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Article ; Online: Antigen-independent, autonomous B cell receptor signaling drives activated B cell DLBCL.

Eken, Janneke A / Koning, Marvyn T / Kupcova, Kristyna / Sepúlveda Yáñez, Julieta H / de Groen, Ruben A L / Quinten, Edwin / Janssen, Jurriaan / van Bergen, Cornelis A M / Vermaat, Joost S P / Cleven, Arjen / Navarrete, Marcelo A / Ylstra, Bauke / de Jong, Daphne / Havranek, Ondrej / Jumaa, Hassan / Veelken, Hendrik

The Journal of experimental medicine

2024 Volume 221, Issue 5

Abstract: Diffuse large B cell lymphoma of activated B cell type (ABC-DLBCL), a major cell-of-origin DLBCL subtype, is characterized by chronic active B cell receptor (BCR) signaling and NF-κB activation, which can be explained by activating mutations of the BCR ... ...

Abstract	Diffuse large B cell lymphoma of activated B cell type (ABC-DLBCL), a major cell-of-origin DLBCL subtype, is characterized by chronic active B cell receptor (BCR) signaling and NF-κB activation, which can be explained by activating mutations of the BCR signaling cascade in a minority of cases. We demonstrate that autonomous BCR signaling, akin to its essential pathogenetic role in chronic lymphocytic leukemia (CLL), can explain chronic active BCR signaling in ABC-DLBCL. 13 of 18 tested DLBCL-derived BCR, including 12 cases selected for expression of IgM, induced spontaneous calcium flux and increased phosphorylation of the BCR signaling cascade in murine triple knockout pre-B cells without antigenic stimulation or external BCR crosslinking. Autonomous BCR signaling was associated with IgM isotype, dependent on somatic BCR mutations and individual HCDR3 sequences, and largely restricted to non-GCB DLBCL. Autonomous BCR signaling represents a novel immunological oncogenic driver mechanism in DLBCL originating from individual BCR sequences and adds a new dimension to currently proposed genetics- and transcriptomics-based DLBCL classifications.
MeSH term(s)	Animals ; Mice ; B-Lymphocytes ; Lymphoma, Large B-Cell, Diffuse/genetics ; Leukemia, Lymphocytic, Chronic, B-Cell ; Receptors, Antigen, B-Cell ; Immunoglobulin M
Chemical Substances	Receptors, Antigen, B-Cell ; Immunoglobulin M
Language	English
Publishing date	2024-03-21
Publishing country	United States
Document type	Journal Article
ZDB-ID	218343-2
ISSN	1540-9538 ; 0022-1007
ISSN (online)	1540-9538
ISSN	0022-1007
DOI	10.1084/jem.20230941
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Article ; Online: Acquisition of a glycosylated B-cell receptor drives follicular lymphoma toward a dark zone phenotype.

van Bergen, Cornelis A M / Kloet, Susan L / Quinten, Edwin / Sepúlveda Yáñez, Julieta H / Menafra, Roberta / Griffioen, Marieke / Jansen, Patty M / Koning, Marvyn T / Knijnenburg, Jeroen / Navarrete, Marcelo A / Kiełbasa, Szymon M / Veelken, Hendrik

Blood advances

2023 Volume 7, Issue 19, Page(s) 5812–5816

Language	English
Publishing date	2023-07-24
Publishing country	United States
Document type	Journal Article
ZDB-ID	2915908-8
ISSN	2473-9537 ; 2473-9529
ISSN (online)	2473-9537
ISSN	2473-9529
DOI	10.1182/bloodadvances.2023010725
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Article ; Online: Autonomous B-cell receptor signaling and genetic aberrations in chronic lymphocytic leukemia-phenotype monoclonal B lymphocytosis in siblings of patients with chronic lymphocytic leukemia.

Haematologica

2024 Volume 109, Issue 3, Page(s) 824–834

Abstract: Clonal expansion of CD5-expressing B cells, commonly designated as monoclonal B lymphocytosis (MBL), is a precursor condition for chronic lymphocytic leukemia (CLL). The mechanisms driving subclinical MBL B-cell expansion and progression to CLL, ... ...

