TREM-1 multimerization is essential for its activation on monocytes and neutrophils.


Journal

Cellular & molecular immunology
ISSN: 2042-0226
Titre abrégé: Cell Mol Immunol
Pays: China
ID NLM: 101242872

Informations de publication

Date de publication:
05 2019
Historique:
received: 31 07 2017
accepted: 09 01 2018
revised: 01 01 2018
pubmed: 24 3 2018
medline: 1 8 2020
entrez: 24 3 2018
Statut: ppublish

Résumé

The triggering receptor expressed on myeloid cells-1 (TREM-1) is a receptor expressed on innate immune cells. By promoting the amplification of inflammatory signals that are initially triggered by Toll-like receptors (TLRs), TREM-1 has been characterized as a major player in the pathophysiology of acute and chronic inflammatory diseases, such as septic shock, myocardial infarction, atherosclerosis, and inflammatory bowel diseases. However, the molecular events leading to the activation of TREM-1 in innate immune cells remain unknown. Here, we show that TREM-1 is activated by multimerization and that the levels of intracellular Ca

Identifiants

pubmed: 29568119
doi: 10.1038/s41423-018-0003-5
pii: 10.1038/s41423-018-0003-5
pmc: PMC6474208
doi:

Substances chimiques

Adaptor Proteins, Signal Transducing 0
Lipopolysaccharides 0
Membrane Proteins 0
Reactive Oxygen Species 0
TREM1 protein, human 0
TYROBP protein, human 0
Triggering Receptor Expressed on Myeloid Cells-1 0

