Integrative biology of T cell activation

Bernard Malissen ¹, Claude Grégoire ², Marie Malissen ¹, Romain Roncagalli ²

Affiliations

¹ 1] Centre d'Immunologie de Marseille-Luminy, UM2 Aix-Marseille Université, Marseille, France. [2] INSERM U1104, Marseille, France. [3] CNRS UMR7280, Marseille, France. [4] Centre d'Immunophénomique, UM2 Aix-Marseille Université, Marseille, France. [5] INSERM US012, Marseille, France. [6] CNRS UMS3367, Marseille, France.
² 1] Centre d'Immunologie de Marseille-Luminy, UM2 Aix-Marseille Université, Marseille, France. [2] INSERM U1104, Marseille, France. [3] CNRS UMR7280, Marseille, France.

PMID: 25137453
103 References
48 citations

Abstract

The activation of T cells mediated by the T cell antigen receptor (TCR) requires the interaction of dozens of proteins, and its malfunction has pathological consequences. Our major focus is on new developments in the systems-level understanding of the TCR signal-transduction network. To make sense of the formidable complexity of this network, we argue that 'fine-grained' methods are needed to assess the relationships among a few components that interact on a nanometric scale, and those should be integrated with high-throughput '-omic' approaches that simultaneously capture large numbers of parameters. We illustrate the utility of this integrative approach with the transmembrane signaling protein Lat, which is a key signaling hub of the TCR signal-transduction network, as a connecting thread.