Abstract	Clonal expansion of CD5-expressing B cells, commonly designated as monoclonal B lymphocytosis (MBL), is a precursor condition for chronic lymphocytic leukemia (CLL). The mechanisms driving subclinical MBL B-cell expansion and progression to CLL, occurring in approximately 1% of affected individuals, are unknown. An autonomously signaling B-cell receptor (BCR) is essential for the pathogenesis of CLL. The objectives of this study were functional characterization of the BCR of MBL in siblings of CLL patients and a comparison of genetic variants in MBL-CLL sibling pairs. Screening of peripheral blood by flow cytometry detected 0.2-480 clonal CLL-phenotype cells per microliter (median: 37/μL) in 34 of 191 (17.8%) siblings of CLL patients. Clonal BCR isolated from highly purified CLL-phenotype cells induced robust calcium mobilization in BCR-deficient murine pre-B cells in the absence of external antigen and without experimental crosslinking. This autonomous BCR signal was less intense than the signal originating from the CLL BCR of their CLL siblings. According to genotyping by single nucleotide polymorphism array, whole exome, and targeted panel sequencing, CLL risk alleles were found with high and similar prevalence in CLL patients and MBL siblings, respectively. Likewise, the prevalence of recurrent CLL-associated genetic variants was similar between CLL and matched MBL samples. However, copy number variations and small variants were frequently subclonal in MBL cells, suggesting their acquisition during subclinical clonal expansion. These findings support a stepwise model of CLL pathogenesis, in which autonomous BCR signaling leads to a non-malignant (oligo)clonal expansion of CD5+ B cells, followed by malignant progression to CLL after acquisition of pathogenic genetic variants.
MeSH term(s)	Humans ; Animals ; Mice ; Leukemia, Lymphocytic, Chronic, B-Cell/genetics ; Siblings ; DNA Copy Number Variations ; Lymphocytosis/genetics ; Leukemia ; Receptors, Antigen, B-Cell/genetics ; Phenotype
Chemical Substances	Receptors, Antigen, B-Cell
Language	English
Publishing date	2024-03-01
Publishing country	Italy
Document type	Journal Article
ZDB-ID	2333-4
ISSN	1592-8721 ; 0017-6567 ; 0390-6078
ISSN (online)	1592-8721
ISSN	0017-6567 ; 0390-6078
DOI	10.3324/haematol.2022.282542
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Article ; Online: Expanding the repertoire reveals recurrent, cryptic, and hematopoietic HLA class I minor histocompatibility antigens.

Fuchs, Kyra J / van de Meent, Marian / Honders, M Willy / Khatri, Indu / Kester, Michel G D / Koster, Eva A S / Koutsoumpli, Georgia / de Ru, Arnoud H / van Bergen, Cornelis A M / van Veelen, Peter A / 't Hoen, Peter A C / van Balen, Peter / van den Akker, Erik B / Veelken, J Hendrik / Halkes, Constantijn J M / Falkenburg, J H Frederik / Griffioen, Marieke

Blood

2024 Volume 143, Issue 18, Page(s) 1856–1872

Abstract: Abstract: Allogeneic stem cell transplantation (alloSCT) is a curative treatment for hematological malignancies. After HLA-matched alloSCT, antitumor immunity is caused by donor T cells recognizing polymorphic peptides, designated minor ... ...

