Cited by 1,284Inflammation biomarkers and pathwaysImmune Response and InflammationNeutrophil, Myeloperoxidase and Oxidative Mechanisms

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Cutting Edge: Inflammatory Responses Can Be Triggered by TREM-1, a Novel Receptor Expressed on Neutrophils and Monocytes

Bouchon, Axel, Dietrich, Jes, Colonna, Marco·2000·The Journal of Immunology

DOI 10.4049/jimmunol.164.10.4991

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Abstract

We have identified new activating receptors of the Ig superfamily expressed on human myeloid cells, called TREM (triggering receptor expressed on myeloid cells). TREM-1 is selectively expressed on blood neutrophils and a subset of monocytes and is up-regulated by bacterial LPS. Engagement of TREM-1 triggers secretion of IL-8, monocyte chemotactic protein-1, and TNF-alpha and induces neutrophil degranulation. Intracellularly, TREM-1 induces Ca2+ mobilization and tyrosine phosphorylation of extracellular signal-related kinase 1 (ERK1), ERK2 and phospholipase C-gamma. To mediate activation, TREM-1 associates with the transmembrane adapter molecule DAP12. Thus, TREM-1 mediates activation of neutrophil and monocytes, and may have a predominant role in inflammatory responses.

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Background
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Background
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“TREM-1 has a role as a regulator of innate and adaptive immunity [30,31].”
Background
TREM2 brain transcript-specific studies in AD and TREM2 mutation carriers
Del‐Aguila, J. L., Benítez, B. A., Li, Z., Dube, U., Mihindukulasuriya, K. A., Budde, J., Farias, F., Fernández, M. V., Ibáñez, L., Jiang, S., et al. (2019) · Molecular Neurodegeneration · doi:10.1186/s13024-019-0319-3 · Cited by 106
“Introduction The Triggering Receptor Expressed in Myeloid cells 2 (TREM2) is a type 1 transmembrane receptor protein expressed on myeloid cells including microglia, monocyte-derived dendritic cells, osteoclasts and bone-marrow derived macrophages [1, 2].”
Background
Modulation of Angiogenic and Inflammatory Response in Glioblastoma by Hypoxia
Murat, A., Migliavacca, E., Hussain, S. F., Heimberger, A. B., Desbaillets, I., Hamou, M., Rüegg, C., Stupp, R., Delorenzi, M., & Hegi, M. E. (2009) · PLoS ONE · doi:10.1371/journal.pone.0005947 · Cited by 108
“Once recruited, tumor-educated macrophages take on non-immunological functions, in particular the production of factors that promote progression of tumors to a more malignant state through paracrine cues, including angiogenic factors (VEGF, TNF-a, ANG1), proteases (MMPs), growth factors (FGF, PDGF, TGF-b), and motilit…”
Background
Paired Activating and Inhibitory Immunoglobulin-like Receptors, MAIR-I and MAIR-II, Regulate Mast Cell and Macrophage Activation
Yotsumoto, K., Okoshi, Y., Shibuya, K., et al. (2003) · The Journal of Experimental Medicine · doi:10.1084/jem.20021825 · Cited by 108
Genetic and Pharmacological Inhibition of TREM-1 Limits the Development of Experimental Atherosclerosis
Joffre, J., Potteaux, S., Zeboudj, L., Loyer, X., Boufenzer, A., Laurans, L., Esposito, B., Vandestienne, M., de Jager, S. C. A., Hénique, C., et al. (2016) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2016.10.015 · Cited by 117
“Data are expressed as median and percentiles (5-95).”
BackgroundInfluential
Activation of Triggering Receptor Expressed on Myeloid Cells-1 on Human Neutrophils by Marburg and Ebola Viruses
Mohamadzadeh, M., Coberley, S. S., Olinger, G. G., Kalina, W. V., Ruthel, G. T., Fuller, C. L., Swenson, D. L., Pratt, W. D., Kuhns, D. B., & Schmaljohn, A. L. (2006) · Journal of Virology · doi:10.1128/jvi.00543-06 · Cited by 107
“Activation of DAP12-coupled receptors results in transient tyrosine phosphorylation of ITAM chains, recruits and promotes activation of the tyrosine kinase Syk, and subsequently leads to activation of extracellular signal-regulated kinases 1/2 (ERK1/2) (33), resulting in the secretion of primary neutrophil cytokines a…”
BackgroundInfluential
Triggering receptor expressed on myeloid cells-1 (TREM-1): a new player in antiviral immunity?
Roe, K., Gibot, S., & Verma, S. (2014) · Frontiers in Microbiology · doi:10.3389/fmicb.2014.00627 · Cited by 107
