | – name: 11 Integrated Research Facility at Fort Detrick, Clinical Monitoring Research Program Directorate, Frederick National Laboratory for Cancer Research sponsored by the National Cancer Institutes, Frederick, MD, USA – name: 7 Department of Pathobiological Sciences, School of Veterinary Medicine, University of Wisconsin-Madison, WI, USA – name: 15 Department of Biostatistics and Bioinformatics, Emory University, Atlanta, GA, USA – name: 4 Viral Special Pathogens Branch, US Centers for Disease Control and Prevention, Atlanta, GA, USA – name: 17 Division of Virology, Department of Microbiology and Immunology, International Research Center for Infectious Diseases, Institute of Medical Science, University of Tokyo, Tokyo, Japan – name: 12 Division of Immunobiology, Department of Pathology and Immunology Washington University School of Medicine, St. Louis, MO, USA – name: 1 Emory Vaccine Center and Department of Microbiology and Immunology, Emory University, Atlanta, GA, USA – name: 14 Department of Medicine, University of California San Diego, La Jolla, CA, USA – name: 8 Virology Division, United States Army Medical Research Institute for Infectious Diseases, Fort Detrick, MD, USA – name: 2 Department of Pathology, Stanford University, Stanford, CA, USA – name: 16 La Jolla Institute for Immunology, La Jolla, CA, USA – name: 13 Division of Vaccine Discovery, La Jolla Institute for Allergy and Immunology, La Jolla, CA, USA – name: 3 Immunology Division, Garvan Institute of Medical Research, Darlinghurst, NSW, Australia – name: 10 Department of Immunology and Microbial Science, The Scripps Research Institute, La Jolla, CA, USA – name: 9 Atreca, Redwood City, CA, USA – name: 18 Division of Infectious Diseases, School of Medicine, Emory University, Atlanta, GA, USA – name: 6 Division of Pediatric Infectious Disease, University of Pittsburgh, Pittsburgh, PA, USA – name: 5 Division of Pediatric Infectious Disease, Emory University, Atlanta, GA, USA |
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| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/31104840$$D View this record in MEDLINE/PubMed |
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| Copyright | 2019 Elsevier Inc. Copyright © 2019 Elsevier Inc. All rights reserved. 2019 The Authors. Published by Elsevier Inc. 2019 Elsevier Inc. |
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| Keywords | antibody evolution B cell repertoire Ebola IgG subclass public clonotype |
| Language | English |
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| SubjectTerms | Adult Amino Acid Sequence - genetics Animals Antibodies, Monoclonal - immunology Antibodies, Monoclonal - isolation & purification Antibodies, Neutralizing - immunology Antibodies, Viral - immunology antibody evolution B cell repertoire B-Lymphocytes - metabolism B-Lymphocytes - physiology Chlorocebus aethiops Ebola Ebola Vaccines - immunology Ebolavirus - genetics Ebolavirus - metabolism Ebolavirus - pathogenicity Epitopes - blood Female Glycoproteins - genetics Hemorrhagic Fever, Ebola - immunology Hemorrhagic Fever, Ebola - metabolism Hemorrhagic Fever, Ebola - virology Humans IgG subclass Immunoglobulin G - immunology Jurkat Cells Longitudinal Studies Male Mice Mice, Inbred BALB C public clonotype Survivors Vero Cells Viral Envelope Proteins - genetics |
| Title | Longitudinal Analysis of the Human B Cell Response to Ebola Virus Infection |
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