Phylogenetic analysis of migration, differentiation, and class switching in B cells

B cells undergo rapid mutation and selection for antibody binding affinity when producing antibodies capable of neutralizing pathogens. This evolutionary process can be intermixed with migration between tissues, differentiation between cellular subsets, and switching between functional isotypes. B c...

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Published inPLoS computational biology Vol. 18; no. 4; p. e1009885
Main Authors Hoehn, Kenneth B., Pybus, Oliver G., Kleinstein, Steven H.
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 01.04.2022
Public Library of Science (PLoS)
Subjects
Algorithms
Allergies
Antibodies
B cells
B-cell receptor
B-Lymphocytes
Biological research
Biology and Life Sciences
Biology, Experimental
Cell adhesion & migration
Cell Differentiation - genetics
Class switching
Computer and Information Sciences
Differentiation (biology)
Evolution
Food allergies
Food hypersensitivity
Genetic aspects
HIV
HIV Infections
Human immunodeficiency virus
Humans
Hypotheses
Immunoglobulin Class Switching
Information processing
Isotypes
Lymphocytes B
Medicine and Health Sciences
Mutation
Phylogenetics
Phylogeny
Phylogeography
Physical Sciences
Physiological aspects
Receptors, Antigen, B-Cell - genetics
Research and Analysis Methods
Statistical analysis
Statistics
Switching
United States
Online AccessGet full text
ISSN1553-7358
1553-734X
1553-7358
DOI10.1371/journal.pcbi.1009885

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Abstract B cells undergo rapid mutation and selection for antibody binding affinity when producing antibodies capable of neutralizing pathogens. This evolutionary process can be intermixed with migration between tissues, differentiation between cellular subsets, and switching between functional isotypes. B cell receptor (BCR) sequence data has the potential to elucidate important information about these processes. However, there is currently no robust, generalizable framework for making such inferences from BCR sequence data. To address this, we develop three parsimony-based summary statistics to characterize migration, differentiation, and isotype switching along B cell phylogenetic trees. We use simulations to demonstrate the effectiveness of this approach. We then use this framework to infer patterns of cellular differentiation and isotype switching from high throughput BCR sequence datasets obtained from patients in a study of HIV infection and a study of food allergy. These methods are implemented in the R package dowser , available at https://dowser.readthedocs.io .
AbstractList B cells undergo rapid mutation and selection for antibody binding affinity when producing antibodies capable of neutralizing pathogens. This evolutionary process can be intermixed with migration between tissues, differentiation between cellular subsets, and switching between functional isotypes. B cell receptor (BCR) sequence data has the potential to elucidate important information about these processes. However, there is currently no robust, generalizable framework for making such inferences from BCR sequence data. To address this, we develop three parsimony-based summary statistics to characterize migration, differentiation, and isotype switching along B cell phylogenetic trees. We use simulations to demonstrate the effectiveness of this approach. We then use this framework to infer patterns of cellular differentiation and isotype switching from high throughput BCR sequence datasets obtained from patients in a study of HIV infection and a study of food allergy. These methods are implemented in the R package dowser, available at https://dowser.readthedocs.io.
B cells undergo rapid mutation and selection for antibody binding affinity when producing antibodies capable of neutralizing pathogens. This evolutionary process can be intermixed with migration between tissues, differentiation between cellular subsets, and switching between functional isotypes. B cell receptor (BCR) sequence data has the potential to elucidate important information about these processes. However, there is currently no robust, generalizable framework for making such inferences from BCR sequence data. To address this, we develop three parsimony-based summary statistics to characterize migration, differentiation, and isotype switching along B cell phylogenetic trees. We use simulations to demonstrate the effectiveness of this approach. We then use this framework to infer patterns of cellular differentiation and isotype switching from high throughput BCR sequence datasets obtained from patients in a study of HIV infection and a study of food allergy. These methods are implemented in the R package dowser, available at https://dowser.readthedocs.io.B cells undergo rapid mutation and selection for antibody binding affinity when producing antibodies capable of neutralizing pathogens. This evolutionary process can be intermixed with migration between tissues, differentiation between cellular subsets, and switching between functional isotypes. B cell receptor (BCR) sequence data has the potential to elucidate important information about these processes. However, there is currently no robust, generalizable framework for making such inferences from BCR sequence data. To address this, we develop three parsimony-based summary statistics to characterize migration, differentiation, and isotype switching along B cell phylogenetic trees. We use simulations to demonstrate the effectiveness of this approach. We then use this framework to infer patterns of cellular differentiation and isotype switching from high throughput BCR sequence datasets obtained from patients in a study of HIV infection and a study of food allergy. These methods are implemented in the R package dowser, available at https://dowser.readthedocs.io.