“Activation of TREM-1 signaling is initiated upon binding of the ligand to the receptor, which triggers the association and phosphorylation of immunoreceptor tyrosine-based activation motif of the adaptor protein DAP12.”
BackgroundInfluential
Triptolide Modulates TREM-1 Signal Pathway to Inhibit the Inflammatory Response in Rheumatoid Arthritis
Fan, D., He, X., Bian, Y., Guo, Q., Zheng, K., Zhao, Y., Lu, C. C., Liu, B.-Q., Xu, X., Zhang, G., et al. (2016) · International Journal of Molecular Sciences · doi:10.3390/ijms17040498 · Cited by 107
“Although the natural ligand of TREM-1 is unknown, activation of TREM-1 using an agonistic antibody leads to activation of a cascade of intracellular events which result in inflammatory effects, such as neutrophils degranulation, phagocytosis, and the proinflammatory chemokines production including monocyte chemoattrac…”
Background
The Pathogenesis of Glaucoma in the Interplay with the Immune System
Rieck, J. (2013) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.12-9781 · Cited by 104
Structure, expression pattern and biological activity of molecular complex TREM-2/DAP12
Paradowska-Gorycka, A., & Jurkowska, M. (2013) · Human Immunology · doi:10.1016/j.humimm.2013.02.003 · Cited by 103
“The cytoplasmic tail of TREM-2 lacks signaling motifs; therefore a separate signal transduction subunit is required to mediate TREM-2 activating signals [30,31,33].”
Background
The innate immune receptor TREM-1 promotes liver injury and fibrosis
Nguyen-Lefebvre, A. T., Ajith, A., Portik-Dobos, V., Horuzsko, D. D., Arbab, A. S., Dzutsev, A., Sadek, R., Trinchieri, G., & Horuzsko, A. (2018) · Journal of Clinical Investigation · doi:10.1172/jci98156 · Cited by 104
“TREM-1 is expressed on neutrophils, monocytes, and macrophages, where it is upregulated during infection, cancer development, and following TLR engagement (16, 17).”
Influential
Developmental Regulation of TREM2 and DAP12 Expression in the Murine CNS: Implications for Nasu-Hakola Disease
Thrash, J. C., Torbett, B. E., & Carson, M. J. (2008) · Neurochemical Research · doi:10.1007/s11064-008-9657-1 · Cited by 103
Identification of genes preferentially expressed by microglia and upregulated during cuprizone‐induced inflammation
Bédard, A., Tremblay, P., Chernomoretz, A., & Vallières, L. (2007) · Glia · doi:10.1002/glia.20477 · Cited by 103
“, 2005), was strongly expressed in these cells, but not in the other types examined, as anticipated from previous studies (Bouchon et al., 2000; Schmid et al., 2002).”
ResultInfluential
Elevated synovial expression of triggering receptor expressed on myeloid cells 1 in patients with septic arthritis or rheumatoid arthritis
Collins, C. E., La, D. T., Yang, H.-T., et al. (2008) · Annals of the Rheumatic Diseases · doi:10.1136/ard.2008.089557 · Cited by 101
“Whereas crosslinking of TREM-1 alone induces modest cellular activation and proinflammatory cytokine secretion, TREM-1 acts synergistically with receptors for pathogenassociated molecular patterns (PAMPs) [3-5, 7].”
BackgroundResultInfluential
Immunoreceptors on neutrophils
van Rees, D. J., Szilagyi, K., Kuijpers, T. W., Matlung, H. L., & van den Berg, T. K. (2016) · Seminars in Immunology · doi:10.1016/j.smim.2016.02.004 · Cited by 100
“Additionally, human and mice also express TREM-like transcripts (TLT)-1 and -2 [145, 146] , but only TREM-1 and TLT-2 are expressed on neutrophils [147, 148] .”
Background
Advanced Role of Neutrophils in Common Respiratory Diseases
Liu, J., Pang, Z., Wang, G., Guan, X., Fang, K., Wang, Z., & Wang, F. (2017) · Journal of Immunology Research · doi:10.1155/2017/6710278 · Cited by 109
“Triggering receptor expressed on myeloid cells-1 (TREM-1) is a receptor on phagocytes known to amplify TLR- and NOD-like receptor inflammatory signaling [136, 137].”
Background
Clinical review: role of triggering receptor expressed on myeloid cells-1 during sepsis.
Gibot, S. (2005) · Critical Care · doi:10.1186/cc3732 · Cited by 101
“TREM-1 as an amplifier of the inflammatory response TREM-1 is expressed by neutrophils, macrophages and mature monocytes [5].”
BackgroundInfluential
Aminophospholipids are signal-transducing TREM2 ligands on apoptotic cells
Shirotani, K., Hori, Y., Yoshizaki, R., Higuchi, E., Colonna, M., Saito, T., Hashimoto, S., Saito, T., Saido, T. C., & Iwata, N. (2019) · Scientific Reports · doi:10.1038/s41598-019-43535-6 · Cited by 116
TREM-1 multimerization is essential for its activation on monocytes and neutrophils