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

460-472

Références

Bouchon, A., Dietrich, J. & Colonna, M. Cutting edge: inflammatory responses can be triggered by TREM-1, a novel receptor expressed on neutrophils and monocytes. J. Immunol. 164, 4991–4995 (2000).
doi: 10.4049/jimmunol.164.10.4991
Jolly, L. et al. Triggering receptor expressed on myeloid cells-1: a new player in platelet aggregation. Thromb. Haemost. 117, 1772–1781 (2017).
doi: 10.1160/TH17-03-0156
Derive, M., Massin, F. & Gibot, S. Triggering receptor expressed on myeloid cells-1 as a new therapeutic target during inflammatory diseases. Self Nonself 1, 225–230 (2010).
doi: 10.4161/self.1.3.12891
Tammaro, A. et al. TREM-1 and its potential ligands in non-infectious diseases: from biology to clinical perspectives. Pharmacol. Ther. 177, 81–95 (2017).
doi: 10.1016/j.pharmthera.2017.02.043
Bouchon, A., Facchetti, F., Weigand, M. A. & Colonna, M. TREM-1 amplifies inflammation and is a crucial mediator of septic shock. Nature 410, 1103–1107 (2001).
doi: 10.1038/35074114
Boufenzer, A. et al. TREM-1 mediates inflammatory injury and cardiac remodeling following myocardial infarction. Circ. Res 116, 1772–1782 (2015).
doi: 10.1161/CIRCRESAHA.116.305628
Zysset, D. et al. TREM-1 links dyslipidemia to inflammation and lipid deposition in atherosclerosis. Nat. Commun. 7, 13151 (2016).
doi: 10.1038/ncomms13151
Joffre, J. et al. Genetic and pharmacological inhibition of TREM-1 limits the development of experimental atherosclerosis. J. Am. Coll. Cardiol. 68, 2776–2793 (2016).
doi: 10.1016/j.jacc.2016.10.015
Tessarz, A. S. & Cerwenka, A. The TREM-1/DAP12 pathway. Immunol. Lett. 116, 111–116 (2008).
doi: 10.1016/j.imlet.2007.11.021
Ormsby, T. et al. Btk is a positive regulator in the TREM-1/DAP12 signaling pathway. Blood 118, 936–945 (2011).
doi: 10.1182/blood-2010-11-317016
McVicar, D. W. et al. DAP12-mediated signal transduction in natural killer cells. A dominant role for the Syk protein-tyrosine kinase. J. Biol. Chem. 273, 32934–32942 (1998).
doi: 10.1074/jbc.273.49.32934
Radsak, M. P., Salih, H. R., Rammensee, H.-G. & Schild, H. Triggering receptor expressed on myeloid cells-1 in neutrophil inflammatory responses: differential regulation of activation and survival. J. Immunol. 172, 4956–4963 (2004).
doi: 10.4049/jimmunol.172.8.4956
Klesney-Tait, J. & Colonna, M. Uncovering the TREM-1-TLR connection. Am. J. Physiol. Lung Cell Mol. Physiol. 293, L1374–L1376 (2007).
doi: 10.1152/ajplung.00415.2007
Gibot, S. Clinical review: Role of triggering receptor expressed on myeloid cells-1 during sepsis. Crit. Care 9, 485 (2005).
doi: 10.1186/cc3732
Knapp, S. et al. Cutting edge: expression patterns of surface and soluble triggering receptor expressed on myeloid cells-1 in human endotoxemia. J. Immunol. 173, 7131–7134 (2004).
doi: 10.4049/jimmunol.173.12.7131
Fortin, C. F., Lesur, O. & Fulop, T. Effects of TREM-1 activation in human neutrophils: activation of signaling pathways, recruitment into lipid rafts and association with TLR4. Int. Immunol. 19, 41–50 (2007).
doi: 10.1093/intimm/dxl119
Ornatowska, M. et al. Functional genomics of silencing TREM-1 on TLR4 signaling in macrophages. Am. J. Physiol. Lung Cell Mol. Physiol. 293, L1377–L1384 (2007).
doi: 10.1152/ajplung.00140.2007
Derive, M. et al. Soluble TREM-like transcript-1 regulates leukocyte activation and controls microbial sepsis. J. Immunol. 188, 5585–5592 (2012).
doi: 10.4049/jimmunol.1102674
Derive, M., Boufenzer, A. & Gibot, S. Attenuation of responses to endotoxin by the triggering receptor expressed on myeloid cells-1 inhibitor LR12 in nonhuman primate. J. Am. Soc. Anesthesiol. 120, 935–942 (2014).
doi: 10.1097/ALN.0000000000000078
Derive, M. et al. Effects of a TREM-like transcript 1-derived peptide during hypodynamic septic shock in pigs. Shock 39, 176–182 (2013).
doi: 10.1097/SHK.0b013e31827bcdfb
Tessarz, A. S. et al. Non-T cell activation linker (NTAL) negatively regulates TREM-1/DAP12-induced inflammatory cytokine production in myeloid cells. J. Immunol. 178, 1991–1999 (2007).
doi: 10.4049/jimmunol.178.4.1991
Lee, B. et al. 1α,25-Dihydroxyvitamin D3 upregulates HIF-1 and TREM-1 via mTOR signaling. Immunol. Lett. 163, 14–21 (2015).
doi: 10.1016/j.imlet.2014.11.004
Wenzel, J. et al. Measurement of TLR-induced macrophage spreading by automated image analysis: differential role of Myd88 and MAPK in early and late responses. Front. Physiol. 2, 71 (2011).
doi: 10.3389/fphys.2011.00071
Leuchowius, K.-J., & Weibrecht, I. & Söderberg, O. In situ proximity ligation assay for microscopy and flow cytometry. Curr. Protoc. Cytom. Chapter 9, Unit 9.36 (2011).
pubmed: 21455970
Kelker, M. S. et al. Crystal structure of human triggering receptor expressed on myeloid cells 1 (TREM-1) at 1.47 A. J. Mol. Biol. 342, 1237–1248 (2004).
doi: 10.1016/j.jmb.2004.07.089
Radaev, S., Kattah, M., Rostro, B., Colonna, M. & Sun, P. D. Crystal structure of the human myeloid cell activating receptor TREM-1. Structure 11, 1527–1535 (2003).
doi: 10.1016/j.str.2003.11.001
van den Heuvel, R. H. H. et al. Improving the performance of a quadrupole time-of-flight instrument for macromolecular mass spectrometry. Anal. Chem. 78, 7473–7483 (2006).
doi: 10.1021/ac061039a
Snijder, J. & Heck, A. J. R. Analytical approaches for size and mass analysis of large protein assemblies. Annu Rev. Anal. Chem. Palo Alto Calif. 7, 43–64 (2014).
doi: 10.1146/annurev-anchem-071213-020015
Wang, G. et al. Molecular basis of assembly and activation of complement component C1 in complex with immunoglobulin G1 and antigen. Mol. Cell 63, 135–145 (2016).
doi: 10.1016/j.molcel.2016.05.016
Wang, G., Johnson, A. J. & Kaltashov, I. A. Evaluation of electrospray ionization mass spectrometry as a tool for characterization of small soluble protein aggregates. Anal. Chem. 84, 1718–1724 (2012).
doi: 10.1021/ac203017x
Read, C. B. et al. Cutting Edge: identification of neutrophil PGLYRP1 as a ligand for TREM-1. J. Immunol. 194, 1417–1421 (2015).
doi: 10.4049/jimmunol.1402303
Barranco-Medina, S., Kakorin, S., Lázaro, J. J. & Dietz, K.-J. Thermodynamics of the dimer-decamer transition of reduced human and plant 2-cys peroxiredoxin. Biochemistry 47, 7196–7204 (2008).
doi: 10.1021/bi8002956
Burrows, S. D. et al. Determination of the monomer-dimer equilibrium of interleukin-8 reveals it is a monomer at physiological concentrations. Biochemistry 33, 12741–12745 (1994).
doi: 10.1021/bi00209a002
Luke, K., Apiyo, D. & Wittung-Stafshede, P. Dissecting homo-heptamer thermodynamics by isothermal titration calorimetry: entropy-driven assembly of co-chaperonin protein 10. Biophys. J. 89, 3332–3336 (2005).
doi: 10.1529/biophysj.105.067223
Nazabal, A., Wenzel, R. J. & Zenobi, R. Immunoassays with direct mass spectrometric detection. Anal. Chem. 78, 3562–3570 (2006).
doi: 10.1021/ac0519108
Bich, C. et al. Characterization of antibody-antigen interactions: comparison between surface plasmon resonance measurements and high-mass matrix-assisted laser desorption/ionization mass spectrometry. Anal. Biochem. 375, 35–45 (2008).
doi: 10.1016/j.ab.2007.11.016
Prüfer, S. et al. Distinct signaling cascades of TREM-1, TLR and NLR in neutrophils and monocytic cells. J. Innate Immun. 6, 339–352 (2014).
doi: 10.1159/000355892
Kolaczkowska, E. & Kubes, P. Neutrophil recruitment and function in health and inflammation. Nat. Rev. Immunol. 13, 159–175 (2013).
doi: 10.1038/nri3399
McDonald, B. et al. Intravascular danger signals guide neutrophils to sites of sterile inflammation. Science 330, 362–366 (2010).
doi: 10.1126/science.1195491
Libby, P., Nahrendorf, M. & Swirski, F. K. Leukocytes link local and systemic inflammation in ischemic cardiovascular disease: an expanded ‘cardiovascular continuum’. J. Am. Coll. Cardiol. 67, 1091–1103 (2016).
doi: 10.1016/j.jacc.2015.12.048
Goodsell, D. S. & Olson, A. J. Structural symmetry and protein function. Annu. Rev. Biophys. Biomol. Struct. 29, 105–153 (2000).
doi: 10.1146/annurev.biophys.29.1.105
Goodsell, D. S. Inside a living cell. Trends Biochem. Sci. 16, 203–206 (1991).
doi: 10.1016/0968-0004(91)90083-8
Mulrooney, T. J., Posch, P. E. & Hurley, C. K. DAP12 impacts trafficking and surface stability of killer immunoglobulin-like receptors on natural killer cells. J. Leukoc. Biol. 94, 301–313 (2013).
doi: 10.1189/jlb.0213093

