Genetic and Pharmacological Inhibition of TREM-1 Limits the Development of Experimental Atherosclerosis

Journal of the American College of Cardiology

Volumn 68, Issue 25, 2016, Pages 2776-2793

  Joffre, Jeremie ^a,b   Potteaux, Stephane ^a,b   Zeboudj, Lynda ^a,b   Loyer, Xavier ^a,b   Boufenzer, Amir ^c   Laurans, Ludivine ^a,b   Esposito, Bruno ^a,b   Vandestienne, Marie ^a,b   de Jager, Saskia C A ^d   Hénique, Carole ^a,b   Zlatanova, Ivana ^a,b   Taleb, Soraya ^a,b   Bruneval, Patrick ^a,b,e   Tedgui, Alain ^a,b   Mallat, Ziad ^a,b,f   Gibot, Sebastien ^g   Ait Oufella, Hafid ^a,b,h  

^a PARIS CARDIOVASCULAR RESEARCH CENTER   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c INOTREM SA   (France)

^d UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^e HÔPITAL EUROPÉEN GEORGES POMPIDOU   (France)

^f UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^g UNIVERSITÉ DE LORRAINE   (France)

^h ASSISTANCE PUBLIQUE HÔPITAUX DE PARIS   (France)

Author keywords

apolipoprotein; foam cells; inflammation; macrophage; toll like receptor

Indexed keywords

CD36 ANTIGEN; LR12 PEPTIDE; PEPTIDE DERIVATIVE; TOLL LIKE RECEPTOR 4; TRIGGERING RECEPTOR EXPRESSED ON MYELOID CELLS 1; UNCLASSIFIED DRUG; IMMUNOGLOBULIN RECEPTOR; LAURIC ACID DERIVATIVE; LISSAMINE-RHODAMINE DODECANOIC ACID; MEMBRANE PROTEIN; RHODAMINE; TREM1 PROTEIN, MOUSE;

ABDOMINAL AORTA; AORTA SINUS; ARTICLE; ATHEROGENESIS; ATHEROSCLEROTIC PLAQUE; BONE MARROW DEPRESSION; DISEASE COURSE; ENZYME INHIBITION; EXPERIMENTAL ATHEROSCLEROSIS; FOAM CELL; HUMAN; HUMAN CELL; IMMUNOREGULATION; INNATE IMMUNE ACTIVATION; INNATE IMMUNITY; KNOCKOUT MOUSE; MACROPHAGE; MALE; MONOCYTE; MOUSE; PRIORITY JOURNAL; PROTEIN FUNCTION; UPREGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; APOPTOSIS; BIOSYNTHESIS; C57BL MOUSE; CAROTID ARTERY; CAROTID ARTERY DISEASES; CELL CULTURE; DISEASE MODEL; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE THERAPY; IMMUNOLOGY; METABOLISM; PATHOLOGY; PLAQUE, ATHEROSCLEROTIC; PROCEDURES; TRANSGENIC MOUSE;

ANIMALS; APOPTOSIS; CAROTID ARTERIES; CAROTID ARTERY DISEASES; CELLS, CULTURED; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; GENETIC THERAPY; HUMANS; IMMUNITY, INNATE; LAURIC ACIDS; MACROPHAGES; MALE; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PLAQUE, ATHEROSCLEROTIC; RECEPTORS, IMMUNOLOGIC; RHODAMINES;

EID: 85006459101     PISSN: 07351097     EISSN: 15583597     Source Type: Journal    
DOI: 10.1016/j.jacc.2016.10.015     Document Type: Article

References (67)