B cells undergo rapid mutation and selection for antibody binding affinity when producing antibodies capable of neutralizing pathogens. This evolutionary process can be intermixed with migration between tissues, differentiation between cellular subsets, and switching between functional isotypes. B cell receptor (BCR) sequence data has the potential to elucidate important information about these processes. However, there is currently no robust, generalizable framework for making such inferences from BCR sequence data. To address this, we develop three parsimony-based summary statistics to characterize migration, differentiation, and isotype switching along B cell phylogenetic trees. We use simulations to demonstrate the effectiveness of this approach. We then use this framework to infer patterns of cellular differentiation and isotype switching from high throughput BCR sequence datasets obtained from patients in a study of HIV infection and a study of food allergy. These methods are implemented in the R package dowser , available at https://dowser.readthedocs.io . B cells produce high affinity antibodies through an evolutionary process of mutation and selection during adaptive immune responses. Migration between tissues, differentiation to cellular subtypes, and switching between different antibody isotypes can be important factors in shaping the role B cells play in response to infection, autoimmune disease, and allergies. B cell receptor (BCR) sequence data has the potential to elucidate important information about these processes. However, there is currently no robust, generalizable framework for making such inferences from BCR sequence data. Here, we develop three parsimony-based summary statistics to characterize migration, differentiation, and isotype switching along B cell phylogenetic trees. We confirm the effectiveness of our approach using simulations and further apply our method to data from patients with HIV and allergy. Our methods are released in the R package dowser : https://dowser.readthedocs.io .
B cells undergo rapid mutation and selection for antibody binding affinity when producing antibodies capable of neutralizing pathogens. This evolutionary process can be intermixed with migration between tissues, differentiation between cellular subsets, and switching between functional isotypes. B cell receptor (BCR) sequence data has the potential to elucidate important information about these processes. However, there is currently no robust, generalizable framework for making such inferences from BCR sequence data. To address this, we develop three parsimony-based summary statistics to characterize migration, differentiation, and isotype switching along B cell phylogenetic trees. We use simulations to demonstrate the effectiveness of this approach. We then use this framework to infer patterns of cellular differentiation and isotype switching from high throughput BCR sequence datasets obtained from patients in a study of HIV infection and a study of food allergy. These methods are implemented in the R package dowser, available at https://dowser.readthedocs.io. Author summary B cells produce high affinity antibodies through an evolutionary process of mutation and selection during adaptive immune responses. Migration between tissues, differentiation to cellular subtypes, and switching between different antibody isotypes can be important factors in shaping the role B cells play in response to infection, autoimmune disease, and allergies. B cell receptor (BCR) sequence data has the potential to elucidate important information about these processes. However, there is currently no robust, generalizable framework for making such inferences from BCR sequence data. Here, we develop three parsimony-based summary statistics to characterize migration, differentiation, and isotype switching along B cell phylogenetic trees. We confirm the effectiveness of our approach using simulations and further apply our method to data from patients with HIV and allergy. Our methods are released in the R package dowser: https://dowser.readthedocs.io.
