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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BackgroundResult
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Background
Crystal Structure of Human Triggering Receptor Expressed on Myeloid Cells 1 (TREM-1) at 1.47Å
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“Copyright © 2005 by The American Association of Immunologists, Inc. 0022-1767/05/$02.00 through tethering of certain PAMPs to the plasma membrane and facilitating their interaction with downstream TLRs and perhaps other signaling elements (37).”
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BackgroundMethod
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Background
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Background
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Background
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Influential
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“TREM-1 was the first TREM identified and initial studies established TREM-1 as an amplifier of the systemic inflammatory response syndrome and sepsis [18] [19] [17] [20].”
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Hommes, T. J., Hoogendijk, A. J., Dessing, M. C., Veer, C. V. ′., Florquin, S., Colonna, M., de Vos, A. F., & van der Poll, T. (2014) · The Journal of Pathology · doi:10.1002/path.4361 · Cited by 53
“Other studies have confirmed the constitutive expression of TREM-1 on human alveolar macrophages and the increased TREM-1 expression on human blood neutrophils during severe infection [6,11,19,26].”
BackgroundResultInfluential
TREM-1 promotes intestinal tumorigenesis
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“[6] in 2000, it has been regarded as a promising marker for its importance in inflammatory responses [7, 8].”
Background
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“Background Triggering receptor expressed on myeloid cells 2 (TREM2) is an immunomodulatory cell surface receptor expressed in myeloid lineage cells including microglia [1, 2].”
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“Bouchon A and his colleagues [4] first identified a new Ig superfamily of receptors exclusively expressed on myeloid cells, which were designated triggering receptor expressed on myeloid cells (TREM).”
HIV-related proteins prolong macrophage survival through induction of Triggering receptor expressed on myeloid cells-1
Yuan, Z., Fan, X., Staitieh, B. S., et al. (2017) · Scientific Reports · doi:10.1038/srep42028 · Cited by 50
The characteristics and pivotal roles of triggering receptor expressed on myeloid cells-1 in autoimmune diseases
Gao, S., Yi, Y., Xia, G., Yu, C., Ye, C., Tu, F., Shen, L., Wang, W., & Hua, C. (2018) · Autoimmunity Reviews · doi:10.1016/j.autrev.2018.07.008 · Cited by 49
Analysis of mouse LMIR5/CLM-7 as an activating receptor: differential regulation of LMIR5/CLM-7 in mouse versus human cells
Yamanishi, Y., Kitaura, J., Izawa, K., Matsuoka, T., Oki, T., Yang, L., Shibata, F., Yamazaki, S., Kumagai, H., Nakajima, H., et al. (2007) · Blood · doi:10.1182/blood-2007-04-085787 · Cited by 50
TREM1 Regulates Neuroinflammatory Injury by Modulate Proinflammatory Subtype Transition of Microglia and Formation of Neutrophil Extracellular Traps via Interaction With SYK in Experimental Subarachnoid Hemorrhage
Wu, X., Zeng, H., Xu, C., et al. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.766178 · Cited by 49
Btk is a positive regulator in the TREM-1/DAP12 signaling pathway
Ormsby, T., Schlecker, E., Ferdin, J., Tessarz, A. S., Angelisová, P., Köprülü, A. D., Borte, M., Warnatz, K., Schulze, I., Ellmeier, W., et al. (2011) · Blood · doi:10.1182/blood-2010-11-317016 · Cited by 49
The Triggering Receptor Expressed on Myeloid Cells 2: “TREM-ming” the Inflammatory Component Associated with Alzheimer's Disease
Rohn, T. T. (2013) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2013/860959 · Cited by 51
“TREM2 is thought to act as a cell surface receptor, and although the endogenous ligand has yet to be identified, it is known that it requires the adaptor protein 12 (DAP12) for the initiation of signaling cascades [63].”
Background
Measurement of Plasma STREM-1 in Patients With Severe Sepsis Receiving Early Goal-Directed Therapy and Evaluation of Its Usefulness
Jeong, S. J., Song, Y. G., Kim, C. O., Kim, H. W., Ku, N. S., Han, S. H., Choi, J. Y., & Kim, J. M. (2012) · Shock · doi:10.1097/shk.0b013e318250da40 · Cited by 49
“Triggering receptor expressed on myeloid cells 1, recently identified to be involved in inflammatory responses (3), acts in synergy with Toll-like receptor signaling”
Background
Cerebrospinal fluid sTREM2 in Alzheimer’s disease: comparisons between clinical presentation and AT classification
Knapskog, A., Henjum, K., Idland, A., Eldholm, R. S., Persson, K., Saltvedt, I. T., Watne, L. O., Engedal, K., & Nilsson, L. N. G. (2020) · Scientific Reports · doi:10.1038/s41598-020-72878-8 · Cited by 53
Ligation of the FcRγ Chain-Associated Human Osteoclast-Associated Receptor Enhances the Proinflammatory Responses of Human Monocytes and Neutrophils
Merck, E., Gaillard, C., Scuiller, M., Scapini, P., Cassatella, M. A., Trinchieri, G., & Bates, E. E. M. (2006) · The Journal of Immunology · doi:10.4049/jimmunol.176.5.3149 · Cited by 49
“In addition, TREM-1 engagement is able to enhance the responses of monocytes and neutrophils upon stimulation with TLR ligands (7, 11, 12).”