Abstract	Abstract: Allogeneic stem cell transplantation (alloSCT) is a curative treatment for hematological malignancies. After HLA-matched alloSCT, antitumor immunity is caused by donor T cells recognizing polymorphic peptides, designated minor histocompatibility antigens (MiHAs), that are presented by HLA on malignant patient cells. However, T cells often target MiHAs on healthy nonhematopoietic tissues of patients, thereby inducing side effects known as graft-versus-host disease. Here, we aimed to identify the dominant repertoire of HLA-I-restricted MiHAs to enable strategies to predict, monitor or modulate immune responses after alloSCT. To systematically identify novel MiHAs by genome-wide association screening, T-cell clones were isolated from 39 transplanted patients and tested for reactivity against 191 Epstein-Barr virus transformed B cell lines of the 1000 Genomes Project. By discovering 81 new MiHAs, we more than doubled the antigen repertoire to 159 MiHAs and demonstrated that, despite many genetic differences between patients and donors, often the same MiHAs are targeted in multiple patients. Furthermore, we showed that one quarter of the antigens are cryptic, that is translated from unconventional open reading frames, for example long noncoding RNAs, showing that these antigen types are relevant targets in natural immune responses. Finally, using single cell RNA-seq data, we analyzed tissue expression of MiHA-encoding genes to explore their potential role in clinical outcome, and characterized 11 new hematopoietic-restricted MiHAs as potential targets for immunotherapy. In conclusion, we expanded the repertoire of HLA-I-restricted MiHAs and identified recurrent, cryptic and hematopoietic-restricted antigens, which are fundamental to predict, follow or manipulate immune responses to improve clinical outcome after alloSCT.
MeSH term(s)	Humans ; Minor Histocompatibility Antigens/genetics ; Minor Histocompatibility Antigens/immunology ; Hematopoietic Stem Cell Transplantation ; Histocompatibility Antigens Class I/immunology ; Histocompatibility Antigens Class I/genetics ; Hematologic Neoplasms/immunology ; Hematologic Neoplasms/therapy ; Hematologic Neoplasms/genetics ; T-Lymphocytes/immunology ; Genome-Wide Association Study ; Transplantation, Homologous ; Female ; Male
Chemical Substances	Minor Histocompatibility Antigens ; Histocompatibility Antigens Class I
Language	English
Publishing date	2024-03-01
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	80069-7
ISSN	1528-0020 ; 0006-4971
ISSN (online)	1528-0020
ISSN	0006-4971
DOI	10.1182/blood.2023022343
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Article ; Online: Prognosis of IGLV3-21

Hengeveld, Paul J / Veelken, Hendrik / van Bergen, Cornelis A M / Quinten, Edwin / Vervoordeldonk, Mischa Y L / Ismailzada, Wahija / Barendse, Rob S / Dubois, Julie M N / van Oers, Marinus H J / Geisler, Christian H / Kater, Arnon P / Westerweel, Peter E / Langerak, Anton W / Levin, Mark-David

Leukemia

2023 Volume 37, Issue 9, Page(s) 1929–1932

MeSH term(s)	Humans ; Leukemia, Lymphocytic, Chronic, B-Cell/drug therapy ; Prognosis
Language	English
Publishing date	2023-07-21
Publishing country	England
Document type	Letter
ZDB-ID	807030-1
ISSN	1476-5551 ; 0887-6924
ISSN (online)	1476-5551
ISSN	0887-6924
DOI	10.1038/s41375-023-01975-0
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Article: Autosomal Minor Histocompatibility Antigens: How Genetic Variants Create Diversity in Immune Targets.

Griffioen, Marieke / van Bergen, Cornelis A M / Falkenburg, J H Frederik

Frontiers in immunology

2016 Volume 7, Page(s) 100

Abstract: Allogeneic stem cell transplantation (alloSCT) can be a curative treatment for hematological malignancies. Unfortunately, the desired anti-tumor or graft-versus-leukemia (GvL) effect is often accompanied with undesired side effects against healthy ... ...

