Dynamic regulation of B cell complement signaling is integral to germinal center responses

Maturation of B cells within germinal centers (GCs) generates diversified B cell pools and high-affinity B cell antigen receptors (BCRs) for pathogen clearance. Increased receptor affinity is achieved by iterative cycles of T cell–dependent, affinity-based B cell positive selection and clonal expans...

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Published inNature Immunology Vol. 22; no. 6; pp. 757 - 768
Main Authors Cumpelik, Arun, Heja, David, Hu, Yuan, Varano, Gabriele, Ordikhani, Farideh, Roberto, Mark P., He, Zhengxiang, Homann, Dirk, Lira, Sergio A., Dominguez-Sola, David, Heeger, Peter S.
Format Journal Article
LanguageEnglish
Published New York Springer Science and Business Media LLC 01.06.2021
Nature Publishing Group US
Nature Publishing Group
Subjects
631/250/2152/2153/1982
631/250/2501
Affinity
Animals
Animals, B-Lymphocytes, CD55 Antigens, CD59 Antigens, Clonal Hematopoiesis, Lymphocyte Activation
Animals, Genetically Modified
Antigens
B cells
B-cell receptor
B-Lymphocytes
B-Lymphocytes - immunology
B-Lymphocytes - metabolism
Bcl-6 protein
Biomedical and Life Sciences
Biomedicine
CD40 antigen
CD55 Antigens
CD55 Antigens - genetics
CD55 Antigens - metabolism
CD59 antigen
CD59 Antigens
CD59 Antigens - metabolism
Cell activation
Cell Line, Tumor
Cellular signal transduction
Clonal Hematopoiesis
Clonal Hematopoiesis - immunology
Clonal selection
Complement (Immunology)
Complement Activation
Complement C3a
Complement C3a - metabolism
Complement C5a
Complement C5a - metabolism
Complement component C3
Complement component C5a
Complement regulatory proteins
Decay-accelerating factor
Genetic aspects
Germinal Center
Germinal Center - cytology
Germinal Center - immunology
Germinal Center - metabolism
Germinal centers
Health aspects
Humans
Immunology
Infectious Diseases
Lymphocyte Activation
Lymphocytes B
Lymphocytes T
Lymphoid tissue
Membrane attack complex
Mice
Palatine Tonsil
Palatine Tonsil - cytology
Palatine Tonsil - pathology
Physiological aspects
Positive selection
Proto-Oncogene Proteins c-bcl-6
Proto-Oncogene Proteins c-bcl-6 - metabolism
Rapamycin
Receptor, Anaphylatoxin C5a
Receptor, Anaphylatoxin C5a - genetics
Receptor, Anaphylatoxin C5a - metabolism
Receptors, Antigen, B-Cell
Receptors, Antigen, B-Cell - metabolism
Receptors, Complement
Receptors, Complement - genetics
Receptors, Complement - metabolism
Signal Transduction
Signal Transduction - immunology
TOR protein
TOR Serine-Threonine Kinases
TOR Serine-Threonine Kinases - metabolism
Transcription factors
United States
Online AccessGet full text
ISSN1529-2908
1529-2916
1529-2916
DOI10.1038/s41590-021-00926-0

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Abstract Maturation of B cells within germinal centers (GCs) generates diversified B cell pools and high-affinity B cell antigen receptors (BCRs) for pathogen clearance. Increased receptor affinity is achieved by iterative cycles of T cell–dependent, affinity-based B cell positive selection and clonal expansion by mechanisms hitherto incompletely understood. Here we found that, as part of a physiologic program, GC B cells repressed expression of decay-accelerating factor (DAF/CD55) and other complement C3 convertase regulators via BCL6, but increased the expression of C5b-9 inhibitor CD59. These changes permitted C3 cleavage on GC B cell surfaces without the formation of membrane attack complex and activated C3a- and C5a-receptor signals required for positive selection. Genetic disruption of this pathway in antigen-activated B cells by conditional transgenic DAF overexpression or deletion of C3a and C5a receptors limited the activation of mechanistic target of rapamycin (mTOR) in response to BCR–CD40 signaling, causing premature GC collapse and impaired affinity maturation. These results reveal that coordinated shifts in complement regulation within the GC provide crucial signals underlying GC B cell positive selection. Heeger and colleagues report that activated B cells dynamically regulate the expression of complement regulatory proteins via the transcription factor BCL6. C3 convertase activity and C3aR1–C5aR1 signaling were both necessary for optimal B cell activation and germinal center formation.