Carrasco, K., Boufenzer, A., Jolly, L., Cordier, H. L., Wang, G., Heck, A. J. R., Cerwenka, A., Vinolo, E., Nazabal, A., Kriznik, A., et al. (2018) · Cellular and Molecular Immunology · doi:10.1038/s41423-018-0003-5 · Cited by 100
TREM-1: A new regulator of innate immunity in sepsis syndrome
Nathan, C., & Ding, A. H. (2001) · Nature Medicine · doi:10.1038/87846 · Cited by 100
TREM‐1 promotes survival during septic shock in mice
Gibot, S., Massin, F., Marcou, M., Taylor, V., Stidwill, R. P., Wilson, P., Singer, M., & Bellingan, G. J. (2007) · European Journal of Immunology · doi:10.1002/eji.200636387 · Cited by 100
Analysis of endogenous peptides bound by soluble MHC class I molecules: a novel approach for identifying tumor-specific antigens
Barnea, E., Beer, I., Patoka, R., Ziv, T., Kessler, O., Tzehoval, E., Eisenbach, L., Zavazava, N., & Admon, A. (2002) · European Journal of Immunology · doi:10.1002/1521-4141(200201)32:1 · Cited by 92
The Three-Dimensional Structure of the Human NK Cell Receptor NKp44, a Triggering Partner in Natural Cytotoxicity
Cantoni, C., Ponassi, M., Biassoni, R., Conte, R., Spallarossa, A., Moretta, A., Moretta, L., Bolognesi, M., & Bordo, D. (2003) · Structure · doi:10.1016/s0969-2126(03)00095-9 · Cited by 100
G-protein coupled receptor, PI3K and Rho signaling pathways regulate the cascades of Tau and amyloid-β in Alzheimer’s disease
Desale, S. E., Chidambaram, H., & Chinnathambi, S. (2021) · Molecular Biomedicine · doi:10.1186/s43556-021-00036-1 · Cited by 99
The systemic inflammatory response syndrome
Weigand, M. A., Hörner, C., Bardenheuer, H. J., & Bouchon, A. (2004) · Best practice & research. Clinical anaesthesiology · doi:10.1016/j.bpa.2003.12.005 · Cited by 98
DAP12 (KARAP) amplifies inflammation and increases mortality from endotoxemia and septic peritonitis
Turnbull, I. R., McDunn, J. E., Takai, T., Townsend, R. R., Cobb, J. P., & Colonna, M. (2005) · The Journal of Experimental Medicine · doi:10.1084/jem.20050986 · Cited by 99
“Therefore, it is possible that high concentrations of LPS, elevated inflammatory cytokines, and an extended time course of inflammation in simple endotoxemia may induce the expression of high affinity DAP12-associated receptor–ligand pairs that can synergize with TLR-mediated pathways to drive cytokine production as d…”
BackgroundInfluential
Microbes-induced EMT at the crossroad of inflammation and cancer
Hofman, P. M., & Vouret‐Craviari, V. (2012) · Gut Microbes · doi:10.4161/gmic.20288 · Cited by 95
Aging and Neutrophils: There Is Still Much To Do
Fortin, C. F., McDonald, P. P., Lesur, O., & Fülöp, T. (2008) · Rejuvenation Research · doi:10.1089/rej.2008.0750 · Cited by 97
“45 TREM-1 is on the surface of PMNs and monocytes, and bacterial lipopolysaccharides (LPS) induce its expression.”
Surface triggering receptor expressed on myeloid cells 1 expression patterns in septic shock
Gibot, S., Renard, P. L., Bollaert, P., Kolopp‐Sarda, M., Béné, M. C., Faure, G. C., & L�vy, B. (2005) · Intensive Care Medicine · doi:10.1007/s00134-005-2572-x · Cited by 93
DAP12: an adapter protein with dual functionality
Takaki, R., Watson, S. R., & Lanier, L. L. (2006) · Immunological Reviews · doi:10.1111/j.1600-065x.2006.00466.x · Cited by 91
“Signaling through TREM-1 has been shown to intersect the TLR signaling pathway and augment the TLRinduced immune response mediated by neutrophils and monocytes (18, 19).”
Background
Innate immune recognition by stimulatory immunoreceptors
Diefenbach, A., & Raulet, D. H. (2003) · Current Opinion in Immunology · doi:10.1016/s0952-7915(02)00007-9 · Cited by 93
ITIM receptors: more than just inhibitors of platelet activation
Coxon, C. H., Geer, M. J., & Senis, Y. A. (2017) · Blood · doi:10.1182/blood-2016-12-720185 · Cited by 92
OSCAR is an FcRγ-associated receptor that is expressed by myeloid cells and is involved in antigen presentation and activation of human dendritic cells
Merck, E., Gaillard, C., Gorman, D. M., Montero‐Julian, F. A., Durand, I., Zurawski, S., Ménétrier‐Caux, C., Carra, G., Lebecque, S., Trinchieri, G., et al. (2004) · Blood · doi:10.1182/blood-2004-03-0850 · Cited by 92
Regulation of TREM expression in hepatic macrophages and endothelial cells during acute endotoxemia
Chen, L. C., Laskin, J. D., Gordon, M. K., & Laskin, D. L. (2007) · Experimental and Molecular Pathology · doi:10.1016/j.yexmp.2007.11.004 · Cited by 90