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References
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Role of Vanadium in Cellular and Molecular Immunology: Association with Immune-Related Inflammation and Pharmacotoxicology Mechanisms. Olga Tsave, Savvas Petanidis, +5 authors, Athanasios Salifoglou. less Oxid Med Cell Longev, 2016 May 18; 2016. PMID: 27190573 Free PMC article. Review.
Inhibition of T cell receptor signaling by cholesterol sulfate, a naturally occurring derivative of membrane cholesterol. Feng Wang, Katharina Beck-García, +2 authors, Carina Zorzin, Wolfgang W A Schamel, Mark M Davis. less Nat Immunol, 2016 May 24; 17(7). PMID: 27213689 Free PMC article.
Protein tyrosine phosphatase SHP-1: resurgence as new drug target for human autoimmune disorders. Yadhu Sharma, Samina Bashir, +2 authors, Puja Bhardwaj, Altaf Ahmad, Farah Khan. less Immunol Res, 2016 May 25; 64(4). PMID: 27216862 Review.
Early onset combined immunodeficiency and autoimmunity in patients with loss-of-function mutation in LAT. Baerbel Keller, Irina Zaidman, +11 authors, Polina Stepensky. less J Exp Med, 2016 Jun 01; 213(7). PMID: 27242165 Free PMC article.
What Happens in the Thymus Does Not Stay in the Thymus: How T Cells Recycle the CD4+-CD8+ Lineage Commitment Transcriptional Circuitry To Control Their Function. Melanie S Vacchio, Rémy Bosselut. J Immunol, 2016 Jun 05; 196(12). PMID: 27260768 Free PMC article. Review.
Time-Course Study of the Transcriptome of Peripheral Blood Mononuclear Cells (PBMCs) from Sheep Infected with Fasciola hepatica. Cristian A Alvarez Rojas, Jean-Pierre Scheerlinck, +3 authors, Aaron R Jex. less PLoS One, 2016 Jul 22; 11(7). PMID: 27438474 Free PMC article.
New Insights into How Trafficking Regulates T Cell Receptor Signaling. Jieqiong Lou, Jérémie Rossy, +2 authors, Qiji Deng, Sophie V Pageon, Katharina Gaus. less Front Cell Dev Biol, 2016 Aug 11; 4. PMID: 27508206 Free PMC article. Review.
The scaffolding function of the RLTPR protein explains its essential role for CD28 co-stimulation in mouse and human T cells. Romain Roncagalli, Margot Cucchetti, +14 authors, Bernard Malissen. less J Exp Med, 2016 Nov 05; 213(11). PMID: 27647348 Free PMC article.
GTPase of the Immune-Associated Nucleotide Protein 5 Regulates the Lysosomal Calcium Compartment in T Lymphocytes. Daniel Serrano, Farnaz Ghobadi, +3 authors, Sheela Ramanathan. less Front Immunol, 2017 Feb 23; 8. PMID: 28223986 Free PMC article.
Tespa1 regulates T cell receptor-induced calcium signals by recruiting inositol 1,4,5-trisphosphate receptors. Jingjing Liang, Jun Lyu, +10 authors, Linrong Lu. less Nat Commun, 2017 Jun 10; 8. PMID: 28598420 Free PMC article.
Proteomics and Network Analyses Reveal Inhibition of Akt-mTOR Signaling in CD4+ T Cells by Mycobacterium tuberculosis Mannose-Capped Lipoarabinomannan. Ahmad F Karim, Obondo J Sande, +8 authors, W Henry Boom. less Proteomics, 2017 Oct 11; 17(22). PMID: 28994205 Free PMC article.
SYK expression in monomorphic epitheliotropic intestinal T-cell lymphoma. Grit Mutzbauer, Katja Maurus, +5 authors, Eva Geissinger. less Mod Pathol, 2017 Oct 21; 31(3). PMID: 29052597
Multifaceted Role of Neuropilins in the Immune System: Potential Targets for Immunotherapy. Sohini Roy, Arup K Bag, +3 authors, Kaustubh Datta. less Front Immunol, 2017 Oct 27; 8. PMID: 29067024 Free PMC article. Review.
T Cells Expressing Checkpoint Receptor TIGIT Are Enriched in Follicular Lymphoma Tumors and Characterized by Reversible Suppression of T-cell Receptor Signaling. Sarah E Josefsson, Kanutte Huse, +10 authors, June H Myklebust. less Clin Cancer Res, 2017 Dec 09; 24(4). PMID: 29217528 Free PMC article.
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New Chimeric Antigen Receptor Design for Solid Tumors. Yuedi Wang, Feifei Luo, +2 authors, Jiao Yang, Chujun Zhao, Yiwei Chu. less Front Immunol, 2018 Jan 10; 8. PMID: 29312360 Free PMC article. Review.
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mDia1/3-dependent actin polymerization spatiotemporally controls LAT phosphorylation by Zap70 at the immune synapse. D Thumkeo, Y Katsura, +9 authors, S Narumiya. less Sci Adv, 2020 Jan 09; 6(1). PMID: 31911947 Free PMC article.
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Synthetic TRuC receptors engaging the complete T cell receptor for potent anti-tumor response. Patrick A Baeuerle, Jian Ding, +18 authors, Robert Hofmeister. less Nat Commun, 2019 May 09; 10(1). PMID: 31064990 Free PMC article.
T Cell Receptor (TCR)-Induced PLC-γ1 Sumoylation via PIASxβ and PIAS3 SUMO E3 Ligases Regulates the Microcluster Assembly and Physiological Function of PLC-γ1. Qi-Long Wang, Jia-Qi Liang, +4 authors, Yingqiu Li. less Front Immunol, 2019 Mar 16; 10. PMID: 30873169 Free PMC article.
Harnessing regulatory T cell neuroprotective activities for treatment of neurodegenerative disorders. Jatin Machhi, Bhavesh D Kevadiya, +4 authors, Howard E Gendelman. less Mol Neurodegener, 2020 Jun 07; 15(1). PMID: 32503641 Free PMC article. Review.
Alternative ZAP70-p38 signals prime a classical p38 pathway through LAT and SOS to support regulatory T cell differentiation. Jesse E Jun, Kayla R Kulhanek, +2 authors, Hang Chen, Arup Chakraborty, Jeroen P Roose. less Sci Signal, 2019 Jul 25; 12(591). PMID: 31337738 Free PMC article.
Manipulation of Regulatory Dendritic Cells for Induction Transplantation Tolerance. Weitao Que, Wen-Zhi Guo, Xiao-Kang Li. Front Immunol, 2020 Nov 10; 11. PMID: 33162996 Free PMC article. Review.
The T cell CD6 receptor operates a multitask signalosome with opposite functions in T cell activation. Daiki Mori, Claude Grégoire, +12 authors, Bernard Malissen. less J Exp Med, 2020 Oct 31; 218(2). PMID: 33125054 Free PMC article.
Naturally Occurring Genetic Alterations in Proximal TCR Signaling and Implications for Cancer Immunotherapy. Andrew Kent, Natalie V Longino, Allison Christians, Eduardo Davila. Front Immunol, 2021 May 21; 12. PMID: 34012443 Free PMC article. Review.
The GIMAP Family Proteins: An Incomplete Puzzle. Marc-André Limoges, Maryse Cloutier, +2 authors, Sheela Ramanathan. less Front Immunol, 2021 Jun 18; 12. PMID: 34135906 Free PMC article. Review.
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The Clinical Aspect of Adaptor Molecules in T Cell Signaling: Lessons Learnt From Inborn Errors of Immunity. Yael Dinur-Schejter, Irina Zaidman, Hagar Mor-Shaked, Polina Stepensky. Front Immunol, 2021 Aug 31; 12. PMID: 34456914 Free PMC article. Review.
T cells at work: How post-transcriptional mechanisms control T cell homeostasis and activation. Anouk P Jurgens, Branka Popović, Monika C Wolkers. Eur J Immunol, 2021 Jun 29; 51(9). PMID: 34180545 Free PMC article. Review.
Systems-level conservation of the proximal TCR signaling network of mice and humans. Philippe Nicolas, Jocelyn Ollier, +12 authors, Bernard Malissen. less J Exp Med, 2022 Jan 22; 219(2). PMID: 35061003 Free PMC article.
Reprogramming and redifferentiation of mucosal-associated invariant T cells reveal tumor inhibitory activity. Chie Sugimoto, Yukie Murakami, +2 authors, Eisuke Ishii, Hiroyoshi Fujita, Hiroshi Wakao. less Elife, 2022 Apr 06; 11. PMID: 35379387 Free PMC article.

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