AbstractList Maturation of B cells within germinal centers (GCs) generates diversified B cell pools and high-affinity B cell antigen receptors (BCRs) for pathogen clearance. Increased receptor affinity is achieved by iterative cycles of T cell-dependent, affinity-based B cell positive selection and clonal expansion by mechanisms hitherto incompletely understood. Here we found that, as part of a physiologic program, GC B cells repressed expression of decay-accelerating factor (DAF/CD55) and other complement C3 convertase regulators via BCL6, but increased the expression of C5b-9 inhibitor CD59. These changes permitted C3 cleavage on GC B cell surfaces without the formation of membrane attack complex and activated C3a- and C5a-receptor signals required for positive selection. Genetic disruption of this pathway in antigen-activated B cells by conditional transgenic DAF overexpression or deletion of C3a and C5a receptors limited the activation of mechanistic target of rapamycin (mTOR) in response to BCR-CD40 signaling, causing premature GC collapse and impaired affinity maturation. These results reveal that coordinated shifts in complement regulation within the GC provide crucial signals underlying GC B cell positive selection.
Maturation of B cells within germinal centers (GCs) generates diversified B cell pools and high-affinity B cell antigen receptors (BCRs) for pathogen clearance. Increased receptor affinity is achieved by iterative cycles of T cell–dependent, affinity-based B cell positive selection and clonal expansion by mechanisms hitherto incompletely understood. Here we found that, as part of a physiologic program, GC B cells repressed expression of decay-accelerating factor (DAF/CD55) and other complement C3 convertase regulators via BCL6, but increased the expression of C5b-9 inhibitor CD59. These changes permitted C3 cleavage on GC B cell surfaces without the formation of membrane attack complex and activated C3a- and C5a-receptor signals required for positive selection. Genetic disruption of this pathway in antigen-activated B cells by conditional transgenic DAF overexpression or deletion of C3a and C5a receptors limited the activation of mechanistic target of rapamycin (mTOR) in response to BCR–CD40 signaling, causing premature GC collapse and impaired affinity maturation. These results reveal that coordinated shifts in complement regulation within the GC provide crucial signals underlying GC B cell positive selection. Heeger and colleagues report that activated B cells dynamically regulate the expression of complement regulatory proteins via the transcription factor BCL6. C3 convertase activity and C3aR1–C5aR1 signaling were both necessary for optimal B cell activation and germinal center formation.
Maturation of B cells within germinal centers (GCs) generates diversified B cell pools and high-affinity B cell antigen receptors (BCRs) for pathogen clearance. Increased receptor affinity is achieved by iterative cycles of T cell-dependent, affinity-based B cell positive selection and clonal expansion by mechanisms hitherto incompletely understood. Here we found that, as part of a physiologic program, GC B cells repressed expression of decay-accelerating factor (DAF/CD55) and other complement C3 convertase regulators via BCL6, but increased the expression of C5b-9 inhibitor CD59. These changes permitted C3 cleavage on GC B cell surfaces without the formation of membrane attack complex and activated C3a- and C5a-receptor signals required for positive selection. Genetic disruption of this pathway in antigen-activated B cells by conditional transgenic DAF overexpression or deletion of C3a and C5a receptors limited the activation of mechanistic target of rapamycin (mTOR) in response to BCR-CD40 signaling, causing premature GC collapse and impaired affinity maturation. These results reveal that coordinated shifts in complement regulation within the GC provide crucial signals underlying GC B cell positive selection. Heeger and colleagues report that activated B cells dynamically regulate the expression of complement regulatory proteins via the transcription factor BCL6. C3 convertase activity and C3aR1-C5aR1 signaling were both necessary for optimal B cell activation and germinal center formation.
