A20 and ABIN-1 cooperate in balancing CBM complex-triggered NF-κB signaling in activated T cells

Research output: Contribution to journal › Journal article › Research › peer-review

Standard

A20 and ABIN-1 cooperate in balancing CBM complex-triggered NF-κB signaling in activated T cells. / Yin, Hongli; Karayel, Ozge; Chao, Ying-Yin; Seeholzer, Thomas; Hamp, Isabel; Plettenburg, Oliver; Gehring, Torben; Zielinski, Christina; Mann, Matthias; Krappmann, Daniel.

In: Cellular and Molecular Life Sciences, Vol. 79, No. 2, 31.01.2022, p. 112.

Research output: Contribution to journal › Journal article › Research › peer-review

Harvard

Yin, H, Karayel, O, Chao, Y-Y, Seeholzer, T, Hamp, I, Plettenburg, O, Gehring, T, Zielinski, C, Mann, M & Krappmann, D 2022, 'A20 and ABIN-1 cooperate in balancing CBM complex-triggered NF-κB signaling in activated T cells', Cellular and Molecular Life Sciences, vol. 79, no. 2, pp. 112. https://doi.org/10.1007/s00018-022-04154-z

APA

Yin, H., Karayel, O., Chao, Y-Y., Seeholzer, T., Hamp, I., Plettenburg, O., Gehring, T., Zielinski, C., Mann, M., & Krappmann, D. (2022). A20 and ABIN-1 cooperate in balancing CBM complex-triggered NF-κB signaling in activated T cells. Cellular and Molecular Life Sciences, 79(2), 112. https://doi.org/10.1007/s00018-022-04154-z

Vancouver

Yin H, Karayel O, Chao Y-Y, Seeholzer T, Hamp I, Plettenburg O et al. A20 and ABIN-1 cooperate in balancing CBM complex-triggered NF-κB signaling in activated T cells. Cellular and Molecular Life Sciences. 2022 Jan 31;79(2):112. https://doi.org/10.1007/s00018-022-04154-z

Author

Yin, Hongli ; Karayel, Ozge ; Chao, Ying-Yin ; Seeholzer, Thomas ; Hamp, Isabel ; Plettenburg, Oliver ; Gehring, Torben ; Zielinski, Christina ; Mann, Matthias ; Krappmann, Daniel. / A20 and ABIN-1 cooperate in balancing CBM complex-triggered NF-κB signaling in activated T cells. In: Cellular and Molecular Life Sciences. 2022 ; Vol. 79, No. 2. pp. 112.

Bibtex

@article{67d534c8d524421da3bb664be5b01136,
title = "A20 and ABIN-1 cooperate in balancing CBM complex-triggered NF-κB signaling in activated T cells",
abstract = "T cell activation initiates protective adaptive immunity, but counterbalancing mechanisms are critical to prevent overshooting responses and to maintain immune homeostasis. The CARD11-BCL10-MALT1 (CBM) complex bridges T cell receptor engagement to NF-κB signaling and MALT1 protease activation. Here, we show that ABIN-1 is modulating the suppressive function of A20 in T cells. Using quantitative mass spectrometry, we identified ABIN-1 as an interactor of the CBM signalosome in activated T cells. A20 and ABIN-1 counteract inducible activation of human primary CD4 and Jurkat T cells. While A20 overexpression is able to silence CBM complex-triggered NF-κB and MALT1 protease activation independent of ABIN-1, the negative regulatory function of ABIN-1 depends on A20. The suppressive function of A20 in T cells relies on ubiquitin binding through the C-terminal zinc finger (ZnF)4/7 motifs, but does not involve the deubiquitinating activity of the OTU domain. Our mechanistic studies reveal that the A20/ABIN-1 module is recruited to the CBM complex via A20 ZnF4/7 and that proteasomal degradation of A20 and ABIN-1 releases the CBM complex from the negative impact of both regulators. Ubiquitin binding to A20 ZnF4/7 promotes destructive K48-polyubiquitination to itself and to ABIN-1. Further, after prolonged T cell stimulation, ABIN-1 antagonizes MALT1-catalyzed cleavage of re-synthesized A20 and thereby diminishes sustained CBM complex signaling. Taken together, interdependent post-translational mechanisms are tightly controlling expression and activity of the A20/ABIN-1 silencing module and the cooperative action of both negative regulators is critical to balance CBM complex signaling and T cell activation.",
keywords = "B-Cell CLL-Lymphoma 10 Protein/metabolism, CARD Signaling Adaptor Proteins/metabolism, Cells, Cultured, DNA-Binding Proteins/physiology, Guanylate Cyclase/metabolism, HEK293 Cells, Humans, Jurkat Cells, Lymphocyte Activation/genetics, Mucosa-Associated Lymphoid Tissue Lymphoma Translocation 1 Protein/metabolism, Multiprotein Complexes/metabolism, NF-kappa B/metabolism, Protein Binding, RNA Interference/immunology, Signal Transduction/physiology, T-Lymphocytes/immunology, Tumor Necrosis Factor alpha-Induced Protein 3/physiology",
author = "Hongli Yin and Ozge Karayel and Ying-Yin Chao and Thomas Seeholzer and Isabel Hamp and Oliver Plettenburg and Torben Gehring and Christina Zielinski and Matthias Mann and Daniel Krappmann",
note = "{\textcopyright} 2022. The Author(s).",
year = "2022",
month = jan,
day = "31",
doi = "10.1007/s00018-022-04154-z",
language = "English",
volume = "79",
pages = "112",
journal = "Cellular and Molecular Life Sciences",
issn = "1420-682X",
publisher = "Birkhauser Verlag Basel",
number = "2",

