Convergent evolution and B-cell recirculation in germinal centers in a human lymph node

Germinal centers (GCs) play a central role in generating an effective immune response against infectious pathogens, and failures in their regulating mechanisms can lead to the development of autoimmune diseases and cancer. Although previous works study experimental systems of the immune response wit...

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Published in:Life science alliance Vol. 6; no. 11; p. e202301959
Main Authors: Pelissier, Aurelien, Stratigopoulou, Maria, Donner, Naomi, Dimitriadis, Evangelos, Bende, Richard J, Guikema, Jeroen E, Rodriguez Martinez, Maria, van Noesel, Carel JM
Format: Journal Article
Language:English
Published: United States Life Science Alliance 01.11.2023
Life Science Alliance LLC
Subjects:
Animal models
Animals
Antigens
Autoimmune Diseases
B-Lymphocytes
Cloning
Competitive advantage
Germinal Center
Germinal centers
Humans
Immunization
Lymph Nodes
Lymphatic system
Lymphocytes B
Mice
Mutation
Phylogeny
Reproducibility
ISSN:2575-1077, 2575-1077
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Abstract Germinal centers (GCs) play a central role in generating an effective immune response against infectious pathogens, and failures in their regulating mechanisms can lead to the development of autoimmune diseases and cancer. Although previous works study experimental systems of the immune response with mouse models that are immunized with specific antigens, our study focused on a real-life situation, with an ongoing GC response in a human lymph node (LN) involving multiple asynchronized GCs reacting simultaneously to unknown antigens. We combined laser capture microdissection of individual GCs from human LN with next-generation repertoire sequencing to characterize individual GCs as distinct evolutionary spaces. In line with well-characterized GC responses in mice, elicited by immunization with model antigens, we observe a heterogeneous clonal diversity across individual GCs from the same human LN. Still, we identify shared clones in several individual GCs, and phylogenetic tree analysis combined with paratope modeling suggest the re-engagement and rediversification of B-cell clones across GCs and expanded clones exhibiting shared antigen responses across distinct GCs, indicating convergent evolution of the GCs.
AbstractList Germinal centers (GCs) play a central role in generating an effective immune response against infectious pathogens, and failures in their regulating mechanisms can lead to the development of autoimmune diseases and cancer. Although previous works study experimental systems of the immune response with mouse models that are immunized with specific antigens, our study focused on a real-life situation, with an ongoing GC response in a human lymph node (LN) involving multiple asynchronized GCs reacting simultaneously to unknown antigens. We combined laser capture microdissection of individual GCs from human LN with next-generation repertoire sequencing to characterize individual GCs as distinct evolutionary spaces. In line with well-characterized GC responses in mice, elicited by immunization with model antigens, we observe a heterogeneous clonal diversity across individual GCs from the same human LN. Still, we identify shared clones in several individual GCs, and phylogenetic tree analysis combined with paratope modeling suggest the re-engagement and rediversification of B-cell clones across GCs and expanded clones exhibiting shared antigen responses across distinct GCs, indicating convergent evolution of the GCs.Germinal centers (GCs) play a central role in generating an effective immune response against infectious pathogens, and failures in their regulating mechanisms can lead to the development of autoimmune diseases and cancer. Although previous works study experimental systems of the immune response with mouse models that are immunized with specific antigens, our study focused on a real-life situation, with an ongoing GC response in a human lymph node (LN) involving multiple asynchronized GCs reacting simultaneously to unknown antigens. We combined laser capture microdissection of individual GCs from human LN with next-generation repertoire sequencing to characterize individual GCs as distinct evolutionary spaces. In line with well-characterized GC responses in mice, elicited by immunization with model antigens, we observe a heterogeneous clonal diversity across individual GCs from the same human LN. Still, we identify shared clones in several individual GCs, and phylogenetic tree analysis combined with paratope modeling suggest the re-engagement and rediversification of B-cell clones across GCs and expanded clones exhibiting shared antigen responses across distinct GCs, indicating convergent evolution of the GCs.