Maturation of B cells within germinal centers (GCs) generates diversified B cell pools and high-affinity B cell antigen receptors (BCRs) for pathogen clearance. Increased receptor affinity is achieved by iterative cycles of T cell-dependent, affinity-based B cell positive selection and clonal expansion by mechanisms hitherto incompletely understood. Here we found that, as part of a physiologic program, GC B cells repressed expression of decay-accelerating factor (DAF/CD55) and other complement C3 convertase regulators via BCL6, but increased the expression of C5b-9 inhibitor CD59. These changes permitted C3 cleavage on GC B cell surfaces without the formation of membrane attack complex and activated C3a- and C5a-receptor signals required for positive selection. Genetic disruption of this pathway in antigen-activated B cells by conditional transgenic DAF overexpression or deletion of C3a and C5a receptors limited the activation of mechanistic target of rapamycin (mTOR) in response to BCR-CD40 signaling, causing premature GC collapse and impaired affinity maturation. These results reveal that coordinated shifts in complement regulation within the GC provide crucial signals underlying GC B cell positive selection.Maturation of B cells within germinal centers (GCs) generates diversified B cell pools and high-affinity B cell antigen receptors (BCRs) for pathogen clearance. Increased receptor affinity is achieved by iterative cycles of T cell-dependent, affinity-based B cell positive selection and clonal expansion by mechanisms hitherto incompletely understood. Here we found that, as part of a physiologic program, GC B cells repressed expression of decay-accelerating factor (DAF/CD55) and other complement C3 convertase regulators via BCL6, but increased the expression of C5b-9 inhibitor CD59. These changes permitted C3 cleavage on GC B cell surfaces without the formation of membrane attack complex and activated C3a- and C5a-receptor signals required for positive selection. Genetic disruption of this pathway in antigen-activated B cells by conditional transgenic DAF overexpression or deletion of C3a and C5a receptors limited the activation of mechanistic target of rapamycin (mTOR) in response to BCR-CD40 signaling, causing premature GC collapse and impaired affinity maturation. These results reveal that coordinated shifts in complement regulation within the GC provide crucial signals underlying GC B cell positive selection.
B cell maturation within germinal centers (GCs) generates diversified B cell pools and high-affinity B cell antigen receptors (BCRs) for pathogen clearance. Increased receptor affinity is achieved by iterative cycles of T cell-dependent, affinity-based B cell positive selection and clonal expansion by incompletely understood mechanisms. Here, we found that as part of a physiologic program, GC B cells repressed expression of decay-accelerating factor (DAF/CD55) and other complement C3-convertase regulators via Bcl-6, but increased C5b-9 inhibitor (CD59) expression. These changes permitted C3 cleavage on GC B cell surfaces, without membrane attack complex formation, and activated C3a-receptor and C5a-receptor signals required for positive selection. Genetic disruption of this pathway in antigen-activated B cells, by conditional transgenic DAF overexpression or deletion of C3a and C5a receptors, limited mTOR activity in response to BCR-CD40 signaling, causing premature GC collapse and impaired affinity maturation. These results reveal that coordinated shifts in complement regulation within the GC provide crucial signals underlying GC B cell positive selection.
Audience Academic
Author Arun Cumpelik
David Heja
Gabriele Varano
Mark P. Roberto
Dirk Homann
Zhengxiang He
Peter S. Heeger
Farideh Ordikhani
Sergio A. Lira
Yuan Hu
David Dominguez-Sola
AuthorAffiliation 6 Graduate School of Biomedical Sciences, Icahn School of Medicine at Mount Sinai, New York, NY
1 Renal Division, Department of Medicine, Icahn School of Medicine at Mount Sinai, New York, NY
3 Department of Oncological Sciences, Icahn School of Medicine at Mount Sinai, New York, NY
7 Department of Pathology, Icahn School of Medicine at Mount Sinai, New York, New York, USA
5 Precision Immunology Institute, Icahn School of Medicine at Mount Sinai, New York, NY
4 Tisch Cancer Institute, Icahn School of Medicine at Mount Sinai, New York, NY
2 Translational Transplant Research Center, Icahn School of Medicine at Mount Sinai, New York, NY
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BackLink https://cir.nii.ac.jp/crid/1870583643269491456$$DView record in CiNii
https://www.ncbi.nlm.nih.gov/pubmed/34031614$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
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COPYRIGHT 2021 Nature Publishing Group
The Author(s), under exclusive licence to Springer Nature America, Inc. 2021.