Background
Doxycycline inhibits TREM-1 induction by Porphyromonas gingivalis
Bostancı, N., & Belibasakis, G. N. (2012) · FEMS Immunology & Medical Microbiology · doi:10.1111/j.1574-695x.2012.00982.x · Cited by 48
Biomarkers in the diagnosis of aspiration syndromes
Jaoude, P., Knight, P. R., Ohtake, P. J., et al. (2010) · Expert Review of Molecular Diagnostics · doi:10.1586/erm.10.7 · Cited by 48
Targeted endothelial gene deletion of triggering receptor expressed on myeloid cells-1 protects mice during septic shock
Jolly, L., Carrasco, K., Derive, M., et al. (2018) · Cardiovascular Research · doi:10.1093/cvr/cvy018 · Cited by 48
“The Triggering Receptor Expressed on Myeloid cells-1 (TREM-1) is an immune-receptor that plays a key role in the amplification of inflammation, crosstalk with other Pattern Recognition Receptors pathways and activation of antigen-presenting cells.(10,11) Membrane TREM-1 presents three distinct domains: an Ig-like stru…”
Frontobasal gray matter loss is associated with the TREM2 p.R47H variant
Luis, E. O., Ortega-Cubero, S., Lamet, I., Razquin, C., Cruchaga, C., Benitez, B. A., Lorenzo, E., Irigoyen, J., Pastor, M. A., & Pastor, P. (2014) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2014.06.007 · Cited by 47
“TREM2 promotes the production of constitutive in ﬂ ammatory cytokines in microglia (Bouchon et al., 2000; Lanier and Bakker, 2000), leading to the phagocytosis of cell debris and amyloid (Paloneva et al., 2002; Takahashi et al., 2005).”
Novel ligands and modulators of triggering receptor expressed on myeloid cells receptor family: 2015-2020 updates
Singh, H., Rai, V., Nooti, S. K., & Agrawal, D. K. (2021) · Expert Opinion on Therapeutic Patents · doi:10.1080/13543776.2021.1883587 · Cited by 47
“lipopolysaccharide (LPS) which is involved in TREM-1 activation and thus can be considered as its non-endogenous ligand [6,39], but it is still a quest whether LPS activates TREM-1 directly or indirectly through other receptors [79].”
Background
TREM1 activation of myeloid cells promotes antitumor immunity
Juric, V., Mayes, E., Binnewies, M., Lee, T., Canaday, P. S., Pollack, J. L., Rudolph, J. D., Du, X., Liu, V. M., Dash, S., et al. (2023) · Science Translational Medicine · doi:10.1126/scitranslmed.add9990 · Cited by 46
TREM-1 Expression Is Increased in Human Placentas From Severe Early-Onset Preeclamptic Pregnancies Where It May Be Involved in Syncytialization
Lim, R., Barker, G., & Lappas, M. (2013) · Reproductive Sciences · doi:10.1177/1933719113503406 · Cited by 47
“The TREM-1 is expressed by neutrophils, macrophages, and mature monocytes and has been described as an amplifier of the inflammatory response.(50) During inflammatory conditions, TREM-1 is upregulated and redirects myeloid cell differentiation and function, thus promoting inflammatory responses.”