1. 1 Libby, P., Lichtman, A.H., Hansson, G.K., Immune effector mechanisms implicated in atherosclerosis: from mice to humans. Immunity 38 (2013), 1092–1104.
2. 2 Hansson, G.K., Inflammation, atherosclerosis, and coronary artery disease. N Engl J Med 352 (2005), 1685–1695.
3. 3 Tedgui, A., Mallat, Z., Cytokines in atherosclerosis: pathogenic and regulatory pathways. Physiol Rev 86 (2006), 515–581.
4. 4 Moore, K.J., Tabas, I., Macrophages in the pathogenesis of atherosclerosis. Cell 145 (2011), 341–355.
5. 5 Weber, C., Noels, H., Atherosclerosis: current pathogenesis and therapeutic options. Nat Med 17 (2011), 1410–1422.
6. 6 Potteaux, S., Ait-Oufella, H., Mallat, Z., Role of splenic monocytes in atherosclerosis. Curr Opin Lipidol 26 (2015), 457–463.
7. 7 Libby, P., Inflammation in atherosclerosis. Nature 420 (2002), 868–874.
8. 8 Ait-Oufella, H., Taleb, S., Mallat, Z., Tedgui, A., Recent advances on the role of cytokines in atherosclerosis. Arterioscler Thromb Vasc Biol 31 (2011), 969–979.
9. 9 Robbins, C.S., Hilgendorf, I., Weber, G.F., et al. Local proliferation dominates lesional macrophage accumulation in atherosclerosis. Nat Med 19 (2013), 1166–1172.
10. 10 Seimon, T.A., Nadolski, M.J., Liao, X., et al. Atherogenic lipids and lipoproteins trigger CD36-TLR2-dependent apoptosis in macrophages undergoing endoplasmic reticulum stress. Cell Metab 12 (2010), 467–482.
11. 11 Stewart, C.R., Stuart, L.M., Wilkinson, K., et al. CD36 ligands promote sterile inflammation through assembly of a Toll-like receptor 4 and 6 heterodimer. Nat Immunol 11 (2010), 155–161.
12. 12 Brown, P.M., Kennedy, D.J., Morton, R.E., Febbraio, M., CD36/SR-B2-TLR2 dependent pathways enhance Porphyromonas gingivalis mediated atherosclerosis in the Ldlr KO mouse model. PLoS One, 10, 2015, e0125126.
13. 13 Moore, K.J., Freeman, M.W., Scavenger receptors in atherosclerosis: beyond lipid uptake. Arterioscler Thromb Vasc Biol 26 (2006), 1702–1711.
14. 14 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 (2000), 4991–4995.
15. 15 Bouchon, A., Facchetti, F., Weigand, M.A., Colonna, M., TREM-1 amplifies inflammation and is a crucial mediator of septic shock. Nature 410 (2001), 1103–1107.
16. 16 Ford, J.W., McVicar, D.W., TREM and TREM-like receptors in inflammation and disease. Curr Opin Immunol 21 (2009), 38–46.
17. 17 Klesney-Tait, J., Keck, K., Li, X., et al. Transepithelial migration of neutrophils into the lung requires TREM-1. J Clin Invest 123 (2013), 138–149.
18. 18 Yasuda, T., Takeyama, Y., Ueda, T., et al. Increased levels of soluble triggering receptor expressed on myeloid cells-1 in patients with acute pancreatitis. Crit Care Med 36 (2008), 2048–2053.
19. 19 Kuai, J., Gregory, B., Hill, A., et al. TREM-1 expression is increased in the synovium of rheumatoid arthritis patients and induces the expression of pro-inflammatory cytokines. Rheumatology (Oxford) 48 (2009), 1352–1358.
20. 20 Derive, M., Bouazza, Y., Sennoun, N., et al. Soluble TREM-like transcript-1 regulates leukocyte activation and controls microbial sepsis. J Immunol 188 (2012), 5585–5592.
21. 21 Derive, M., Boufenzer, A., Bouazza, Y., et al. Effects of a TREM-like transcript 1-derived peptide during hypodynamic septic shock in pigs. Shock 39 (2013), 176–182.
22. 22 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. Anesthesiology 120 (2014), 935–942.
23. 23 Boufenzer, A., Lemarie, J., Simon, T., et al. TREM-1 mediates inflammatory injury and cardiac remodeling following myocardial infarction. Circ Res 116 (2015), 1772–1782.
24. 24 Verhoeven, B.A., Velema, E., Schoneveld, A.H., et al. Athero-express: differential atherosclerotic plaque expression of mRNA and protein in relation to cardiovascular events and patient characteristics. Rationale and design. Eur J Epidemiol 19 (2004), 1127–1133.