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– notice: COPYRIGHT 2021 Nature Publishing Group
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These authors jointly supervised this work
Author contributions: A.C. contributed to the study design, performed the majority of in vivo and in vitro studies, prepared figures, wrote and edited the manuscript. D.H. and Z.H designed and prepared the DAF-TM targeting construct and performed in vitro characterization of the DAF-TM gene product in founder mice. Y.H and G.V. performed the studies on DAF gene regulation by BCL-6 experiments, BCR sequencing and together with M.P.R. performed RNA-Seq analyses, as well as reviewed and edited the manuscript. F.O. performed experiments including all studies with B1-8hi mice and reviewed and edited the manuscript. D.H. and S.L. outlined the strategy for DAF-TM generation, served as critical reviewers of data and edited the manuscript. D.D-S. and P.S.H. conceptualized, designed and supervised the project, reviewed all data, wrote and edited the manuscript and provided funding.
Present addresses: Gabriele Varano: Department of Translational Medicine, Laboratory for Advanced Therapy Technologies (LTTA), University of Ferrara, Ferrara, Italy, David Heja: eGenesis Inc. Cambridge Massachusetts, USA
ORCID 0000-0001-9569-8402
0000-0002-8961-859x
0000-0002-7622-5754
0000-0002-8961-859X
0000-0003-4673-6913
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Snippet Maturation of B cells within germinal centers (GCs) generates diversified B cell pools and high-affinity B cell antigen receptors (BCRs) for pathogen...
Maturation of B cells within germinal centers (GCs) generates diversified B cell pools and high-affinity B cell antigen receptors (BCRs) for pathogen...
B cell maturation within germinal centers (GCs) generates diversified B cell pools and high-affinity B cell antigen receptors (BCRs) for pathogen clearance....
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SourceType Open Access Repository
Aggregation Database
Index Database
Enrichment Source
Publisher
StartPage 757
SubjectTerms 631/250/2152/2153/1982
631/250/2501
Affinity
Animals
Animals, B-Lymphocytes, CD55 Antigens, CD59 Antigens, Clonal Hematopoiesis, Lymphocyte Activation
Animals, Genetically Modified
Antigens
B cells
B-cell receptor
B-Lymphocytes
B-Lymphocytes - immunology
B-Lymphocytes - metabolism
Bcl-6 protein
Biomedical and Life Sciences
Biomedicine
CD40 antigen
CD55 Antigens
CD55 Antigens - genetics
CD55 Antigens - metabolism
CD59 antigen
CD59 Antigens
CD59 Antigens - metabolism
Cell activation
Cell Line, Tumor
Cellular signal transduction
Clonal Hematopoiesis
Clonal Hematopoiesis - immunology
Clonal selection
Complement (Immunology)
Complement Activation
Complement C3a
Complement C3a - metabolism
Complement C5a
Complement C5a - metabolism
Complement component C3
Complement component C5a
Complement regulatory proteins
Decay-accelerating factor
Genetic aspects
Germinal Center
Germinal Center - cytology
Germinal Center - immunology
Germinal Center - metabolism
Germinal centers
Health aspects
Humans
Immunology
Infectious Diseases
Lymphocyte Activation
Lymphocytes B
Lymphocytes T
Lymphoid tissue
Membrane attack complex
Mice
Palatine Tonsil
Palatine Tonsil - cytology
Palatine Tonsil - pathology
Physiological aspects
Positive selection
Proto-Oncogene Proteins c-bcl-6
Proto-Oncogene Proteins c-bcl-6 - metabolism
Rapamycin
Receptor, Anaphylatoxin C5a
Receptor, Anaphylatoxin C5a - genetics
Receptor, Anaphylatoxin C5a - metabolism
Receptors, Antigen, B-Cell
Receptors, Antigen, B-Cell - metabolism
Receptors, Complement
Receptors, Complement - genetics
Receptors, Complement - metabolism
Signal Transduction
Signal Transduction - immunology
TOR protein
TOR Serine-Threonine Kinases
TOR Serine-Threonine Kinases - metabolism
Transcription factors
Title Dynamic regulation of B cell complement signaling is integral to germinal center responses
URI https://cir.nii.ac.jp/crid/1870583643269491456
https://link.springer.com/article/10.1038/s41590-021-00926-0
https://www.ncbi.nlm.nih.gov/pubmed/34031614
https://www.proquest.com/docview/2532427442
https://www.proquest.com/docview/2532246084
https://pubmed.ncbi.nlm.nih.gov/PMC8297556
Volume 22
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