Background
The Role of TREM2 in Alzheimer’s Disease and Other Neurological Disorders
Yaghmoor, F. (2014) · Journal of Alzheimer’s Disease & Parkinsonism · doi:10.4172/2161-0460.1000160 · Cited by 45
Identification of Extracellular Actin As a Ligand for Triggering Receptor Expressed on Myeloid Cells-1 Signaling
Fu, L., Li, H., Xie, C., Li, W., Lin, L., Pan, S.-S., Zhou, Y., Li, Z., Jin, M., & Zhang, A. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.00917 · Cited by 47
HIV and HCV augments inflammatory responses through increased TREM-1 expression and signaling in Kupffer and Myeloid cells
Hyun, J., McMahon, R. S., Lang, A. L., Edwards, J. S., Badilla, A. D., Greene, M. E., Stone, G. W., Pallikkuth, S., Stevenson, M., Dykxhoorn, D. M., et al. (2019) · PLoS Pathogens · doi:10.1371/journal.ppat.1007883 · Cited by 46
Triggering Receptor Expressed on Myeloid cells-1 (TREM-1) Modulates Immune Responses toAspergillus fumigatusDuring Fungal Asthma in Mice
Buckland, K. F., Ramaprakash, H., Murray, L. A., et al. (2011) · Immunological Investigations · doi:10.3109/08820139.2011.578270 · Cited by 47
Natural killer cells and lung transplantation, roles in rejection, infection, and tolerance
Fildes, J. E., Yonan, N. A., & Leonard, C. T. (2008) · Transplant Immunology · doi:10.1016/j.trim.2008.01.004 · Cited by 46
Triggering Receptor Expressed on Myeloid Cells (TREM) Family and the Application of Its Antagonists
Molloy, E. J. (2009) · Recent Patents on Anti-Infective Drug Discovery · doi:10.2174/157489109787236292 · Cited by 46
“Furthermore, LPS causes synergistic enhancement of cytokine production by monocytes in response to the agonistic monoclonal antibody, indicating that TREM-1 amplifies inflammatory responses initiated by TLRs [14,15, 17,18].”
BackgroundMethodInfluential
Functional analysis of the CD300e receptor in human monocytes and myeloid dendritic cells
Brckalo, T., Calzetti, F., Pérez‐Cabezas, B., Borràs, F. E., Cassatella, M. A., & López‐Botet, M. (2009) · European Journal of Immunology · doi:10.1002/eji.200939468 · Cited by 46
Resveratrol attenuates the pathogenic and inflammatory properties of Porphyromonas gingivalis
Lagha, A. B., Andrian, E., & Grenier, D. (2019) · Molecular Oral Microbiology · doi:10.1111/omi.12260 · Cited by 46
Differential Regulation of DAP12 and Molecules Associated with DAP12 during Host Responses to Mycobacterial Infection
Aoki, N., Zganiacz, A., Margetts, P. J., & Xing, Z. (2004) · Infection and Immunity · doi:10.1128/iai.72.5.2477-2483.2004 · Cited by 46
Endocan and Soluble Triggering Receptor Expressed on Myeloid Cells-1 as Novel Markers for Neonatal Sepsis
Saldır, M., Tunç, T., Çekmez, F., et al. (2015) · Pediatrics & Neonatology · doi:10.1016/j.pedneo.2015.03.006 · Cited by 45
Involvement of the TREM-1/DAP12 pathway in the innate immune responses to Porphyromonas gingivalis
Bostancı, N., Thurnheer, T., & Belibasakis, G. N. (2011) · Molecular Immunology · doi:10.1016/j.molimm.2011.09.012 · Cited by 45
Involvement of FcR in signal transduction of osteoclast-associated receptor (OSCAR)
Ishikawa, S. (2004) · International Immunology · doi:10.1093/intimm/dxh103 · Cited by 45
Biomarkers: A Definite Plus in Pneumonia
Summah, H. D., & Qu, J. (2009) · Mediators of Inflammation · doi:10.1155/2009/675753 · Cited by 45
“It has been found that the tansmembrane adapter protein DAP12 is the signal transduction molecule through which TREM-1 activates neutrophils and monocytes [56].”
Background
Expression of TREM-1 mRNA in acute pancreatitis
Wang, D.-Y. (2004) · World Journal of Gastroenterology · doi:10.3748/wjg.v10.i18.2744 · Cited by 45
Biomarkers and infection in the emergency unit
Hausfater, P. (2014) · Médecine et Maladies Infectieuses · doi:10.1016/j.medmal.2014.01.002 · Cited by 44
Role of TREM-1 in response to Aspergillus fumigatus infection in corneal epithelial cells
Hu, L., Du, Z., Zhao, G., Jiang, N., Lin, J., Wang, Q., Xu, Q., Lin, C., & Qiu, S. (2014) · International Immunopharmacology · doi:10.1016/j.intimp.2014.09.011 · Cited by 44
Therapeutic Effect of Modulating TREM-1 via Anti-inflammation and Autophagy in Parkinson’s Disease
Feng, C., Chen, N., Sung, C., Kuo, H., Yang, S., Chen, C., Hung, H.-C., Chen, B., Wen, Z., & Chen, W.-F. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.00769 · Cited by 44
Neutrophil dynamics and inflammaging in acute ischemic stroke: A transcriptomic review
Bui, T. A., Jickling, G. C., & Winship, I. R. (2022) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2022.1041333 · Cited by 46
“Significant and wellstudied neutrophil-specific pathways post-ischemia include mTOR (Maiese, 2014), ERK5 (Becker, 1998), integrin (Bouchon et al., 2000), thrombopoietin (Yang et al.”
