Mapping the SLP76 interactome in T cells lacking each of the GRB2-family adaptors reveals molecular plasticity of the TCR signaling pathway.


Journal

Frontiers in immunology
ISSN: 1664-3224
Titre abrégé: Front Immunol
Pays: Switzerland
ID NLM: 101560960

Informations de publication

Date de publication:
2023
Historique:
received: 06 01 2023
accepted: 02 03 2023
medline: 4 4 2023
entrez: 3 4 2023
pubmed: 4 4 2023
Statut: epublish

Résumé

The propagation and diversification of signals downstream of the T cell receptor (TCR) involve several adaptor proteins that control the assembly of multimolecular signaling complexes (signalosomes). The global characterization of changes in protein-protein interactions (PPI) following genetic perturbations is critical to understand the resulting phenotypes. Here, by combining genome editing techniques in T cells and interactomics studies based on affinity purification coupled to mass spectrometry (AP-MS) analysis, we determined and quantified the molecular reorganization of the SLP76 interactome resulting from the ablation of each of the three GRB2-family adaptors. Our data showed that the absence of GADS or GRB2 induces a major remodeling of the PPI network associated with SLP76 following TCR engagement. Unexpectedly, this PPI network rewiring minimally affects proximal molecular events of the TCR signaling pathway. Nevertheless, during prolonged TCR stimulation, GRB2- and GADS-deficient cells displayed a reduced level of activation and cytokine secretion capacity. Using the canonical SLP76 signalosome, this analysis highlights the plasticity of PPI networks and their reorganization following specific genetic perturbations.

Identifiants

pubmed: 37006259
doi: 10.3389/fimmu.2023.1139123
pmc: PMC10057548
doi:

Substances chimiques

Receptors, Antigen, T-Cell 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1139123

Informations de copyright

Copyright © 2023 Ruminski, Celis-Gutierrez, Jarmuzynski, Maturin, Audebert, Malissen, Camoin, Voisinne, Malissen and Roncagalli.

Déclaration de conflit d'intérêts

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Références

J Cell Sci. 2018 Nov 8;131(21):
pubmed: 30305305
Mol Cell Biol. 2002 May;22(10):3230-6
pubmed: 11971956
J Biol Chem. 1994 Mar 25;269(12):9019-23
pubmed: 7510700
Cell Signal. 2015 Apr;27(4):841-50
pubmed: 25636200
Nat Struct Mol Biol. 2006 Sep;13(9):798-805
pubmed: 16906159
Science. 1998 Jul 17;281(5375):413-6
pubmed: 9665884
EMBO Rep. 2012 Apr;13(4):386-91
pubmed: 22344067
J Exp Med. 2004 Feb 2;199(3):429-34
pubmed: 14757747
Immunity. 1999 Mar;10(3):323-32
pubmed: 10204488
Science. 2001 Mar 9;291(5510):1987-91
pubmed: 11239162
Mol Cell Biol. 2000 Sep;20(18):6945-57
pubmed: 10958690
Proc Natl Acad Sci U S A. 2010 Jun 8;107(23):10620-5
pubmed: 20498059
Nat Immunol. 2019 Nov;20(11):1542-1554
pubmed: 31591570
EMBO J. 2007 Feb 7;26(3):678-89
pubmed: 17235283
Proc Natl Acad Sci U S A. 2007 Apr 17;104(16):6638-43
pubmed: 17420479
Nature. 2000 Mar 23;404(6776):402-7
pubmed: 10746729
J Biol Chem. 1997 Jan 10;272(2):894-902
pubmed: 8995379
Mol Cell Biol. 2006 Sep;26(17):6727-38
pubmed: 16914752
J Immunol. 2021 May 15;206(10):2322-2337
pubmed: 33931484
Cold Spring Harb Perspect Biol. 2010 Apr;2(4):a002501
pubmed: 20452948
Mol Cell Biol. 2017 May 16;37(11):
pubmed: 28289074
Proc Natl Acad Sci U S A. 1999 Mar 16;96(6):3035-40
pubmed: 10077632
Nat Immunol. 2019 Nov;20(11):1530-1541
pubmed: 31591574
Nat Immunol. 2014 Apr;15(4):384-392
pubmed: 24584089
Nat Rev Immunol. 2018 Aug;18(8):485-497
pubmed: 29789755
Nat Immunol. 2001 Apr;2(4):325-32
pubmed: 11276203
Science. 2016 Apr 29;352(6285):595-9
pubmed: 27056844
Curr Biol. 1998 May 7;8(10):554-62
pubmed: 9601639
Eur J Immunol. 2015 Aug;45(8):2389-95
pubmed: 25973715
Front Immunol. 2019 Jul 25;10:1704
pubmed: 31402911
Cell Rep. 2019 Jun 11;27(11):3315-3330.e7
pubmed: 31189114
J Immunol. 2006 Jul 15;177(2):1152-9
pubmed: 16818773
Curr Biol. 2002 Aug 6;12(15):1336-41
pubmed: 12176364
Eur J Immunol. 2004 Apr;34(4):930-40
pubmed: 15048703
Mol Cell Biol. 2007 Apr;27(7):2732-45
pubmed: 17283063
Sci Signal. 2017 Sep 26;10(498):
pubmed: 28951535
EMBO J. 2011 Jul 01;30(15):3160-72
pubmed: 21725281
Cell Signal. 2015 Jan;27(1):125-34
pubmed: 25452106
Front Immunol. 2012 Jul 11;3:197
pubmed: 22798961
J Biol Chem. 2005 Apr 15;280(15):15289-99
pubmed: 15708849
Nat Rev Immunol. 2004 Aug;4(8):603-16
pubmed: 15286727
Front Immunol. 2018 Dec 18;9:2994
pubmed: 30619347
J Immunol. 2001 Mar 15;166(6):3797-803
pubmed: 11238622
Trends Immunol. 2001 Sep;22(9):490-6
pubmed: 11525939
J Biol Chem. 2007 Feb 2;282(5):2937-46
pubmed: 17148460
J Exp Med. 2021 Feb 1;218(2):
pubmed: 33125054
Cold Spring Harb Perspect Biol. 2010 Aug;2(8):a005512
pubmed: 20610546
Mol Cell Biol. 2013 Nov;33(21):4140-51
pubmed: 23979596
J Immunol. 2004 Aug 1;173(3):1711-20
pubmed: 15265900
Nat Struct Mol Biol. 2016 Jun;23(6):608-18
pubmed: 27136326
Cell Rep. 2017 Mar 28;18(13):3219-3226
pubmed: 28355572

