A single, improbable B cell receptor mutation confers potent neutralization against cytomegalovirus

Cytomegalovirus (CMV) is a leading cause of infant hearing loss and neurodevelopmental delay, but there are no clinically licensed vaccines to prevent infection, in part due to challenges eliciting neutralizing antibodies. One of the most well-studied targets for CMV vaccines is the viral fusogen gl...

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Published inPLoS pathogens Vol. 19; no. 1; p. e1011107
Main Authors Jenks, Jennifer A., Amin, Sharmi, Sponholtz, Madeline R., Kumar, Amit, Wrapp, Daniel, Venkatayogi, Sravani, Tu, Joshua J., Karthigeyan, Krithika, Valencia, Sarah M., Connors, Megan, Harnois, Melissa J., Hora, Bhavna, Rochat, Eric, McLellan, Jason S., Wiehe, Kevin, Permar, Sallie R.
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 20.01.2023
Public Library of Science (PLoS)
Subjects
Amino acids
Antibodies
Antibodies, Neutralizing - genetics
Antibodies, Neutralizing - immunology
Antibodies, Viral - genetics
Antibodies, Viral - immunology
Antigens
BASIC BIOLOGICAL SCIENCES
Biology and Life Sciences
Care and treatment
Cell receptors
Cloning
Congenital diseases
Cytomegalovirus
Cytomegalovirus - genetics
Cytomegalovirus - immunology
Cytomegalovirus infections
Cytomegalovirus Infections - genetics
Cytomegalovirus Infections - immunology
Cytomegalovirus Vaccines - therapeutic use
Development and progression
Epitopes
Gene mutations
Genealogy
Genetic aspects
Glycoprotein B
Glycoproteins
Health aspects
Hearing loss
Host-virus relationships
Humans
Immune response
Infections
Lymphocytes B
Medicine and Health Sciences
Microbiology
Mutation
Neutralization
Neutralizing
Parasitology
Phylogenetics
Receptors, Antigen, B-Cell - genetics
Receptors, Antigen, B-Cell - immunology
Somatic hypermutation
Vaccines
Viral Envelope Proteins - genetics
Viral Envelope Proteins - immunology
Virology
United States
Online AccessGet full text
ISSN1553-7374
1553-7366
1553-7374
DOI10.1371/journal.ppat.1011107

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Abstract Cytomegalovirus (CMV) is a leading cause of infant hearing loss and neurodevelopmental delay, but there are no clinically licensed vaccines to prevent infection, in part due to challenges eliciting neutralizing antibodies. One of the most well-studied targets for CMV vaccines is the viral fusogen glycoprotein B (gB), which is required for viral entry into host cells. Within gB, antigenic domain 2 site 1 (AD-2S1) is a target of potently neutralizing antibodies, but gB-based candidate vaccines have yet to elicit robust responses against this region. We mapped the genealogy of B cells encoding potently neutralizing anti-gB AD-2S1 antibodies from their inferred unmutated common ancestor (UCA) and characterized the binding and function of early lineage ancestors. Surprisingly, we found that a single amino acid heavy chain mutation A33N, which was an improbable mutation rarely generated by somatic hypermutation machinery, conferred broad CMV neutralization to the non-neutralizing UCA antibody. Structural studies revealed that this mutation mediated key contacts with the gB AD-2S1 epitope. Collectively, these results provide insight into potently neutralizing gB-directed antibody evolution in a single donor and lay a foundation for using this B cell-lineage directed approach for the design of next-generation CMV vaccines.
AbstractList Cytomegalovirus (CMV) is a leading cause of infant hearing loss and neurodevelopmental delay, but there are no clinically licensed vaccines to prevent infection, in part due to challenges eliciting neutralizing antibodies. One of the most well-studied targets for CMV vaccines is the viral fusogen glycoprotein B (gB), which is required for viral entry into host cells. Within gB, antigenic domain 2 site 1 (AD-2S1) is a target of potently neutralizing antibodies, but gB-based candidate vaccines have yet to elicit robust responses against this region. We mapped the genealogy of B cells encoding potently neutralizing anti-gB AD-2S1 antibodies from their inferred unmutated common ancestor (UCA) and characterized the binding and function of early lineage ancestors. Surprisingly, we found that a single amino acid heavy chain mutation A33N, which was an improbable mutation rarely generated by somatic hypermutation machinery, conferred broad CMV neutralization to the non-neutralizing UCA antibody. Structural studies revealed that this mutation mediated key contacts with the gB AD-2S1 epitope. Collectively, these results provide insight into potently neutralizing gB-directed antibody evolution in a single donor and lay a foundation for using this B cell-lineage directed approach for the design of next-generation CMV vaccines.