Abstract	Allogeneic stem cell transplantation (alloSCT) can be a curative treatment for hematological malignancies. Unfortunately, the desired anti-tumor or graft-versus-leukemia (GvL) effect is often accompanied with undesired side effects against healthy tissues known as graft-versus-host disease (GvHD). After HLA-matched alloSCT, GvL and GvHD are both mediated by donor-derived T-cells recognizing polymorphic peptides presented by HLA surface molecules on patient cells. These polymorphic peptides or minor histocompatibility antigens (MiHA) are produced by genetic differences between patient and donor. Since polymorphic peptides may be useful targets to manipulate the balance between GvL and GvHD, the dominant repertoire of MiHA needs to be discovered. In this review, the diversity of autosomal MiHA characterized thus far as well as the various molecular mechanisms by which genetic variants create immune targets and the role of cryptic transcripts and proteins as antigen sources are described. The tissue distribution of MiHA as important factor in GvL and GvHD is considered as well as possibilities how hematopoietic MiHA can be used for immunotherapy to augment GvL after alloSCT. Although more MiHA are still needed for comprehensive understanding of the biology of GvL and GvHD and manipulation by immunotherapy, this review shows insight into the composition and kinetics of in vivo immune responses with respect to specificity, diversity, and frequency of specific T-cells and surface expression of HLA-peptide complexes and other (accessory) molecules on the target cell. A complex interplay between these factors and their environment ultimately determines the spectrum of clinical manifestations caused by immune responses after alloSCT.
Language	English
Publishing date	2016
Publishing country	Switzerland
Document type	Journal Article ; Review
ZDB-ID	2606827-8
ISSN	1664-3224
ISSN	1664-3224
DOI	10.3389/fimmu.2016.00100
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Article ; Online: Peripheral IgE Repertoires of Healthy Donors Carry Moderate Mutation Loads and Do Not Overlap With Other Isotypes.

Koning, Marvyn T / Trollmann, Ignis J M / van Bergen, Cornelis A M / Alvarez Saravia, Diego / Navarrete, Marcelo A / Kiełbasa, Szymon M / Veelken, Hendrik

Frontiers in immunology

2019 Volume 10, Page(s) 1543

Abstract: IgE-mediated allergic disease represents an increasing health problem. Although numerous studies have investigated IgE sequences in allergic patients, little information is available on the healthy IgE repertoire. IgM, IgG, IgA, and IgE transcripts from ... ...

Abstract	IgE-mediated allergic disease represents an increasing health problem. Although numerous studies have investigated IgE sequences in allergic patients, little information is available on the healthy IgE repertoire. IgM, IgG, IgA, and IgE transcripts from peripheral blood B cells of five healthy, non-atopic individuals were amplified by unbiased, template-switching, isotype-specific PCR. Complete VDJ regions were sequenced to near-exhaustion on the PacBio platform. Sequences were analyzed for clonal relationships, degree of somatic hypermutation, IGHV gene usage, evidence of antigenic selection, and N-linked glycosylation motifs. IgE repertoires appeared to be highly oligoclonal with preferential usage of certain IGHV genes compared to the other isotypes. IgE sequences carried more somatic mutations than IgM, yet fewer than IgG and IgA. Many IgE sequences contained N-linked glycosylation motifs. IgE sequences had no clonal relationship with the other isotypes. The IgE repertoire in healthy individuals is derived from relatively few clonal expansions without apparent relations to immune reactions that give rise to IgG or IgA. The mutational burden of normal IgE suggests an origin through direct class-switching from the IgM repertoire with little evidence of antigenic drive, and hence presumably low affinity for specific antigens. These findings are compatible with a primary function of the healthy IgE repertoire to occupy Fcε receptors for competitive protection against mast cell degranulation induced by allergen-specific, high-affinity IgE. This background knowledge may help to elucidate pathogenic mechanisms in allergic disease and to design improved desensitization strategies.
MeSH term(s)	Adult ; Antibody Affinity/genetics ; B-Lymphocytes/immunology ; Female ; Glycosylation ; Humans ; Immunoglobulin A/genetics ; Immunoglobulin A/immunology ; Immunoglobulin E/genetics ; Immunoglobulin E/immunology ; Immunoglobulin G/genetics ; Immunoglobulin G/immunology ; Immunoglobulin M/genetics ; Immunoglobulin M/immunology ; Male ; Middle Aged ; Mutation
Chemical Substances	Immunoglobulin A ; Immunoglobulin G ; Immunoglobulin M ; Immunoglobulin E (37341-29-0)
Language	English
Publishing date	2019-07-03
Publishing country	Switzerland
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2606827-8
ISSN	1664-3224 ; 1664-3224
ISSN (online)	1664-3224
ISSN	1664-3224
DOI	10.3389/fimmu.2019.01543
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Article ; Online: Integration of Mutational Signature Analysis with 3D Chromatin Data Unveils Differential AID-Related Mutagenesis in Indolent Lymphomas.