“Activation of TREM-1 is associated with release of proinflammatory mediators and reactive oxygen and nitrogen intermediates by phagocytic leukocytes (Bouchon et al., 2000; Gibot et al., 2007; Radsak et al., 2004).”
Background
Inflammatory cytokines and signaling pathways are associated with survival of primary chronic lymphocytic leukemia cells in vitro: a dominant role of CCL2
Schulz, A., Toedt, G., Zenz, T., Stilgenbauer, S., Lichter, P., & Seiffert, M. (2011) · Haematologica · doi:10.3324/haematol.2010.031377 · Cited by 100
“immune responses in cooperation with Toll-like receptors and in inflammatory processes.(34) Immune-related and inflammatory conditions have been recognized to be of importance in the pathogenesis of CLL, and anti-inflammatory drugs are currently being tested as potential therapeutic agents for CLL patients.”
Background
TREM-1 expression is increased in the synovium of rheumatoid arthritis patients and induces the expression of pro-inflammatory cytokines
Kuai, J., Gregory, B., Hill, A., Pittman, D. D., Feldman, J. L., Brown, T., Carito, B. A., O’Toole, M., Ramsey, R., Adolfsson, O., et al. (2009) · Lara D. Veeken · doi:10.1093/rheumatology/kep235 · Cited by 92
Triggering receptor expressed on myeloid cells: role in the diagnosis of lung infections
Richeldi, L., Mariani, M., Losi, M., Maselli, F., Corbetta, L., Buonsanti, C., Colonna, M., Sinigaglia, F., Panina‐Bordignon, P., & Fabbri, L. M. (2004) · European Respiratory Journal · doi:10.1183/09031936.04.00014204 · Cited by 92
Vps35-dependent recycling of Trem2 regulates microglial function
Yin, J., Liu, X., He, Q., Zhou, L., Yuan, Z., & Zhao, S. (2016) · Traffic · doi:10.1111/tra.12451 · Cited by 90
“Trem2 consists of a leading signal peptide, a single type V extracellular region containing 3 potential N-glycosylation sites, a transmembrane domain and a short cytoplasmic tail lacking signaling motifs.(1) Owing to its short cytoplasmic tail, Trem2 needed to transfer its signaling by Dap12, an adaptor protein,(2) wh…”
TREM2 suppresses the proinflammatory response to facilitate PRRSV infection via PI3K/NF-κB signaling
Zhu, Z., Zhang, X., Dong, W., Wang, X., he, S. T., Zhang, H., Wang, X., Wei, R., Chen, Y., Liu, X., et al. (2020) · PLoS Pathogens · doi:10.1371/journal.ppat.1008543 · Cited by 91
“Triggering receptor expressed on myeloid cells 2 (TREM2) is a novel cell surface receptor, which was first identified in 2000 [21].”
Background
Current Evidence and Limitation of Biomarkers for Detecting Sepsis and Systemic Infection
Hung, S.-K., Lan, H.-M., Han, S.-T., Wu, C., & Chen, K. (2020) · Biomedicines · doi:10.3390/biomedicines8110494 · Cited by 94
Potentiation of NETs release is novel characteristic of TREM-1 activation and the pharmacological inhibition of TREM-1 could prevent from the deleterious consequences of NETs release in sepsis
Boufenzer, A., Carrasco, K., Jolly, L., Brustolin, B., Pillo, E. D., Derive, M., & Gibot, S. (2021) · Cellular and Molecular Immunology · doi:10.1038/s41423-020-00591-7 · Cited by 89
TREM-1 Activation Alters the Dynamics of Pulmonary IRAK-M Expression In Vivo and Improves Host Defense during Pneumococcal Pneumonia
Lagler, H., Sharif, O., Haslinger, I., Matt, U., Stich, K., Furtner, T., Doninger, B., Schmid, K., Gattringer, R., de Vos, A. F., et al. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.0803862 · Cited by 90
Diagnostic value of the soluble triggering receptor expressed on myeloid cells-1 in bacterial infection: a meta-analysis
Jiyong, J., Tiancha, H., Cui, W., & Huahao, S. (2008) · Intensive Care Medicine · doi:10.1007/s00134-008-1333-z · Cited by 89
“The triggering receptor expressed on myeloid cells-1 (TREM-1) is a recently discovered member of the immunoglobulin super family, the expression of which on phagocytosis is up-regulated by exposure to bacteria and fungi [12].”
BackgroundInfluential
Dynamic changes of serum soluble triggering receptor expressed on myeloid cells-1 (sTREM-1) reflect sepsis severity and can predict prognosis: a prospective study
Zhang, J., She, D., Feng, D., et al. (2011) · BMC Infectious Diseases · doi:10.1186/1471-2334-11-53 · Cited by 89
“in 2000 [1], is a member of the immunoglobulin superfamily of receptors that is specifically expressed on the surfaces of monocytes and neutrophils.”
Background