Background
Single-cell spatial transcriptomics reveals distinct patterns of dysregulation in non-neuronal and neuronal cells induced by the Trem2R47H Alzheimer’s risk gene mutation
Johnston, K. G., Berackey, B. T., Tran, K. M., Gelber, A., Yu, Z., MacGregor, G. R., Mukamel, E. A., Tan, Z., Green, K. N., & Xu, X. (2024) · Molecular Psychiatry · doi:10.1038/s41380-024-02651-0 · Cited by 51
“TREM2 is an immunomodulatory cell surface receptor expressed primarily in microglia in the brain [4, 5], and is activated by a variety of ligands including amyloid-beta (A β ), APOE, and phospholipids [6].”
The role of the triggering receptor expressed on myeloid cells-1 (TREM-1) in non-bacterial infections
Matos, A. D. O., Dantas, P. H. D. S., Silva‐Sales, M., & Sales‐Campos, H. (2020) · Critical Reviews in Microbiology · doi:10.1080/1040841x.2020.1751060 · Cited by 43
“The receptor establishes a complex with DAP12 (Figure 1), a transmembrane adaptor protein that mediates signal transduction (Bouchon et al. 2000; Kelker et al. 2004) and helps in the stabilization of the receptor on the cell surface (Carrasco et al. 2019).”
BackgroundInfluential
sTREM-1 predicts mortality in hospitalized patients with infection in a tropical, middle-income country
Wright, S. W., Lovelace-Macon, L., Hantrakun, V., Rudd, K. E., Teparrukkul, P., Harju-Baker, S., Liles, W. C., Limmathurotsakul, D., & West, T. E. (2020) · BMC Medicine · doi:10.1186/s12916-020-01627-5 · Cited by 43
The gene encoding the immunoregulatory signaling molecule CMRF‐35A localized to human chromosome 17 in close proximity to other members of the CMRF‐35 family
Clark, G. J., Cooper, B., Fitzpatrick, S., et al. (2001) · Tissue Antigens · doi:10.1034/j.1399-0039.2001.057005415.x · Cited by 43
Deletion of cognate CD8 T cells by immature dendritic cells: a novel role for perforin, granzyme A, TREM-1, and TLR7
Zangi, L., Klionsky, Y. Z., Yarimi, L., Bachar-Lustig, E., Eidelstein, Y., Shezen, E., Hagin, D., Ito, Y., Takai, T., Reich-Zeliger, S., et al. (2012) · Blood · doi:10.1182/blood-2012-02-410803 · Cited by 42
Sepsis: From Bench to Bedside
Silva, E., Passos, R. D. H., Ferri, M. B., & de Figueiredo, L. F. P. (2008) · Clinics · doi:10.1590/s1807-59322008000100019 · Cited by 43
A first‐in‐man safety and pharmacokinetics study of nangibotide, a new modulator of innate immune response through TREM‐1 receptor inhibition
Cuvier, V., Lorch, U., Witte, S., Olivier, A., Gibot, S., Delor, I., Garaud, J., Derive, M., & Salcedo‐Magguilli, M. (2018) · British Journal of Clinical Pharmacology · doi:10.1111/bcp.13668 · Cited by 45
Immunomodulatory effect of ibrutinib: Reducing the barrier against fungal infections
Maffei, R., Maccaferri, M., Arletti, L., Fiorcari, S., Benatti, S., Potenza, L., Luppi, M., & Marasca, R. (2019) · Blood Reviews · doi:10.1016/j.blre.2019.100635 · Cited by 43
Triggering receptor expressed on myeloid cells-1 (TREM-1) as a therapeutic target in infectious and noninfectious disease: a critical review
Dantas, P. H. D. S., Matos, A. D. O., Filho, E. D. S., Silva‐Sales, M., & Sales‐Campos, H. (2020) · International Reviews of Immunology · doi:10.1080/08830185.2020.1762597 · Cited by 42
Trem1 Induces Periodontal Inflammation via Regulating M1 Polarization
Wu, D., Weng, Y., Feng, Y., et al. (2021) · Journal of Dental Research · doi:10.1177/00220345211044681 · Cited by 42
“In addition, we found a positive correlation between Trem1 and M1 macrophages, which is consistent with previous studies (Bouchon et al. 2000; Chen et al. 2017).”
Result

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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