Systems‐wide analysis of BCR signalosomes and downstream phosphorylation and ubiquitylation
Open accessAbstract
B‐cell receptor (BCR) signaling is essential for the development and function of B cells; however, the spectrum of proteins involved in BCR signaling is not fully known. Here we used quantitative mass spectrometry‐based proteomics to monitor the dynamics of BCR signaling complexes (signalosomes) and to investigate the dynamics of downstream phosphorylation and ubiquitylation signaling. We identify most of the previously known components of BCR signaling, as well as many proteins that have not yet been implicated in this system. BCR activation leads to rapid tyrosine phosphorylation and ubiquitylation of the receptor‐proximal signaling components, many of which are co‐regulated by both the modifications. We illustrate the power of multilayered proteomic analyses for discovering novel BCR signaling components by demonstrating that BCR‐induced phosphorylation of RAB7A at S72 prevents its association with effector proteins and with endo‐lysosomal compartments. In addition, we show that BCL10 is modified by LUBAC‐mediated linear ubiquitylation, and demonstrate an important function of LUBAC in BCR‐induced NF‐κB signaling. Our results offer a global and integrated view of BCR signaling, and the provided datasets can serve as a valuable resource for further understanding BCR signaling networks.
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Anti-IgM antibodies stimulate B cells through the B cell receptor (BCR) thereby activating downstream signaling cascades like PI3K, AKT and MAPK pathways.
“Anti-IgM antibodies stimulate B cells through the B cell receptor (BCR) thereby activating further downstream signaling cascades like the phosphatidylinositol 3-kinase (PI3K), protein kinase B (AKT) and mitogen-activated protein kinase (MAPK) pathways [51–53].”
From The oncoprotein TBX3 is controlling severity in experimental arthritis (2019) · cites this paper as [53]
The Results (BCR-regulated phosphoproteome; page not provided) identify PI3K–AKT and RAS–MAPK as pathways activated by BCR signaling. However, the study stimulated BCRs with anti-IgG, not anti-IgM, as specified in the Results (Strategy for analysis of BCR-regulated signaling networks) and Methods (Cell stimulation). It therefore supports the downstream-pathway claim but not the stated antibody condition. (LLM, conf=0.90)
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Phosphoproteomics reveals that Parkinson's disease kinase LRRK2 regulates a subset of Rab GTPases
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Resolving the Complexity of Ubiquitin Networks
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Rapid and deep-scale ubiquitylation profiling for biology and translational research
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Self-citationMultilayered proteomics reveals molecular switches dictating ligand-dependent EGFR trafficking
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Self-citationTargeting Non-proteolytic Protein Ubiquitination for the Treatment of Diffuse Large B Cell Lymphoma
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Lymphocyte signaling and activation by the CARMA1-BCL10-MALT1 signalosome
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Met1-linked ubiquitin signalling in health and disease: inflammation, immunity, cancer, and beyond
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Chronic calcium signaling in IgE+ B cells limits plasma cell differentiation and survival
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Ubiquitin diGLY Proteomics as an Approach to Identify and Quantify the Ubiquitin-Modified Proteome
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Regulation of B cell receptor-dependent NF-κB signaling by the tumor suppressor KLHL14
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DPP9 is a novel component of the N-end rule pathway targeting the tyrosine kinase Syk
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BCL10 – Bridging CARDs to Immune Activation
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Post translational modifications of Rab GTPases
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Identification of differentially expressed peptides in high-throughput proteomics data
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Self-citationRegulation of B-Cell Receptor Signaling and Its Therapeutic Relevance in Aggressive B-Cell Lymphomas
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LUBAC accelerates B-cell lymphomagenesis by conferring resistance to genotoxic stress on B cells
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Molecular Mechanisms of B Cell Antigen Gathering and Endocytosis
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Self-citationSingle-cell intracellular epitope and transcript detection reveals signal transduction dynamics
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The Ins and Outs of Antigen Uptake in B cells
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Ubiquitination and phosphorylation of the CARD11-BCL10-MALT1 signalosome in T cells.