Authors: Bouchon, A., Dietrich, J., & Colonna, M.
Affiliations: Basel Institute for Immunology , Basel ,
ORCID: Dietrich, Jes
Colonna, Marco
Venue: The Journal of Immunology
Publisher: Oxford University Press (OUP)
Published: 2000-05
Volume: 164
Issue: 10
Pages: 4991-4995
ISSN: 0022-1767 (ISSN-L)
1550-6606
DOI: 10.4049/jimmunol.164.10.4991
OpenAlex: W2149698238
Semantic Scholar: c6fffd66acdcb27c928605f7aca443056a3a6c3f
Cited by: 1,284
References: 13
Citations by year: 2026: 38 · 2025: 47 · 2024: 73 · 2023: 87 · 2022: 51 · 2021: 65 · 2020: 83 · 2019: 49 · 2018: 55 · 2017: 51 · 2016: 59 · 2015: 47 · 2014: 48 · 2013: 68 · 2012: 50
FWCI: 6.50
Type: journal article
Language: en
Open access: closed
Licence: academic.oup.com/pages/standard-publication-reuse-rights (vor)
Locations: The Journal of Immunology (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Immunology and Microbiology › Immunology › Inflammation biomarkers and pathways
Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
Life Sciences › Immunology and Microbiology › Immunology › Neutrophil, Myeloperoxidase and Oxidative Mechanisms
Keywords: TREM-1, neutrophils, monocytes, inflammation, IL-8 secretion, MCP-1, TNF-α, neutrophil degranulation, calcium mobilization, phospholipase C-gamma, myeloid cell activation
MeSH terms: Triggering Receptor Expressed on Myeloid Cells-1, Amino Acid Sequence, Fungi, Multigene Family, Gram-Negative Bacteria, Gram-Positive Bacteria, Humans, Immunoglobulins, Inflammation, Macrophage Activation, Membrane Glycoproteins, Membrane Proteins, Molecular Sequence Data, Molecular Weight, Monocytes, Neutrophils, Phosphorylation, Receptors, Immunologic, Tyrosine, Biomarkers, Up-Regulation, Cytokines, Neutrophil Activation, Chemokines, Calcium Signaling, Adaptor Proteins, Signal Transducing

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Cutting Edge: Inflammatory Responses Can Be Triggered by TREM-1, a Novel Receptor Expressed on Neutrophils and Monocytes

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