Sepulveda-Yanez, Julieta H / Alvarez-Saravia, Diego / Fernandez-Goycoolea, Jose / Aldridge, Jacqueline / van Bergen, Cornelis A M / Posthuma, Ward / Uribe-Paredes, Roberto / Veelken, Hendrik / Navarrete, Marcelo A

International journal of molecular sciences

2021 Volume 22, Issue 23

Abstract: Activation-induced deaminase (AID) is required for somatic hypermutation in immunoglobulin genes, but also induces off-target mutations. Follicular lymphoma (FL) and chronic lymphocytic leukemia (CLL), the most frequent types of indolent B-cell tumors, ... ...

Abstract	Activation-induced deaminase (AID) is required for somatic hypermutation in immunoglobulin genes, but also induces off-target mutations. Follicular lymphoma (FL) and chronic lymphocytic leukemia (CLL), the most frequent types of indolent B-cell tumors, are exposed to AID activity during lymphomagenesis. We designed a workflow integrating de novo mutational signatures extraction and fitting of COSMIC (Catalogue Of Somatic Mutations In Cancer) signatures, with tridimensional chromatin conformation data (Hi-C). We applied the workflow to exome sequencing data from lymphoma samples. In 33 FL and 30 CLL samples, 42% and 34% of the contextual mutations could be traced to a known AID motif. We demonstrate that both CLL and FL share mutational processes dominated by spontaneous deamination, failures in DNA repair, and AID activity. The processes had equiproportional distribution across active and nonactive chromatin compartments in CLL. In contrast, canonical AID activity and failures in DNA repair pathways in FL were significantly higher within the active chromatin compartment. Analysis of DNA repair genes revealed a higher prevalence of base excision repair gene mutations (
MeSH term(s)	Alleles ; Chromatin/metabolism ; Cytidine Deaminase/genetics ; DNA Mutational Analysis ; DNA Repair/genetics ; Databases, Genetic ; Gene Frequency ; Humans ; Leukemia, Lymphocytic, Chronic, B-Cell/genetics ; Leukemia, Lymphocytic, Chronic, B-Cell/pathology ; Lymphoma, Follicular/genetics ; Lymphoma, Follicular/pathology ; Polymorphism, Single Nucleotide
Chemical Substances	Chromatin ; AICDA (activation-induced cytidine deaminase) (EC 3.5.4.-) ; Cytidine Deaminase (EC 3.5.4.5)
Language	English
Publishing date	2021-12-01
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2019364-6
ISSN	1422-0067 ; 1422-0067 ; 1661-6596
ISSN (online)	1422-0067
ISSN	1422-0067 ; 1661-6596
DOI	10.3390/ijms222313015
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Article ; Online: CACTUS: integrating clonal architecture with genomic clustering and transcriptome profiling of single tumor cells.

Shafighi, Shadi Darvish / Kiełbasa, Szymon M / Sepúlveda-Yáñez, Julieta / Monajemi, Ramin / Cats, Davy / Mei, Hailiang / Menafra, Roberta / Kloet, Susan / Veelken, Hendrik / van Bergen, Cornelis A M / Szczurek, Ewa

Genome medicine

2021 Volume 13, Issue 1, Page(s) 45

Abstract: Background: Drawing genotype-to-phenotype maps in tumors is of paramount importance for understanding tumor heterogeneity. Assignment of single cells to their tumor clones of origin can be approached by matching the genotypes of the clones to the ... ...

