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Granzyme B produced by human plasmacytoid dendritic cells suppresses T-cell expansion
Open accessAbstract
Human plasmacytoid dendritic cells (pDCs) are crucially involved in the modulation of adaptive T-cell responses in the course of neoplastic, viral, and autoimmune disorders. In several of these diseases elevated extracellular levels of the serine protease granzyme B (GrB) are observed. Here we demonstrate that human pDCs can be an abundant source of GrB and that such GrB+ pDCs potently suppress T-cell proliferation in a GrB-dependent, perforin-independent manner, a process reminiscent of regulatory T cells. Moreover, we show that GrB expression is strictly regulated on a transcriptional level involving Janus kinase 1 (JAK1), signal transducer and activator of transcription 3 (STAT3), and STAT5 and that interleukin-3 (IL-3), a cytokine secreted by activated T cells, plays a central role for GrB induction. Moreover, we find that the immunosuppressive cytokine IL-10 enhances, while Toll-like receptor agonists and CD40 ligand strongly inhibit, GrB secretion by pDCs. GrB-secreting pDCs may play a regulatory role for immune evasion of tumors, antiviral immune responses, and autoimmune processes. Our results provide novel information about the complex network of pDC–T-cell interactions and may contribute to an improvement of prophylactic and therapeutic vaccinations.
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“Differential gene analyses showed that pDCs were enriched in proinflammatory genes (MZB1, SPIB and UGCG), enabling them to secrete high amounts of IFNα and genes such as TLR7 and GZMB27, reported to mediate inflammation resolution and suppression of T cell expansion, respectively (Fig. 4c,d).”
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Cites
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Plasmacytoid dendritic cells sense self-DNA coupled with antimicrobial peptide
Lande, R., Gregorio, J., Facchinetti, V., Chatterjee, B., Wang, Y.-H., Homey, B., Cao, W., Wang, Y.-H., Su, B., Nestle, F. O., et al. (2007) · Nature · doi:10.1038/nature06116 · Cited by 1,910
Plasmacytoid dendritic cells in immunity
Colonna, M., Trinchieri, G., & Liu, Y. (2004) · Nature Immunology · doi:10.1038/ni1141 · Cited by 1,659
IPC: Professional Type 1 Interferon-Producing Cells and Plasmacytoid Dendritic Cell Precursors
Liu, Y.-J. (2004) · Annual Review of Immunology · doi:10.1146/annurev.immunol.23.021704.115633 · Cited by 1,618
Plasmacytoid dendritic cells: sensing nucleic acids in viral infection and autoimmune diseases
Gilliet, M., Cao, W., & Liu, Y.-J. (2008) · Nature Reviews Immunology · doi:10.1038/nri2358 · Cited by 1,190
Grouard, G., Rissoan, M., Filgueira, L., Durand, I., Banchereau, J., & Liu, Y.-J. (1997) · The Journal of Experimental Medicine · doi:10.1084/jem.185.6.1101 · Cited by 1,187
Granzyme B and Perforin Are Important for Regulatory T Cell-Mediated Suppression of Tumor Clearance
Cao, X., Cai, S. F., Fehniger, T. A., Song, J., Collins, L. I., Piwnica-Worms, D. R., & Ley, T. J. (2007) · Immunity · doi:10.1016/j.immuni.2007.08.014 · Cited by 1,117
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Death by a Thousand Cuts: Granzyme Pathways of Programmed Cell Death
Chowdhury, D., & Lieberman, J. (2008) · Annual Review of Immunology · doi:10.1146/annurev.immunol.26.021607.090404 · Cited by 705
Antigen-presentation properties of plasmacytoid dendritic cells.
Villadangos, J., & Young, L. J. (2008) · Immunity · doi:10.1016/j.immuni.2008.09.002 · Cited by 577
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Metadata
- Authors
- Jahrsdörfer, B., Vollmer, A., Blackwell, S. E., Maier, J., Sontheimer, K., Beyer, T., Mandel, B., Lunov, O., Tron, K., Nienhaus, G. U., Simmet, T., Debatin, K.-M., Weiner, G. J., & Fabricius, D.
- Affiliations
- Universität Ulm (DE)
- University of Iowa (US)
- Institute of Pharmacology (CZ)
- Karlsruhe Institute of Technology (DE)
- ORCID
- Venue
- Blood
- Publisher
- American Society of Hematology
- Published
- 2010-02-11
- Volume
- 115
- Issue
- 6
- Pages
- 1156-1165
- ISSN
- 0006-4971 (ISSN-L)
- 1528-0020
- PMC
- PMC2920226
- OpenAlex
- W2018280156
- Cited by
- 180
- References
- 57
- Citations by year
- 2026: 6 · 2025: 13 · 2024: 11 · 2023: 10 · 2022: 18 · 2021: 6 · 2020: 17 · 2019: 8 · 2018: 9 · 2017: 11 · 2016: 5 · 2015: 11 · 2014: 10 · 2013: 17 · 2012: 11
- FWCI
- 3.88
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Blood (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Leuka
- Deutscher Akademischer Austauschdienst
- Deutsche Forschungsgemeinschaft
- Universität Ulm
- National Cancer Institute (P50CA97274, P50CA097274)
- European Social Fund
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
- Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
- Life Sciences › Immunology and Microbiology › Immunology › Cytokine Signaling Pathways and Interactions
- Keywords
- granzyme B, plasmacytoid dendritic cells, T cell suppression, regulatory T cells, JAK1, STAT3, STAT5, interleukin-3, IL-10, TLR agonists, CD40 ligand, transcriptional regulation, tumor immune evasion, antiviral immunity, autoimmune disease, prophylactic and therapeutic vaccination
- MeSH terms
- Arthritis, Juvenile, Cell Differentiation, Cells, Cultured, Child, Cytotoxicity, Immunologic, Dendritic Cells, Enzyme-Linked Immunosorbent Assay, Flow Cytometry, Humans, Interleukin-3, Lymphocyte Activation, RNA, Messenger, T-Lymphocytes, Blotting, Western, Signal Transduction, Reverse Transcriptase Polymerase Chain Reaction, Cell Proliferation, STAT3 Transcription Factor, STAT5 Transcription Factor, Granzymes
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