}

RIS

TY - JOUR

T1 - A20 and ABIN-1 cooperate in balancing CBM complex-triggered NF-κB signaling in activated T cells

AU - Yin, Hongli

AU - Karayel, Ozge

AU - Chao, Ying-Yin

AU - Seeholzer, Thomas

AU - Hamp, Isabel

AU - Plettenburg, Oliver

AU - Gehring, Torben

AU - Zielinski, Christina

AU - Mann, Matthias

AU - Krappmann, Daniel

N1 - © 2022. The Author(s).

PY - 2022/1/31

Y1 - 2022/1/31

N2 - T cell activation initiates protective adaptive immunity, but counterbalancing mechanisms are critical to prevent overshooting responses and to maintain immune homeostasis. The CARD11-BCL10-MALT1 (CBM) complex bridges T cell receptor engagement to NF-κB signaling and MALT1 protease activation. Here, we show that ABIN-1 is modulating the suppressive function of A20 in T cells. Using quantitative mass spectrometry, we identified ABIN-1 as an interactor of the CBM signalosome in activated T cells. A20 and ABIN-1 counteract inducible activation of human primary CD4 and Jurkat T cells. While A20 overexpression is able to silence CBM complex-triggered NF-κB and MALT1 protease activation independent of ABIN-1, the negative regulatory function of ABIN-1 depends on A20. The suppressive function of A20 in T cells relies on ubiquitin binding through the C-terminal zinc finger (ZnF)4/7 motifs, but does not involve the deubiquitinating activity of the OTU domain. Our mechanistic studies reveal that the A20/ABIN-1 module is recruited to the CBM complex via A20 ZnF4/7 and that proteasomal degradation of A20 and ABIN-1 releases the CBM complex from the negative impact of both regulators. Ubiquitin binding to A20 ZnF4/7 promotes destructive K48-polyubiquitination to itself and to ABIN-1. Further, after prolonged T cell stimulation, ABIN-1 antagonizes MALT1-catalyzed cleavage of re-synthesized A20 and thereby diminishes sustained CBM complex signaling. Taken together, interdependent post-translational mechanisms are tightly controlling expression and activity of the A20/ABIN-1 silencing module and the cooperative action of both negative regulators is critical to balance CBM complex signaling and T cell activation.

AB - T cell activation initiates protective adaptive immunity, but counterbalancing mechanisms are critical to prevent overshooting responses and to maintain immune homeostasis. The CARD11-BCL10-MALT1 (CBM) complex bridges T cell receptor engagement to NF-κB signaling and MALT1 protease activation. Here, we show that ABIN-1 is modulating the suppressive function of A20 in T cells. Using quantitative mass spectrometry, we identified ABIN-1 as an interactor of the CBM signalosome in activated T cells. A20 and ABIN-1 counteract inducible activation of human primary CD4 and Jurkat T cells. While A20 overexpression is able to silence CBM complex-triggered NF-κB and MALT1 protease activation independent of ABIN-1, the negative regulatory function of ABIN-1 depends on A20. The suppressive function of A20 in T cells relies on ubiquitin binding through the C-terminal zinc finger (ZnF)4/7 motifs, but does not involve the deubiquitinating activity of the OTU domain. Our mechanistic studies reveal that the A20/ABIN-1 module is recruited to the CBM complex via A20 ZnF4/7 and that proteasomal degradation of A20 and ABIN-1 releases the CBM complex from the negative impact of both regulators. Ubiquitin binding to A20 ZnF4/7 promotes destructive K48-polyubiquitination to itself and to ABIN-1. Further, after prolonged T cell stimulation, ABIN-1 antagonizes MALT1-catalyzed cleavage of re-synthesized A20 and thereby diminishes sustained CBM complex signaling. Taken together, interdependent post-translational mechanisms are tightly controlling expression and activity of the A20/ABIN-1 silencing module and the cooperative action of both negative regulators is critical to balance CBM complex signaling and T cell activation.

KW - B-Cell CLL-Lymphoma 10 Protein/metabolism

KW - CARD Signaling Adaptor Proteins/metabolism

KW - Cells, Cultured

KW - DNA-Binding Proteins/physiology

KW - Guanylate Cyclase/metabolism

KW - HEK293 Cells

KW - Humans

KW - Jurkat Cells

KW - Lymphocyte Activation/genetics

KW - Mucosa-Associated Lymphoid Tissue Lymphoma Translocation 1 Protein/metabolism

KW - Multiprotein Complexes/metabolism

KW - NF-kappa B/metabolism

KW - Protein Binding

KW - RNA Interference/immunology

KW - Signal Transduction/physiology

KW - T-Lymphocytes/immunology

KW - Tumor Necrosis Factor alpha-Induced Protein 3/physiology

U2 - 10.1007/s00018-022-04154-z

DO - 10.1007/s00018-022-04154-z

M3 - Journal article

C2 - 35099607

VL - 79

SP - 112

JO - Cellular and Molecular Life Sciences

JF - Cellular and Molecular Life Sciences

SN - 1420-682X

IS - 2

ER -

ID: 303114070