B cells undergo rapid mutation and selection for antibody binding affinity when producing antibodies capable of neutralizing pathogens. This evolutionary process can be intermixed with migration between tissues, differentiation between cellular subsets, and switching between functional isotypes. B cell receptor (BCR) sequence data has the potential to elucidate important information about these processes. However, there is currently no robust, generalizable framework for making such inferences from BCR sequence data. To address this, we develop three parsimony-based summary statistics to characterize migration, differentiation, and isotype switching along B cell phylogenetic trees. We use simulations to demonstrate the effectiveness of this approach. We then use this framework to infer patterns of cellular differentiation and isotype switching from high throughput BCR sequence datasets obtained from patients in a study of HIV infection and a study of food allergy. These methods are implemented in the R package dowser, available at
B cells undergo rapid mutation and selection for antibody binding affinity when producing antibodies capable of neutralizing pathogens. This evolutionary process can be intermixed with migration between tissues, differentiation between cellular subsets, and switching between functional isotypes. B cell receptor (BCR) sequence data has the potential to elucidate important information about these processes. However, there is currently no robust, generalizable framework for making such inferences from BCR sequence data. To address this, we develop three parsimony-based summary statistics to characterize migration, differentiation, and isotype switching along B cell phylogenetic trees. We use simulations to demonstrate the effectiveness of this approach. We then use this framework to infer patterns of cellular differentiation and isotype switching from high throughput BCR sequence datasets obtained from patients in a study of HIV infection and a study of food allergy. These methods are implemented in the R package dowser , available at https://dowser.readthedocs.io .
Audience Academic
Author Pybus, Oliver G.
Kleinstein, Steven H.
Hoehn, Kenneth B.
AuthorAffiliation 2 Department of Zoology, University of Oxford, Oxford, United Kingdom
Columbia University Medical Center: Columbia University Irving Medical Center, UNITED STATES
5 Department of Immunobiology, Yale School of Medicine, New Haven, Connecticut, United States of America
1 Department of Pathology, Yale School of Medicine, New Haven, Connecticut, United States of America
4 Program in Computational Biology and Bioinformatics, Yale University, New Haven, Connecticut, United States of America
3 Department of Pathobiology and Population Sciences, Royal Veterinary College London, London, United Kingdom
AuthorAffiliation_xml – name: 1 Department of Pathology, Yale School of Medicine, New Haven, Connecticut, United States of America
– name: 3 Department of Pathobiology and Population Sciences, Royal Veterinary College London, London, United Kingdom
– name: 4 Program in Computational Biology and Bioinformatics, Yale University, New Haven, Connecticut, United States of America
– name: 5 Department of Immunobiology, Yale School of Medicine, New Haven, Connecticut, United States of America
– name: 2 Department of Zoology, University of Oxford, Oxford, United Kingdom
– name: Columbia University Medical Center: Columbia University Irving Medical Center, UNITED STATES
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I have read the journal’s policy and the authors of this manuscript have the following competing interests: S.H.K. receives consulting fees from Northrop Grumman and Peraton. K.B.H receives consulting fees from Prellis Biologics.
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Snippet B cells undergo rapid mutation and selection for antibody binding affinity when producing antibodies capable of neutralizing pathogens. This evolutionary...
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SubjectTerms Algorithms
Allergies
Antibodies
B cells
B-cell receptor
B-Lymphocytes
Biological research
Biology and Life Sciences
Biology, Experimental
Cell adhesion & migration
Cell Differentiation - genetics
Class switching
Computer and Information Sciences
Differentiation (biology)
Evolution
Food allergies
Food hypersensitivity
Genetic aspects
HIV
HIV Infections
Human immunodeficiency virus
Humans
Hypotheses
Immunoglobulin Class Switching
Information processing
Isotypes
Lymphocytes B
Medicine and Health Sciences
Mutation
Phylogenetics
Phylogeny
Phylogeography
Physical Sciences
Physiological aspects
Receptors, Antigen, B-Cell - genetics
Research and Analysis Methods
Statistical analysis
Statistics
Switching
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Title Phylogenetic analysis of migration, differentiation, and class switching in B cells
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http://dx.doi.org/10.1371/journal.pcbi.1009885
Volume 18
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