25. 25 Hellings, W.E., Pasterkamp, G., Vollebregt, A., et al. Intraobserver and interobserver variability and spatial differences in histologic examination of carotid endarterectomy specimens. J Vasc Surg 46 (2007), 1147–1154.
26. 26 Bariety, J., Mandet, C., Hill, G.S., Bruneval, P., Parietal podocytes in normal human glomeruli. J Am Soc Nephrol 17 (2006), 2770–2780.
27. 27 Ait-Oufella, H., Herbin, O., Bouaziz, J.D., et al. B cell depletion reduces the development of atherosclerosis in mice. J Exp Med 207 (2010), 1579–1587.
28. 28 Daugherty, A., Whitman, S.C., Quantification of atherosclerosis in mice. Methods Mol Biol 209 (2003), 293–309.
29. 29 Mallat, Z., Gojova, A., Brun, V., et al. Induction of a regulatory T cell type 1 response reduces the development of atherosclerosis in apolipoprotein E-knockout mice. Circulation 108 (2003), 1232–1237.
30. −/− mice during disease regression. J Clin Invest 121 (2011), 2025–2036.
31. 31 Klesney-Tait, J., Keck, K., Li, X., et al. Transepithelial migration of neutrophils into the lung requires TREM-1. J Clin Invest 123 (2013), 138–149.
32. 32 Zanzinger, K., Schellack, C., Nausch, N., Cerwenka, A., Regulation of triggering receptor expressed on myeloid cells 1 expression on mouse inflammatory monocytes. Immunology 128 (2009), 185–195.
33. 33 Dower, K., Ellis, D.K., Saraf, K., Jelinsky, S.A., Lin, L.L., Innate immune responses to TREM-1 activation: overlap, divergence, and positive and negative cross-talk with bacterial lipopolysaccharide. J Immunol 180 (2008), 3520–3534.
34. 34 Geissmann, F., Jung, S., Littman, D.R., Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity 19 (2003), 71–82.
35. 35 Freigang, S., Ampenberger, F., Weiss, A., et al. Fatty acid-induced mitochondrial uncoupling elicits inflammasome-independent IL-1alpha and sterile vascular inflammation in atherosclerosis. Nat Immunol 14 (2013), 1045–1053.
36. 36 Xanthoulea, S., Gijbels, M.J., van der Made, I., et al. P55 tumour necrosis factor receptor in bone marrow-derived cells promotes atherosclerosis development in low-density lipoprotein receptor knock-out mice. Cardiovasc Res 80 (2008), 309–318.
37. 37 Klesney-Tait, J., Turnbull, I.R., Colonna, M., The TREM receptor family and signal integration. Nat Immunol 7 (2006), 1266–1273.
38. 38 Drechsler, M., Megens, R.T., van Zandvoort, M., Weber, C., Soehnlein, O., Hyperlipidemia-triggered neutrophilia promotes early atherosclerosis. Circulation 122 (2010), 1837–1845.
39. 39 Combadiere, C., Potteaux, S., Gao, J.L., et al. Decreased atherosclerotic lesion formation in CX3CR1/apolipoprotein E double knockout mice. Circulation 107 (2003), 1009–1016.
40. −/− mice reveals a role for fractalkine in atherogenesis. J Clin Invest 111 (2003), 333–340.
41. 41 Combadiere, C., Potteaux, S., Rodero, M., et al. Combined inhibition of CCL2, CX3CR1 and CCR5 abrogates Ly6C(hi) and Ly6C(lo) monocytosis and almost abolishes atherosclerosis in hypercholesterolemic mice. Circulation 117 (2008), 1649–1657.
42. 42 Cheng, C., Tempel, D., van Haperen, R., et al. Shear stress-induced changes in atherosclerotic plaque composition are modulated by chemokines. J Clin Invest 117 (2007), 616–626.
43. 43 Mallat, Z., Besnard, S., Duriez, M., et al. Protective role of interleukin-10 in atherosclerosis. Circ Res 85 (1999), e17–e24.
44. 44 Potteaux, S., Deleuze, V., Merval, R., et al. In vivo electrotransfer of interleukin-10 cDNA prevents endothelial upregulation of activated NF-kappaB and adhesion molecules following an atherogenic diet. Eur Cytokine Netw 17 (2006), 13–18.
45. 45 Gibot, S., Kolopp-Sarda, M.N., Bene, M.C., et al. A soluble form of the triggering receptor expressed on myeloid cells-1 modulates the inflammatory response in murine sepsis. J Exp Med 200 (2004), 1419–1426.
46. 46 Wang, Y.S., Li, X.J., Zhao, W.O., TREM-1 is a positive regulator of TNF-alpha and IL-8 production in U937 foam cells. Bosn J Basic Med Sci 12 (2012), 94–101.