Cytomegalovirus (CMV) is a leading cause of infant hearing loss and neurodevelopmental delay, but there are no clinically licensed vaccines to prevent infection, in part due to challenges eliciting neutralizing antibodies. One of the most well-studied targets for CMV vaccines is the viral fusogen glycoprotein B (gB), which is required for viral entry into host cells. Within gB, antigenic domain 2 site 1 (AD-2S1) is a target of potently neutralizing antibodies, but gB-based candidate vaccines have yet to elicit robust responses against this region. We mapped the genealogy of B cells encoding potently neutralizing anti-gB AD-2S1 antibodies from their inferred unmutated common ancestor (UCA) and characterized the binding and function of early lineage ancestors. Surprisingly, we found that a single amino acid heavy chain mutation A33N, which was an improbable mutation rarely generated by somatic hypermutation machinery, conferred broad CMV neutralization to the non-neutralizing UCA antibody. Structural studies revealed that this mutation mediated key contacts with the gB AD-2S1 epitope. Collectively, these results provide insight into potently neutralizing gB-directed antibody evolution in a single donor and lay a foundation for using this B cell-lineage directed approach for the design of next-generation CMV vaccines. Despite over 50 years of research, CMV vaccine candidates have achieved only up to 50% efficacy in clinical trials, in part due to challenges generating neutralizing antibody responses. One of the most promising targets is CMV gB, which mediates viral entry into host cells, and specifically the gB AD-2S1 epitope, which is a target of neutralizing antibodies in natural infection that have not yet been successfully elicited by vaccination. Utilizing B cell lineage analysis of a neutralizing gB AD-2S1-specific monoclonal antibody lineage, we identified a single, improbable heavy chain mutation that conferred neutralizing function and mediated a key contact within the epitope. Our study suggests that lineage-based vaccine design may be used to target induction of CMV gB AD-2S1-specific potently neutralizing antibodies.
Cytomegalovirus (CMV) is a leading cause of infant hearing loss and neurodevelopmental delay, but there are no clinically licensed vaccines to prevent infection, in part due to challenges eliciting neutralizing antibodies. One of the most well-studied targets for CMV vaccines is the viral fusogen glycoprotein B (gB), which is required for viral entry into host cells. Within gB, antigenic domain 2 site 1 (AD-2S1) is a target of potently neutralizing antibodies, but gB-based candidate vaccines have yet to elicit robust responses against this region. We mapped the genealogy of B cells encoding potently neutralizing anti-gB AD-2S1 antibodies from their inferred unmutated common ancestor (UCA) and characterized the binding and function of early lineage ancestors. Surprisingly, we found that a single amino acid heavy chain mutation A33N, which was an improbable mutation rarely generated by somatic hypermutation machinery, conferred broad CMV neutralization to the non-neutralizing UCA antibody. Structural studies revealed that this mutation mediated key contacts with the gB AD-2S1 epitope. Collectively, these results provide insight into potently neutralizing gB-directed antibody evolution in a single donor and lay a foundation for using this B cell-lineage directed approach for the design of next-generation CMV vaccines.Cytomegalovirus (CMV) is a leading cause of infant hearing loss and neurodevelopmental delay, but there are no clinically licensed vaccines to prevent infection, in part due to challenges eliciting neutralizing antibodies. One of the most well-studied targets for CMV vaccines is the viral fusogen glycoprotein B (gB), which is required for viral entry into host cells. Within gB, antigenic domain 2 site 1 (AD-2S1) is a target of potently neutralizing antibodies, but gB-based candidate vaccines have yet to elicit robust responses against this region. We mapped the genealogy of B cells encoding potently neutralizing anti-gB AD-2S1 antibodies from their inferred unmutated common ancestor (UCA) and characterized the binding and function of early lineage ancestors. Surprisingly, we found that a single amino acid heavy chain mutation A33N, which was an improbable mutation rarely generated by somatic hypermutation machinery, conferred broad CMV neutralization to the non-neutralizing UCA antibody. Structural studies revealed that this mutation mediated key contacts with the gB AD-2S1 epitope. Collectively, these results provide insight into potently neutralizing gB-directed antibody evolution in a single donor and lay a foundation for using this B cell-lineage directed approach for the design of next-generation CMV vaccines.