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MALT1 Phosphorylation Controls Activation of T Lymphocytes and Survival of ABC-DLBCL Tumor Cells
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Inhibition of Canonical NF-κB Signaling by a Small Molecule Targeting NEMO-Ubiquitin Interaction
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Ubiquitinomics: History, methods, and applications in basic research and drug discovery
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Population Genetic Structure and Selection Signature Analysis of Beijing Black Pig
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Automating UbiFast for High-throughput and Multiplexed Ubiquitin Enrichment
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A spatiotemporal map of co-receptor signaling networks underlying B cell activation
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Self-citationSyk degradation restrains plasma cell formation and promotes zonal transitions in germinal centers
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MALT1 substrate cleavage: what is it good for?
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Endophilin A2 regulates B-cell endocytosis and is required for germinal center and humoral responses
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Self-citationTargeting MALT1 for the treatment of diffuse large B-cell lymphoma
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Cross-regulation between LUBAC and caspase-1 modulates cell death and inflammation
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ANKRD13a controls early cell-death checkpoint by interacting with RIP1 independent of NF-κB
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K128 ubiquitination constrains RAS activity by expanding its binding interface with GAP proteins
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Post-translational modification of MALT1 and its role in B cell- and T cell-related diseases
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Advances in antibody discovery from human BCR repertoires
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From Affinity to Proximity Techniques to Investigate Protein Complexes in Plants
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The immunobiology of ubiquitin-dependent B cell receptor functions
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The oncoprotein TBX3 is controlling severity in experimental arthritis
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Self-citationQuantitative proteomics identifies PTP1B as modulator of B cell antigen receptor signaling
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KLHL6 Is Preferentially Expressed in Germinal Center–Derived B-Cell Lymphomas
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Ecm29-Dependent Proteasome Localization Regulates Cytoskeleton Remodeling at the Immune Synapse
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The LUBAC participates in Lysophosphatidic Acid-induced NF-κB Activation
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PTPN14 regulates Roquin2 stability by tyrosine dephosphorylation
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Serine 165 phosphorylation of SHARPIN regulates the activation of NF-κB
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Targeting B-Cell Receptor Signaling in Leukemia and Lymphoma: How and Why?
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- Authors
- Satpathy, S., Wagner, S. A., Beli, P., Gupta, R., Kristiansen, T. A., Malinova, D., Francavilla, C., Tolar, P., Bishop, G. A., Hostager, B. S., & Choudhary, C.
- Affiliations
- University of Copenhagen (DK)
- National Institute for Medical Research (GB)
- University of Iowa (US)
- Corresponding author
- Choudhary, Chunaram
- ORCID
- Venue
- Molecular Systems Biology
- Published
- 2015-06-01
- Volume
- 11
- Issue
- 6
- Pages
- 810-810
- ISSN
- 1744-4292 (ISSN-L)
- PMC
- PMC4501846
- OpenAlex
- W1894912312
- Cited by
- 124
- References
- 92
- Citations by year
- 2026: 3 · 2025: 3 · 2024: 9 · 2023: 10 · 2022: 9 · 2021: 17 · 2020: 19 · 2019: 7 · 2018: 14 · 2017: 15 · 2016: 16 · 2015: 2
- FWCI
- 5.18
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Molecular Systems Biology (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Research at the University of Copenhagen (University of Copenhagen) (publishedVersion, other-oa)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- Figshare (submittedVersion, cc-by)
- Research Explorer (The University of Manchester) (submittedVersion)
- Funders
- EMBO long‐term Fellowship
- Novo Nordisk Foundation (NNF14CC0001)
- EMBO Young Investigator Program
- Sapere Aude Program
- Danish Council for Independent Research
- Biological Sciences Funding Program
- Medical Research Council UK (U117597138)
- LOEWE Program Ubiquitin Networks (Ub‐Net) of the State of Hesse
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › NF-κB Signaling Pathways
- Physical Sciences › Chemistry › Spectroscopy › Advanced Proteomics Techniques and Applications
- Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
- Keywords
- B cell receptor signaling, signalosome, tyrosine phosphorylation, ubiquitination, LUBAC, Rab7, BCL10, NF-κB signaling, B cell development
- MeSH terms
- B-Cell CLL-Lymphoma 10 Protein, B-Lymphocytes, HeLa Cells, Humans, Membrane Proteins, Phosphorylation, Receptors, Antigen, B-Cell, Signal Transduction, NF-kappa B, Proteomics, Ubiquitin-Protein Ligases, Adaptor Proteins, Signal Transducing, Ubiquitination, HEK293 Cells
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