47. 47 Schenk, M., Bouchon, A., Seibold, F., Mueller, C., TREM-1-expressing intestinal macrophages crucially amplify chronic inflammation in experimental colitis and inflammatory bowel diseases. J Clin Invest 117 (2007), 3097–3106.
48. 48 Weber, B., Schuster, S., Zysset, D., et al. TREM-1 deficiency can attenuate disease severity without affecting pathogen clearance. PLoS Pathog, 10, 2014, e1003900.
49. 49 Lo, T.H., Tseng, K.Y., Tsao, W.S., et al. TREM-1 regulates macrophage polarization in ureteral obstruction. Kidney Int 86 (2014), 1174–1186.
50. 50 Gosselin, D., Link, V.M., Romanoski, C.E., et al. Environment drives selection and function of enhancers controlling tissue-specific macrophage identities. Cell 159 (2014), 1327–1340.
51. 51 Virmani, R., Burke, A.P., Farb, A., Kolodgie, F.D., Pathology of the vulnerable plaque. J Am Coll Cardiol 47 (2006), C13–C18.
52. 52 Colonna, M., TREMs in the immune system and beyond. Nat Rev Immunol 3 (2003), 445–453.
53. 53 Tessarz, A.S., Cerwenka, A., The TREM-1/DAP12 pathway. Immunol Lett 116 (2008), 111–116.
54. 54 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 (2004), 4956–4963.
55. 55 Cai, M., Chen, Q., Chen, C., et al. Activation of triggering receptor expressed on myeloid cells-1 protects monocyte from apoptosis through regulation of myeloid cell leukemia-1. Anesthesiology 118 (2013), 1140–1149.
56. 56 Gomez-Pina, V., Martinez, E., Fernandez-Ruiz, I., et al. Role of MMPs in orchestrating inflammatory response in human monocytes via a TREM-1-PI3K-NF-kappaB pathway. J Leukoc Biol 91 (2012), 933–945.
57. 57 Lin, C.S., Lin, F.Y., Ho, L.J., et al. PKCdelta signalling regulates SR-A and CD36 expression and foam cell formation. Cardiovasc Res 95 (2012), 346–355.
58. 58 Mwaikambo, B.R., Yang, C., Chemtob, S., Hardy, P., Hypoxia up-regulates CD36 expression and function via hypoxia-inducible factor-1- and phosphatidylinositol 3-kinase-dependent mechanisms. J Biol Chem 284 (2009), 26695–26707.
59. 59 Febbraio, M., Podrez, E.A., Smith, J.D., et al. Targeted disruption of the class B scavenger receptor CD36 protects against atherosclerotic lesion development in mice. J Clin Invest 105 (2000), 1049–1056.
60. 60 Moore, K.J., Kunjathoor, V.V., Koehn, S.L., et al. Loss of receptor-mediated lipid uptake via scavenger receptor A or CD36 pathways does not ameliorate atherosclerosis in hyperlipidemic mice. J Clin Invest 115 (2005), 2192–2201.
61. 61 Kennedy, D.J., Kuchibhotla, S.D., Guy, E., et al. Dietary cholesterol plays a role in CD36-mediated atherogenesis in LDLR-knockout mice. Arterioscler Thromb Vasc Biol 29 (2009), 1481–1487.
62. 62 Sheedy, F.J., Grebe, A., Rayner, K.J., et al. CD36 coordinates NLRP3 inflammasome activation by facilitating intracellular nucleation of soluble ligands into particulate ligands in sterile inflammation. Nat Immunol 14 (2013), 812–820.
63. 63 Arts, R.J., Joosten, L.A., van der Meer, J.W., Netea, M.G., TREM-1: intracellular signaling pathways and interaction with pattern recognition receptors. J Leukoc Biol 93 (2013), 209–215.
64. 64 Weber, C., Zernecke, A., Libby, P., The multifaceted contributions of leukocyte subsets to atherosclerosis: lessons from mouse models. Nat Rev Immunol 8 (2008), 802–815.
65. 65 Ridker, P.M., Howard, C.P., Walter, V., et al. Effects of interleukin-1beta inhibition with canakinumab on hemoglobin A1c, lipids, C-reactive protein, interleukin-6, and fibrinogen: a phase IIb randomized, placebo-controlled trial. Circulation 126 (2012), 2739–2748.
66. 66 Dutta, P., Courties, G., Wei, Y., et al. Myocardial infarction accelerates atherosclerosis. Nature 487 (2012), 325–329.
67. 67 Keeley, E.C., Velez, C.A., O'Neill, W.W., Safian, R.D., Long-term clinical outcome and predictors of major adverse cardiac events after percutaneous interventions on saphenous vein grafts. J Am Coll Cardiol 38 (2001), 659–665.