Auteurs

Kilian Ruminski (K)

Centre d'Immunologie de Marseille-Luminy, Aix Marseille Université, INSERM, CNRS, Marseille, France.

Javier Celis-Gutierrez (J)

Centre d'Immunologie de Marseille-Luminy, Aix Marseille Université, INSERM, CNRS, Marseille, France.
Centre d'Immunophénomique, Aix Marseille Université, INSERM, CNRS UMR, Marseille, France.

Nicolas Jarmuzynski (N)

Centre d'Immunologie de Marseille-Luminy, Aix Marseille Université, INSERM, CNRS, Marseille, France.
Centre d'Immunophénomique, Aix Marseille Université, INSERM, CNRS UMR, Marseille, France.

Emilie Maturin (E)

Centre d'Immunologie de Marseille-Luminy, Aix Marseille Université, INSERM, CNRS, Marseille, France.

Stephane Audebert (S)

Institut Paoli-Calmettes, CRCM, Aix Marseille Université, CNRS, INSERM, Marseille Protóomique, Marseille, France.

Marie Malissen (M)

Centre d'Immunologie de Marseille-Luminy, Aix Marseille Université, INSERM, CNRS, Marseille, France.
Centre d'Immunophénomique, Aix Marseille Université, INSERM, CNRS UMR, Marseille, France.

Luc Camoin (L)

Institut Paoli-Calmettes, CRCM, Aix Marseille Université, CNRS, INSERM, Marseille Protóomique, Marseille, France.

Guillaume Voisinne (G)

Centre d'Immunologie de Marseille-Luminy, Aix Marseille Université, INSERM, CNRS, Marseille, France.

Bernard Malissen (B)

Centre d'Immunologie de Marseille-Luminy, Aix Marseille Université, INSERM, CNRS, Marseille, France.
Centre d'Immunophénomique, Aix Marseille Université, INSERM, CNRS UMR, Marseille, France.

Romain Roncagalli (R)

Centre d'Immunologie de Marseille-Luminy, Aix Marseille Université, INSERM, CNRS, Marseille, France.

Articles similaires

Humans Receptors, Antigen, T-Cell Proto-Oncogene Proteins p21(ras) Pancreatic Neoplasms T-Lymphocytes

The FGF/FGFR/c-Myc axis as a promising therapeutic target in multiple myeloma.

Arianna Giacomini, Sara Taranto, Giorgia Gazzaroli et al.
1.00
Humans Multiple Myeloma Receptors, Fibroblast Growth Factor Fibroblast Growth Factors Proto-Oncogene Proteins c-myc
Humans Colorectal Neoplasms Biomarkers, Tumor Prognosis Gene Expression Regulation, Neoplastic
Animals Lung India Sheep Transcriptome

Classifications MeSH