Audience Academic
Author Amin, Sharmi
Connors, Megan
Karthigeyan, Krithika
Venkatayogi, Sravani
Valencia, Sarah M.
Harnois, Melissa J.
Tu, Joshua J.
Wrapp, Daniel
Rochat, Eric
Jenks, Jennifer A.
Permar, Sallie R.
McLellan, Jason S.
Wiehe, Kevin
Kumar, Amit
Hora, Bhavna
Sponholtz, Madeline R.
AuthorAffiliation University of Wisconsin-Madison, UNITED STATES
3 Department of Pediatrics, Weill Cornell Medicine, New York, New York, United States of America
2 Department of Molecular Biosciences, The University of Texas at Austin, Austin, Texas, United States of America
4 Department of Medicine, Duke University School of Medicine, Durham, North Carolina, United States of America
1 Duke Human Vaccine Institute, Duke University Medical Center, Durham, North Carolina, United States of America
AuthorAffiliation_xml – name: 2 Department of Molecular Biosciences, The University of Texas at Austin, Austin, Texas, United States of America
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– name: University of Wisconsin-Madison, UNITED STATES
– name: 3 Department of Pediatrics, Weill Cornell Medicine, New York, New York, United States of America
– name: 4 Department of Medicine, Duke University School of Medicine, Durham, North Carolina, United States of America
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/36662906$$D View this record in MEDLINE/PubMed
https://www.osti.gov/servlets/purl/2470043$$D View this record in Osti.gov
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CitedBy_id crossref_primary_10_1073_pnas_2404250121
crossref_primary_10_3390_vaccines12111231
crossref_primary_10_1016_j_vaccine_2023_12_019
crossref_primary_10_1128_jvi_00213_24
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Copyright Copyright: © 2023 Jenks et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
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AC02-06CH11357
USDOE Office of Science (SC), Biological and Environmental Research (BER)
I have read the journal’s policy and the authors of this manuscript have the following competing interests: J.A.J. has been a paid invited speaker by Moderna x Popsugar. S.R.P. serves as a consultant for Moderna, Merck, Dynavax, Pfizer, and Hookipa CMV vaccine programs and has a sponsored research program on CMV vaccine immunogenicity with Moderna and Merck. J.A.J., K.W., and S.R.P. submitted a provisional patent (#9878-01-US) for antibodies described in this manuscript.
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SSID ssj0041316
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Snippet Cytomegalovirus (CMV) is a leading cause of infant hearing loss and neurodevelopmental delay, but there are no clinically licensed vaccines to prevent...
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doaj
pubmedcentral
osti
proquest
gale
pubmed
crossref
SourceType Open Website
Open Access Repository
Aggregation Database
Index Database
Enrichment Source
StartPage e1011107
SubjectTerms Amino acids
Antibodies
Antibodies, Neutralizing - genetics
Antibodies, Neutralizing - immunology
Antibodies, Viral - genetics
Antibodies, Viral - immunology
Antigens
BASIC BIOLOGICAL SCIENCES
Biology and Life Sciences
Care and treatment
Cell receptors
Cloning
Congenital diseases
Cytomegalovirus
Cytomegalovirus - genetics
Cytomegalovirus - immunology
Cytomegalovirus infections
Cytomegalovirus Infections - genetics
Cytomegalovirus Infections - immunology
Cytomegalovirus Vaccines - therapeutic use
Development and progression
Epitopes
Gene mutations
Genealogy
Genetic aspects
Glycoprotein B
Glycoproteins
Health aspects
Hearing loss
Host-virus relationships
Humans
Immune response
Infections
Lymphocytes B
Medicine and Health Sciences
Microbiology
Mutation
Neutralization
Neutralizing
Parasitology
Phylogenetics
Receptors, Antigen, B-Cell - genetics
Receptors, Antigen, B-Cell - immunology
Somatic hypermutation
Vaccines
Viral Envelope Proteins - genetics
Viral Envelope Proteins - immunology
Virology
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Title A single, improbable B cell receptor mutation confers potent neutralization against cytomegalovirus
URI https://www.ncbi.nlm.nih.gov/pubmed/36662906
https://www.proquest.com/docview/2777449600
https://www.proquest.com/docview/2768238356
https://www.osti.gov/servlets/purl/2470043
https://pubmed.ncbi.nlm.nih.gov/PMC9891502
https://doaj.org/article/111b8730bca84593945e121697cbd932
http://dx.doi.org/10.1371/journal.ppat.1011107
Volume 19
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