Abstract	Background: Drawing genotype-to-phenotype maps in tumors is of paramount importance for understanding tumor heterogeneity. Assignment of single cells to their tumor clones of origin can be approached by matching the genotypes of the clones to the mutations found in RNA sequencing of the cells. The confidence of the cell-to-clone mapping can be increased by accounting for additional measurements. Follicular lymphoma, a malignancy of mature B cells that continuously acquire mutations in parallel in the exome and in B cell receptor loci, presents a unique opportunity to join exome-derived mutations with B cell receptor sequences as independent sources of evidence for clonal evolution. Methods: Here, we propose CACTUS, a probabilistic model that leverages the information from an independent genomic clustering of cells and exploits the scarce single cell RNA sequencing data to map single cells to given imperfect genotypes of tumor clones. Results: We apply CACTUS to two follicular lymphoma patient samples, integrating three measurements: whole exome, single-cell RNA, and B cell receptor sequencing. CACTUS outperforms a predecessor model by confidently assigning cells and B cell receptor-based clusters to the tumor clones. Conclusions: The integration of independent measurements increases model certainty and is the key to improving model performance in the challenging task of charting the genotype-to-phenotype maps in tumors. CACTUS opens the avenue to study the functional implications of tumor heterogeneity, and origins of resistance to targeted therapies. CACTUS is written in R and source code, along with all supporting files, are available on GitHub ( https://github.com/LUMC/CACTUS ).
MeSH term(s)	Clone Cells ; Cluster Analysis ; Gene Expression Profiling ; Gene Expression Regulation, Neoplastic ; Genomics ; Humans ; Lymphoma, Follicular/genetics ; Models, Statistical ; Neoplasms/genetics ; Reproducibility of Results ; Single-Cell Analysis ; Software ; Whole Exome Sequencing
Language	English
Publishing date	2021-03-24
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2484394-5
ISSN	1756-994X ; 1756-994X
ISSN (online)	1756-994X
ISSN	1756-994X
DOI	10.1186/s13073-021-00842-w
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Article ; Online: Templated insertions at VD and DJ junctions create unique B-cell receptors in the healthy B-cell repertoire.

Koning, Marvyn T / Vletter, Esther M / Rademaker, Rik / Vergroesen, Rochelle D / Trollmann, Ignis J M / Parren, Paul / van Bergen, Cornelis A M / Scherer, Hans U / Kiełbasa, Szymon M / Toes, René E M / Veelken, Hendrik

European journal of immunology

2020 Volume 50, Issue 12, Page(s) 2099–2101

Abstract: RAG complexes recognise (cryptic) RSS sites both in and outside immunoglobulin sites. Excision circles may be reinserted into V(D)J rearrangements as long templated insertions to diversify the adaptive immune repertoire. We show that such VDJ with ... ...

Abstract	RAG complexes recognise (cryptic) RSS sites both in and outside immunoglobulin sites. Excision circles may be reinserted into V(D)J rearrangements as long templated insertions to diversify the adaptive immune repertoire. We show that such VDJ with templated insertions are incidentally found in the repertoire of healthy donors.
MeSH term(s)	Adaptive Immunity/genetics ; Adaptive Immunity/immunology ; B-Lymphocytes/immunology ; Humans ; Receptors, Antigen, B-Cell/genetics ; Receptors, Antigen, B-Cell/immunology ; V(D)J Recombination/genetics ; V(D)J Recombination/immunology ; VDJ Recombinases/genetics ; VDJ Recombinases/immunology
Chemical Substances	Receptors, Antigen, B-Cell ; VDJ Recombinases (EC 2.7.7.-)
Language	English
Publishing date	2020-08-27
Publishing country	Germany
Document type	Letter ; Research Support, Non-U.S. Gov't
ZDB-ID	120108-6
ISSN	1521-4141 ; 0014-2980
ISSN (online)	1521-4141
ISSN	0014-2980
DOI	10.1002/eji.202048828
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