Germinal centers (GCs) play a central role in generating an effective immune response against infectious pathogens, and failures in their regulating mechanisms can lead to the development of autoimmune diseases and cancer. Although previous works study experimental systems of the immune response with mouse models that are immunized with specific antigens, our study focused on a real-life situation, with an ongoing GC response in a human lymph node (LN) involving multiple asynchronized GCs reacting simultaneously to unknown antigens. We combined laser capture microdissection of individual GCs from human LN with next-generation repertoire sequencing to characterize individual GCs as distinct evolutionary spaces. In line with well-characterized GC responses in mice, elicited by immunization with model antigens, we observe a heterogeneous clonal diversity across individual GCs from the same human LN. Still, we identify shared clones in several individual GCs, and phylogenetic tree analysis combined with paratope modeling suggest the re-engagement and rediversification of B-cell clones across GCs and expanded clones exhibiting shared antigen responses across distinct GCs, indicating convergent evolution of the GCs.
The study characterizes an ongoing immune response by sequencing B-cells from 10 germinal centers and finds diverse clonal patterns and convergent evolution, indicating re-engagement and rediversification of B-cell clones across GCs. Germinal centers (GCs) play a central role in generating an effective immune response against infectious pathogens, and failures in their regulating mechanisms can lead to the development of autoimmune diseases and cancer. Although previous works study experimental systems of the immune response with mouse models that are immunized with specific antigens, our study focused on a real-life situation, with an ongoing GC response in a human lymph node (LN) involving multiple asynchronized GCs reacting simultaneously to unknown antigens. We combined laser capture microdissection of individual GCs from human LN with next-generation repertoire sequencing to characterize individual GCs as distinct evolutionary spaces. In line with well-characterized GC responses in mice, elicited by immunization with model antigens, we observe a heterogeneous clonal diversity across individual GCs from the same human LN. Still, we identify shared clones in several individual GCs, and phylogenetic tree analysis combined with paratope modeling suggest the re-engagement and rediversification of B-cell clones across GCs and expanded clones exhibiting shared antigen responses across distinct GCs, indicating convergent evolution of the GCs.
Author Pelissier, Aurelien
Guikema, Jeroen E
Stratigopoulou, Maria
van Noesel, Carel JM
Donner, Naomi
Dimitriadis, Evangelos
Bende, Richard J
Rodriguez Martinez, Maria
AuthorAffiliation 2 Department of Biosystems Science and Engineering, ETH Zurich, Basel, Switzerland
4 MonetDB Solutions, Amsterdam, Netherlands
3 Department of Pathology, Amsterdam University Medical Centers, Location AMC, Lymphoma and Myeloma Center Amsterdam, Amsterdam, Netherlands
1 https://ror.org/02js37d36 IBM Research Europe , Rüschlikon, Switzerland
AuthorAffiliation_xml – name: 2 Department of Biosystems Science and Engineering, ETH Zurich, Basel, Switzerland
– name: 1 https://ror.org/02js37d36 IBM Research Europe , Rüschlikon, Switzerland
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– name: 3 Department of Pathology, Amsterdam University Medical Centers, Location AMC, Lymphoma and Myeloma Center Amsterdam, Amsterdam, Netherlands
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Aurelien Pelissier and Maria Stratigopoulou contributed equally to this work
Jeroen E Guikema, Rodriguez Martinez, and Carel JM van Noesel contributed equally to this work
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Snippet Germinal centers (GCs) play a central role in generating an effective immune response against infectious pathogens, and failures in their regulating mechanisms...
The study characterizes an ongoing immune response by sequencing B-cells from 10 germinal centers and finds diverse clonal patterns and convergent evolution,...
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StartPage e202301959
SubjectTerms Animal models
Animals
Antigens
Autoimmune Diseases
B-Lymphocytes
Cloning
Competitive advantage
Germinal Center
Germinal centers
Humans
Immunization
Lymph Nodes
Lymphatic system
Lymphocytes B
Mice
Mutation
Phylogeny
Reproducibility
Title Convergent evolution and B-cell recirculation in germinal centers in a human lymph node
URI https://www.ncbi.nlm.nih.gov/pubmed/37640448
https://www.proquest.com/docview/3251116415
https://www.proquest.com/docview/2858989680
https://pubmed.ncbi.nlm.nih.gov/PMC10462906
Volume 6
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