Auteurs

Kevin Carrasco (K)

INOTREM, Vandœuvre-les-Nancy, France.
UMR-S 1116, Defaillance cardiovasculaire aigue et chronique, Vandœuvre-les-Nancy, France.

Amir Boufenzer (A)

INOTREM, Vandœuvre-les-Nancy, France.

Lucie Jolly (L)

INOTREM, Vandœuvre-les-Nancy, France.
UMR-S 1116, Defaillance cardiovasculaire aigue et chronique, Vandœuvre-les-Nancy, France.

Helene Le Cordier (H)

UMR7365, Ingénierie Moléculaire et Physiopathologie Articulaire (IMoPA), CNRS-Université de Lorraine, Vandœuvre-les-Nancy, France.

Guanbo Wang (G)

Biomolecular Mass Spectrometry and Proteomics, Bijvoet Center for Biomolecular Research and Utrecht Institute for Pharmaceutical Sciences and Netherlands Proteomics Center, Utrecht University, Utrecht, The Netherlands.

Albert Jr Heck (AJ)

Biomolecular Mass Spectrometry and Proteomics, Bijvoet Center for Biomolecular Research and Utrecht Institute for Pharmaceutical Sciences and Netherlands Proteomics Center, Utrecht University, Utrecht, The Netherlands.

Adelheid Cerwenka (A)

Innate Immunity, German Cancer Research Center (DKFZ), Heidelberg, Germany.

Emilie Vinolo (E)

INOTREM, Vandœuvre-les-Nancy, France.

Alexis Nazabal (A)

CovalX, Zurich, Switzerland.

Alexandre Kriznik (A)

Service Commun de Biophysique Interactions Moléculaires (SCBIM), FR3209, Biopôle de l'Université de Lorraine, Vandœuvre-les-Nancy, France.

Pierre Launay (P)

Inatherys, Evry Cedex, France.

Sebastien Gibot (S)

UMR-S 1116, Defaillance cardiovasculaire aigue et chronique, Vandœuvre-les-Nancy, France.

Marc Derive (M)

INOTREM, Vandœuvre-les-Nancy, France. md@inotrem.com.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH