Regulation of atherosclerotic plaque inflammation

Journal of Internal Medicine

Volumn 278, Issue 5, 2015, Pages 462-482

  Back M ^a,b   Weber, C ^c,d,e   Lutgens, E ^c,d,f,g  

^a KAROLINSKA INSTITUTE   (Sweden)

^b KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^c LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^d DZHK GERMAN CENTRE FOR CARDIOVASCULAR RESEARCH   (Germany)

^e MAASTRICHT UNIVERSITY   (Netherlands)

^f UNIVERSITY OF AMSTERDAM   (Netherlands)

^g ACADEMIC MEDICAL CENTER   (Netherlands)

Author keywords

Chemokines; Costimulatory molecules; Leukotrienes; Lipoxins; Lipoxygenase

Indexed keywords

CHEMOKINE; CHEMOKINE RECEPTOR; CHEMOKINE RECEPTOR ANTAGONIST; CHEMOKINE RECEPTOR CCR1; CHEMOKINE RECEPTOR CCR2; CHEMOKINE RECEPTOR CCR4; CHEMOKINE RECEPTOR CCR5; CHEMOKINE RECEPTOR CCR6; CHEMOKINE RECEPTOR CCR7; CHEMOKINE RECEPTOR CXCR2; CHEMOKINE RECEPTOR CXCR3; CHEMOKINE RECEPTOR CXCR4; CXCL1 CHEMOKINE; CXCL16 CHEMOKINE; CYTOKINE; EPITHELIAL DERIVED NEUTROPHIL ACTIVATING FACTOR 78; FRACTALKINE; GAMMA INTERFERON INDUCIBLE PROTEIN 10; LEUKOTRIENE; LIPOXIN; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 3BETA; MONOCLONAL ANTIBODY; MONOCYTE CHEMOTACTIC PROTEIN 1; N [4 [[[6,7 DIHYDRO 2 (4 METHYLPHENYL) 5H BENZOCYCLOHEPTEN 8 YL]CARBONYL]AMINO]BENZYL] N,N DIMETHYL 2H TETRAHYDROPYRAN 4 AMINIUM CHLORIDE; RANTES; SECONDARY LYMPHOID TISSUE CHEMOKINE; STROMAL CELL DERIVED FACTOR 1; THYMUS AND ACTIVATION REGULATED CHEMOKINE;

ATHEROGENESIS; ATHEROSCLEROTIC PLAQUE; B LYMPHOCYTE; CELL PROLIFERATION; CYTOKINE PRODUCTION; DISEASE CONTROL; DRUG TARGETING; ENDOTHELIAL DYSFUNCTION; EXPERIMENTAL ATHEROSCLEROSIS; GRANULOCYTE; HUMAN; IMMUNOCOMPETENT CELL; INFLAMMATION; LYMPHOCYTE; MONOCYTE; NEUTROPHIL; POSITIVE FEEDBACK; PRIORITY JOURNAL; REVIEW; SMOOTH MUSCLE FIBER; T LYMPHOCYTE; ADAPTIVE IMMUNITY; ANIMAL; CELLULAR IMMUNITY; CLASSIFICATION; IMMUNOLOGY; METABOLISM; PARACRINE SIGNALING; PATHOPHYSIOLOGY; VASCULAR ENDOTHELIUM;

ADAPTIVE IMMUNITY; ANIMALS; CHEMOKINES; ENDOTHELIUM, VASCULAR; HUMANS; IMMUNITY, CELLULAR; INFLAMMATION; LEUKOTRIENES; LIPOXINS; PARACRINE COMMUNICATION; PLAQUE, ATHEROSCLEROTIC; RECEPTORS, CHEMOKINE;

EID: 84944681535     PISSN: 09546820     EISSN: 13652796     Source Type: Journal    
DOI: 10.1111/joim.12367     Document Type: Review

References (177)

1. Murray CJL, Vos T, Lozano R et al. Disability-adjusted life years (DALYs) for 291 diseases and injuries in 21 regions, 1990-2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet 2012; 380: 2197-223.
2. Libby P, Lichtman AH, Hansson GK. Immune effector mechanisms implicated in atherosclerosis: from mice to humans. Immunity 2013; 38: 1092-104.
3. Weber C, Noels H. Atherosclerosis: current pathogenesis and therapeutic options. Nat Med 2011; 17: 1410-22.
4. Legein B, Temmerman L, Biessen EAL, Lutgens E. Inflammation and immune system interactions in atherosclerosis. Cell Mol Life Sci 2013; 70: 3847-69.
5. Cholesterol Treatment Trialists' (CTT) Collaborators, Mihaylova B, Emberson J et al. The effects of lowering LDL cholesterol with statin therapy in people at low risk of vascular disease: meta-analysis of individual data from 27 randomised trials. Lancet 2012; 380: 581-90.
6. Kwak BR, Bäck M, Bochaton-Piallat M-L et al. Biomechanical factors in atherosclerosis: mechanisms and clinical implications†. Eur Heart J 2014; 35: 3013-20.
7. Fogelstrand P, Borén J. Retention of atherogenic lipoproteins in the artery wall and its role in atherogenesis. Nutr Metab Cardiovasc Dis 2012; 22: 1-7.
8. Hansson GK, Hermansson A. The immune system in atherosclerosis. Nat Immunol 2011; 12: 204-12.
9. Ketelhuth DFJ, Bäck M. The role of matrix metalloproteinases in atherothrombosis. Curr Atheroscler Rep 2011; 13: 162-9.
10. Moore KJ, Tabas I. Macrophages in the pathogenesis of atherosclerosis. Cell 2011; 145: 341-55.
11. Gordon S, Martinez FO. Alternative activation of macrophages: mechanism and functions. Immunity 2010; 32: 593-604.
12. Lee S, Huen S, Nishio H et al. Distinct macrophage phenotypes contribute to kidney injury and repair. J Am Soc Nephrol 2011; 22: 317-26.
13. Bouhlel MA, Derudas B, Rigamonti E et al. PPARgamma activation primes human monocytes into alternative M2 macrophages with anti-inflammatory properties. Cell Metab 2007; 6: 137-43.
14. Stöger JL, Gijbels MJJ, van der Velden S et al. Distribution of macrophage polarization markers in human atherosclerosis. Atherosclerosis 2012; 225: 461-8.
15. Waldo SW, Li Y, Buono C et al. Heterogeneity of human macrophages in culture and in atherosclerotic plaques. Am J Pathol 2008; 172: 1112-26.
16. Kadl A, Meher AK, Sharma PR et al. Identification of a novel macrophage phenotype that develops in response to atherogenic phospholipids via Nrf2. Circ Res 2010; 107: 737-46.
17. Gleissner CA, Shaked I, Erbel C, Böckler D, Katus HA, Ley K. CXCL4 downregulates the atheroprotective hemoglobin receptor CD163 in human macrophages. Circ Res 2010; 106: 203-11.
18. Bystrom J, Evans I, Newson J et al. Resolution-phase macrophages possess a unique inflammatory phenotype that is controlled by cAMP. Blood 2008; 112: 4117-27.
19. Smeets E, Meiler S, Lutgens E. Lymphocytic tumor necrosis factor receptor superfamily co-stimulatory molecules in the pathogenesis of atherosclerosis. Curr Opin Lipidol 2013; 24: 518-24.
20. Caligiuri G, Rudling M, Ollivier V et al. Interleukin-10 deficiency increases atherosclerosis, thrombosis, and low-density lipoproteins in apolipoprotein E knockout mice. Mol Med 2003; 9: 10-7.
21. Lutgens E, Gijbels M, Smook M et al. Transforming growth factor-beta mediates balance between inflammation and fibrosis during plaque progression. Arterioscler Thromb Vasc Biol 2002; 22: 975-82.
22. Mallat Z, Besnard S, Duriez M et al. Protective role of interleukin-10 in atherosclerosis. Circ Res 1999; 85: e17-24.
23. Robertson A-KL, Rudling M, Zhou X, Gorelik L, Flavell RA, Hansson GK. Disruption of TGF-beta signaling in T cells accelerates atherosclerosis. J Clin Invest 2003; 112: 1342-50.
24. Lievens D, Habets KL, Robertson A-K et al. Abrogated transforming growth factor beta receptor II (TGFβRII) signalling in dendritic cells promotes immune reactivity of T cells resulting in enhanced atherosclerosis. Eur Heart J 2013; 34: 3717-27.
25. Bäck M, Sultan A, Ovchinnikova O, Hansson GK. 5-Lipoxygenase-activating protein: a potential link between innate and adaptive immunity in atherosclerosis and adipose tissue inflammation. Circ Res 2007; 100: 946-9.
26. Bäck M, Powell WS, Dahlén S-E et al. Update on leukotriene, lipoxin and oxoeicosanoid receptors: IUPHAR Review 7. Br J Pharmacol 2014; 171: 3551-74.
27. Ait-Oufella H, Salomon BL, Potteaux S et al. Natural regulatory T cells control the development of atherosclerosis in mice. Nat Med 2006; 12: 178-80.
28. Klingenberg R, Gerdes N, Badeau RM et al. Depletion of FOXP3 + regulatory T cells promotes hypercholesterolemia and atherosclerosis. J Clin Invest 2013; 123: 1323-34.
29. Ovchinnikova OA, Berge N, Kang C et al. Mycobacterium bovis BCG killed by extended freeze-drying induces an immunoregulatory profile and protects against atherosclerosis. J Intern Med 2014; 275: 49-58.
30. Binder CJ, Hartvigsen K, Chang M-K et al. IL-5 links adaptive and natural immunity specific for epitopes of oxidized LDL and protects from atherosclerosis. J Clin Invest 2004; 114: 427-37.
31. Ait-Oufella H, Herbin O, Bouaziz J-D et al. B cell depletion reduces the development of atherosclerosis in mice. J Exp Med 2010; 207: 1579-87.
32. Houard X, Ollivier V, Louedec L, Michel J-B, Bäck M. Differential inflammatory activity across human abdominal aortic aneurysms reveals neutrophil-derived leukotriene B4 as a major chemotactic factor released from the intraluminal thrombus. FASEB J 2009; 23: 1376-83.
33. Michel J-B, Virmani R, Arbustini E, Pasterkamp G. Intraplaque haemorrhages as the trigger of plaque vulnerability. Eur Heart J 2011; 32: 1977-85-1985a-1985b-1985c.
34. Houard X, Touat Z, Ollivier V et al. Mediators of neutrophil recruitment in human abdominal aortic aneurysms. Cardiovasc Res 2009; 82: 532-41.
35. Drechsler M, Megens RTA, van Zandvoort M, Weber C, Soehnlein O. Hyperlipidemia-triggered neutrophilia promotes early atherosclerosis. Circulation 2010; 122: 1837-45.
36. Leclercq A, Houard X, Philippe M et al. Involvement of intraplaque hemorrhage in atherothrombosis evolution via neutrophil protease enrichment. J Leukoc Biol 2007; 82: 1420-9.
37. Zernecke A, Weber C. Chemokines in atherosclerosis: proceedings resumed. Arterioscler Thromb Vasc Biol 2014; 34: 742-50.
38. Weber C, Zernecke A, Libby P. The multifaceted contributions of leukocyte subsets to atherosclerosis: lessons from mouse models. Nat Rev Immunol 2008; 8: 802-15.
39. Zhou Z, Subramanian P, Sevilmis G et al. Lipoprotein-derived lysophosphatidic acid promotes atherosclerosis by releasing CXCL1 from the endothelium. Cell Metab 2011; 13: 592-600.
40. Tacke F, Alvarez D, Kaplan TJ et al. Monocyte subsets differentially employ CCR2, CCR5, and CX3CR1 to accumulate within atherosclerotic plaques. J Clin Invest 2007; 117: 185-94.
41. Swirski FK, Libby P, Aikawa E et al. Ly-6Chi monocytes dominate hypercholesterolemia-associated monocytosis and give rise to macrophages in atheromata. J Clin Invest 2007; 117: 195-205.
42. Robbins CS, Chudnovskiy A, Rauch PJ et al. Extramedullary hematopoiesis generates Ly-6C(high) monocytes that infiltrate atherosclerotic lesions. Circulation 2012; 125: 364-74.
43. Soehnlein O, Drechsler M, Döring Y et al. Distinct functions of chemokine receptor axes in the atherogenic mobilization and recruitment of classical monocytes. EMBO Mol Med 2013; 5: 471-81.
44. Kennedy A, Gruen ML, Gutierrez DA et al. Impact of macrophage inflammatory protein-1α deficiency on atherosclerotic lesion formation, hepatic steatosis, and adipose tissue expansion. PLoS One 2012; 7: e31508.
45. de Jager SCA, Bot I, Kraaijeveld AO et al. Leukocyte-specific CCL3 deficiency inhibits atherosclerotic lesion development by affecting neutrophil accumulation. Arterioscler Thromb Vasc Biol 2013; 33: e75-83.
46. Braunersreuther V, Zernecke A, Arnaud C et al. Ccr5 but not Ccr1 deficiency reduces development of diet-induced atherosclerosis in mice. Arterioscler Thromb Vasc Biol 2007; 27: 373-9.
47. Zernecke A, Liehn EA, Gao J-L, Kuziel WA, Murphy PM, Weber C. Deficiency in CCR5 but not CCR1 protects against neointima formation in atherosclerosis-prone mice: involvement of IL-10. Blood 2006; 107: 4240-3.
48. Potteaux S, Combadière C, Esposito B et al. Chemokine receptor CCR1 disruption in bone marrow cells enhances atherosclerotic lesion development and inflammation in mice. Mol Med 2005; 11: 16-20.
49. Boring L, Gosling J, Cleary M, Charo IF. Decreased lesion formation in CCR2-/- mice reveals a role for chemokines in the initiation of atherosclerosis. Nature 1998; 394: 894-7.
50. Landsman L, Bar-On L, Zernecke A et al. CX3CR1 is required for monocyte homeostasis and atherogenesis by promoting cell survival. Blood 2009; 113: 963-72.
51. Poupel L, Boissonnas A, Hermand P et al. Pharmacological inhibition of the chemokine receptor, CX3CR1, reduces atherosclerosis in mice. Arterioscler Thromb Vasc Biol 2013; 33: 2297-305.
52. Postea O, Vasina EM, Cauwenberghs S et al. Contribution of platelet CX(3)CR1 to platelet-monocyte complex formation and vascular recruitment during hyperlipidemia. Arterioscler Thromb Vasc Biol 2012; 32: 1186-93.
53. Serbina NV, Pamer EG. Monocyte emigration from bone marrow during bacterial infection requires signals mediated by chemokine receptor CCR2. Nat Immunol 2006; 7: 311-7.
54. Döring Y, Noels H, Mandl M et al. Deficiency of the sialyltransferase St3Gal4 reduces Ccl5-mediated myeloid cell recruitment and arrest: short communication. Circ Res 2014; 114: 976-81.
55. Boisvert WA, Santiago R, Curtiss LK, Terkeltaub RA. A leukocyte homologue of the IL-8 receptor CXCR-2 mediates the accumulation of macrophages in atherosclerotic lesions of LDL receptor-deficient mice. J Clin Invest 1998; 101: 353-63.
56. Boisvert WA, Rose DM, Johnson KA et al. Up-regulated expression of the CXCR2 ligand KC/GRO-alpha in atherosclerotic lesions plays a central role in macrophage accumulation and lesion progression. Am J Pathol 2006; 168: 1385-95.
57. Rousselle A, Qadri F, Leukel L et al. CXCL5 limits macrophage foam cell formation in atherosclerosis. J Clin Invest 2013; 123: 1343-7.
58. Bernhagen J, Krohn R, Lue H et al. MIF is a noncognate ligand of CXC chemokine receptors in inflammatory and atherogenic cell recruitment. Nat Med 2007; 13: 587-96.
59. Manthey HD, Cochain C, Barnsteiner S et al. CCR6 selectively promotes monocyte mediated inflammation and atherogenesis in mice. Thromb Haemost 2013; 110: 1267-77.
60. Wan W, Lim JK, Lionakis MS et al. Genetic deletion of chemokine receptor Ccr6 decreases atherogenesis in ApoE-deficient mice. Circ Res 2011; 109: 374-81.
61. Wan W, Murphy PM. Regulation of atherogenesis by chemokine receptor CCR6. Trends Cardiovasc Med 2011; 21: 140-4.
62. Doran AC, Lipinski MJ, Oldham SN et al. B-cell aortic homing and atheroprotection depend on Id3. Circ Res 2012; 110: e1-12.
63. Trogan E, Feig JE, Dogan S et al. Gene expression changes in foam cells and the role of chemokine receptor CCR7 during atherosclerosis regression in ApoE-deficient mice. Proc Natl Acad Sci USA 2006; 103: 3781-6.
64. Potteaux S, Gautier EL, Hutchison SB et al. Suppressed monocyte recruitment drives macrophage removal from atherosclerotic plaques of Apoe-/- mice during disease regression. J Clin Invest 2011; 121: 2025-36.
65. Wan W, Lionakis MS, Liu Q, Roffê E, Murphy PM. Genetic deletion of chemokine receptor Ccr7 exacerbates atherogenesis in ApoE-deficient mice. Cardiovasc Res 2013; 97: 580-8.
66. Luchtefeld M, Grothusen C, Gagalick A et al. Chemokine receptor 7 knockout attenuates atherosclerotic plaque development. Circulation 2010; 122: 1621-8.
67. Weber C, Meiler S, Döring Y et al. CCL17-expressing dendritic cells drive atherosclerosis by restraining regulatory T cell homeostasis in mice. J Clin Invest 2011; 121: 2898-910.
68. Veillard NR, Steffens S, Pelli G et al. Differential influence of chemokine receptors CCR2 and CXCR3 in development of atherosclerosis in vivo. Circulation 2005; 112: 870-8.
69. Heller EA, Liu E, Tager AM et al. Chemokine CXCL10 promotes atherogenesis by modulating the local balance of effector and regulatory T cells. Circulation 2006; 113: 2301-12.
70. Aslanian AM, Charo IF. Targeted disruption of the scavenger receptor and chemokine CXCL16 accelerates atherosclerosis. Circulation 2006; 114: 583-90.
71. Galkina E, Harry BL, Ludwig A et al. CXCR6 promotes atherosclerosis by supporting T-cell homing, interferon-gamma production, and macrophage accumulation in the aortic wall. Circulation 2007; 116: 1801-11.
72. Zernecke A, Schober A, Bot I et al. SDF-1alpha/CXCR4 axis is instrumental in neointimal hyperplasia and recruitment of smooth muscle progenitor cells. Circ Res 2005; 96: 784-91.
73. Zernecke A, Bot I, Djalali-Talab Y et al. Protective role of CXC receptor 4/CXC ligand 12 unveils the importance of neutrophils in atherosclerosis. Circ Res 2008; 102: 209-17.
74. Zernecke A, Bidzhekov K, Noels H et al. Delivery of microRNA-126 by apoptotic bodies induces CXCL12-dependent vascular protection. Sci Signal 2009; 2: ra81.
75. Schober A, Nazari-Jahantigh M, Wei Y et al. MicroRNA-126-5p promotes endothelial proliferation and limits atherosclerosis by suppressing Dlk1. Nat Med 2014; 20: 368-76.
76. Li X, Zhu M, Penfold ME et al. Activation of CXCR7 limits atherosclerosis and improves hyperlipidemia by increasing cholesterol uptake in adipose tissue. Circulation 2014; 129: 1244-53.
77. Sachais BS, Kuo A, Nassar T et al. Platelet factor 4 binds to low-density lipoprotein receptors and disrupts the endocytic machinery, resulting in retention of low-density lipoprotein on the cell surface. Blood 2002; 99: 3613-22.
78. Koenen RR, von Hundelshausen P, Nesmelova IV et al. Disrupting functional interactions between platelet chemokines inhibits atherosclerosis in hyperlipidemic mice. Nat Med 2009; 15: 97-103.
79. Sohy D, Yano H, de Nadai P et al. Hetero-oligomerization of CCR2, CCR5, and CXCR4 and the protean effects of "selective" antagonists. J Biol Chem 2009; 284: 31270-9.
80. Veillard NR, Kwak B, Pelli G et al. Antagonism of RANTES receptors reduces atherosclerotic plaque formation in mice. Circ Res 2004; 94: 253-61.
81. van Wanrooij EJA, Happé H, Hauer AD et al. HIV entry inhibitor TAK-779 attenuates atherogenesis in low-density lipoprotein receptor-deficient mice. Arterioscler Thromb Vasc Biol 2005; 25: 2642-7.
82. Copin J-C, da Silva RF, Fraga-Silva RA et al. Treatment with Evasin-3 reduces atherosclerotic vulnerability for ischemic stroke, but not brain injury in mice. J Cereb Blood Flow Metab 2013; 33: 490-8.
83. Cipriani S, Francisci D, Mencarelli A et al. Efficacy of the CCR5 antagonist maraviroc in reducing early, ritonavir-induced atherogenesis and advanced plaque progression in mice. Circulation 2013; 127: 2114-24.
84. Gilbert J, Lekstrom-Himes J, Donaldson D et al. Effect of CC chemokine receptor 2 CCR2 blockade on serum C-reactive protein in individuals at atherosclerotic risk and with a single nucleotide polymorphism of the monocyte chemoattractant protein-1 promoter region. Am J Cardiol 2011; 107: 906-11.
85. Rådmark O, Samuelsson B. Regulation of the activity of 5-lipoxygenase, a key enzyme in leukotriene biosynthesis. Biochem Biophys Res Commun 2010; 396: 105-10.
86. Bäck M, Hansson GK. Leukotriene receptors in atherosclerosis. Ann Med 2006; 38: 493-502.
87. Bäck M. Leukotriene signaling in atherosclerosis and ischemia. Cardiovasc Drugs Ther 2009; 23: 41-8.
88. Nagy E, Andersson DC, Caidahl K et al. Upregulation of the 5-lipoxygenase pathway in human aortic valves correlates with severity of stenosis and leads to leukotriene-induced effects on valvular myofibroblasts. Circulation 2011; 123: 1316-25.
89. Bäck M. Inhibitors of the 5-lipoxygenase pathway in atherosclerosis. Curr Pharm Des 2009; 15: 3116-32.
90. Bäck M, Bu D-X, Bränström R, Sheikine Y, Yan Z-Q, Hansson GK. Leukotriene B4 signaling through NF-kappaB-dependent BLT1 receptors on vascular smooth muscle cells in atherosclerosis and intimal hyperplasia. Proc Natl Acad Sci USA 2005; 102: 17501-6.
91. Heller EA, Liu E, Tager AM et al. Inhibition of atherogenesis in BLT1-deficient mice reveals a role for LTB4 and BLT1 in smooth muscle cell recruitment. Circulation 2005; 112: 578-86.
92. Hlawaty H, Jacob M-P, Louedec L et al. Leukotriene receptor antagonism and the prevention of extracellular matrix degradation during atherosclerosis and in-stent stenosis. Arterioscler Thromb Vasc Biol 2009; 29: 518-24.
93. Mueller CFH, Wassmann K, Widder JD et al. Multidrug resistance protein-1 affects oxidative stress, endothelial dysfunction, and atherogenesis via leukotriene C4 export. Circulation 2008; 117: 2912-8.
94. Bäck M. Inflammatory signaling through leukotriene receptors in atherosclerosis. Curr Atheroscler Rep 2008; 10: 244-51.
95. Serhan CN. Pro-resolving lipid mediators are leads for resolution physiology. Nature 2014; 510: 92-101.
96. Brezinski DA, Nesto RW, Serhan CN. Angioplasty triggers intracoronary leukotrienes and lipoxin A4. Impact of aspirin therapy. Circulation 1992; 86: 56-63.
97. Ho KJ, Spite M, Owens CD et al. Aspirin-triggered lipoxin and resolvin E1 modulate vascular smooth muscle phenotype and correlate with peripheral atherosclerosis. Am J Pathol 2010; 177: 2116-23.
98. Van Noolen L, Bäck M, Arnaud C et al. Docosahexaenoic acid supplementation modifies fatty acid incorporation in tissues and prevents hypoxia induced-atherosclerosis progression in apolipoprotein-E deficient mice. Prostaglandins Leukot Essent Fatty Acids 2014; 91: 111-7.
99. Wang H-H, Hung T-M, Wei J, Chiang A-N. Fish oil increases antioxidant enzyme activities in macrophages and reduces atherosclerotic lesions in apoE-knockout mice. Cardiovasc Res 2004; 61: 169-76.
100. Zampolli A, Bysted A, Leth T, Mortensen A, De Caterina R, Falk E. Contrasting effect of fish oil supplementation on the development of atherosclerosis in murine models. Atherosclerosis 2006; 184: 78-85.
101. Stanke-Labesque F, Pépin J-L, Gautier-Veyret E, Levy P, Bäck M. Leukotrienes as a molecular link between obstructive sleep apnoea and atherosclerosis. Cardiovasc Res 2014; 101: 187-93.
102. Ye RD, Boulay F, Wang JM et al. International Union of Basic and Clinical Pharmacology. LXXIII. Nomenclature for the formyl peptide receptor (FPR) family. Pharmacol Rev 2009; 61: 119-61.
103. Edfeldt K, Agerberth B, Rottenberg ME et al. Involvement of the antimicrobial peptide LL-37 in human atherosclerosis. Arterioscler Thromb Vasc Biol 2006; 26: 1551-7.
104. Döring Y, Drechsler M, Wantha S et al. Lack of neutrophil-derived CRAMP reduces atherosclerosis in mice. Circ Res 2012; 110: 1052-6.
105. Petri MH, Laguna-Fernández A, Gonzalez-Diez M, Paulsson-Berne G, Hansson GK, Bäck M. The role of the FPR2/ALX receptor in atherosclerosis development and plaque stability. Cardiovasc Res 2015; 105: 65-75.
106. Drechsler M, de Jong RJ, Rossaint J et al. Annexin A1 counteracts chemokine-induced arterial myeloid cell recruitment. Circ Res 2015; 116: 827-35.
107. Petri MH, Laguna-Fernández A, Tseng C-N, Hedin U, Perretti M, Bäck M. Aspirin-triggered 15-epi-lipoxin A4 signals through FPR2/ALX in vascular smooth muscle cells and protects against intimal hyperplasia after carotid ligation. Int J Cardiol 2015; 179: 370-2.
108. Maderna P, Cottell DC, Toivonen T et al. FPR2/ALX receptor expression and internalization are critical for lipoxin A4 and annexin-derived peptide-stimulated phagocytosis. FASEB J 2010; 24: 4240-9.
109. Hakonarson H, Thorvaldsson S, Helgadottir A et al. Effects of a 5-lipoxygenase-activating protein inhibitor on biomarkers associated with risk of myocardial infarction: a randomized trial. JAMA 2005; 293: 2245-56.
110. Tardif J-C, L'allier PL, Ibrahim R et al. Treatment with 5-lipoxygenase inhibitor VIA-2291 (Atreleuton) in patients with recent acute coronary syndrome. Circ Cardiovasc Imaging 2010; 3: 298-307.
111. Allayee H, Hartiala J, Lee W et al. The effect of montelukast and low-dose theophylline on cardiovascular disease risk factors in asthmatics. Chest 2007; 132: 868-74.
112. Ingelsson E, Yin L, Bäck M. Nationwide cohort study of the leukotriene receptor antagonist montelukast and incident or recurrent cardiovascular disease. J Allergy Clin Immunol 2012; 129: 702-7.
113. Croft M. The role of TNF superfamily members in T-cell function and diseases. Nat Rev Immunol 2009; 9: 271-85.
114. Engel D, Seijkens T, Poggi M et al. The immunobiology of CD154-CD40-TRAF interactions in atherosclerosis. Semin Immunol 2009; 21: 308-12.
115. Lichtman AH, Binder CJ, Tsimikas S, Witztum JL. Adaptive immunity in atherogenesis: new insights and therapeutic approaches. J Clin Invest 2013; 123: 27-36.
116. Chen L, Flies DB. Molecular mechanisms of T cell co-stimulation and co-inhibition. Nat Rev Immunol 2013; 13: 227-42.
117. Dopheide JF, Sester U, Schlitt A et al. Monocyte-derived dendritic cells of patients with coronary artery disease show an increased expression of costimulatory molecules CD40, CD80 and CD86 in vitro. Coron Artery Dis 2007; 18: 523-31.
118. Mantani PT, Ljungcrantz I, Andersson L et al. Circulating CD40 + and CD86 + B cell subsets demonstrate opposing associations with risk of stroke. Arterioscler Thromb Vasc Biol 2014; 34: 211-8.
119. Müller A, Mu L, Meletta R et al. Towards non-invasive imaging of vulnerable atherosclerotic plaques by targeting co-stimulatory molecules. Int J Cardiol 2014; 174: 503-15.
120. Buono C, Pang H, Uchida Y, Libby P, Sharpe AH, Lichtman AH. B7-1/B7-2 costimulation regulates plaque antigen-specific T-cell responses and atherogenesis in low-density lipoprotein receptor-deficient mice. Circulation 2004; 109: 2009-15.
121. Afek A, Harats D, Roth A, Keren G, George J. A functional role for inducible costimulator (ICOS) in atherosclerosis. Atherosclerosis 2005; 183: 57-63.
122. Gotsman I, Grabie N, Gupta R et al. Impaired regulatory T-cell response and enhanced atherosclerosis in the absence of inducible costimulatory molecule. Circulation 2006; 114: 2047-55.
123. Ewing MM, Karper JC, Abdul S et al. T-cell co-stimulation by CD28-CD80/86 and its negative regulator CTLA-4 strongly influence accelerated atherosclerosis development. Int J Cardiol 2013; 168: 1965-74.
124. Ma K, Lv S, Liu B et al. CTLA4-IgG ameliorates homocysteine-accelerated atherosclerosis by inhibiting T-cell overactivation in apoE(-/-) mice. Cardiovasc Res 2013; 97: 349-59.
125. Gotsman I, Grabie N, Dacosta R, Sukhova G, Sharpe A, Lichtman AH. Proatherogenic immune responses are regulated by the PD-1/PD-L pathway in mice. J Clin Invest 2007; 117: 2974-82.
126. Bu D-X, Tarrio M, Maganto-Garcia E et al. Impairment of the programmed cell death-1 pathway increases atherosclerotic lesion development and inflammation. Arterioscler Thromb Vasc Biol 2011; 31: 1100-7.
127. Cochain C, Chaudhari SM, Koch M, Wiendl H, Eckstein H-H, Zernecke A. Programmed cell death-1 deficiency exacerbates T cell activation and atherogenesis despite expansion of regulatory T cells in atherosclerosis-prone mice. PLoS One 2014; 9: e93280.
128. Lievens D, Eijgelaar WJ, Biessen EAL, Daemen MJAP, Lutgens E. The multi-functionality of CD40L and its receptor CD40 in atherosclerosis. Thromb Haemost 2009; 102: 206-14.
129. Seijkens T, Engel D, Tjwa M, Lutgens E. The role of CD154 in haematopoietic development. Thromb Haemost 2010; 104: 693-701.
130. Bishop GA, Moore CR, Xie P, Stunz LL, Kraus ZJ. TRAF proteins in CD40 signaling. Adv Exp Med Biol 2007; 597: 131-51.
131. Aukrust P, Müller F, Ueland T et al. Enhanced levels of soluble and membrane-bound CD40 ligand in patients with unstable angina. Possible reflection of T lymphocyte and platelet involvement in the pathogenesis of acute coronary syndromes. Circulation 1999; 100: 614-20.
132. Leroyer AS, Rautou P-E, Silvestre J-S et al. CD40 ligand+ microparticles from human atherosclerotic plaques stimulate endothelial proliferation and angiogenesis a potential mechanism for intraplaque neovascularization. J Am Coll Cardiol 2008; 52: 1302-11.
133. Lutgens E, Gorelik L, Daemen MJ et al. Requirement for CD154 in the progression of atherosclerosis. Nat Med 1999; 5: 1313-6.
134. Lutgens E, Cleutjens KB, Heeneman S, Koteliansky VE, Burkly LC, Daemen MJ. Both early and delayed anti-CD40L antibody treatment induces a stable plaque phenotype. Proc Natl Acad Sci USA 2000; 97: 7464-9.
135. Mach F, Schönbeck U, Sukhova GK, Atkinson E, Libby P. Reduction of atherosclerosis in mice by inhibition of CD40 signalling. Nature 1998; 394: 200-3.
136. Schönbeck U, Sukhova GK, Shimizu K, Mach F, Libby P. Inhibition of CD40 signaling limits evolution of established atherosclerosis in mice. Proc Natl Acad Sci USA 2000; 97: 7458-63.
137. Donners MMPC, Beckers L, Lievens D et al. The CD40-TRAF6 axis is the key regulator of the CD40/CD40L system in neointima formation and arterial remodeling. Blood 2008; 111: 4596-604.
138. Willecke F, Tiwari S, Rupprecht B et al. Interruption of classic CD40L-CD40 signalling but not of the novel CD40L-Mac-1 interaction limits arterial neointima formation in mice. Thromb Haemost 2014; 112: 379-89.
139. Smook MLF, van Leeuwen M, Heeringa P et al. Anti-oxLDL antibody isotype levels, as potential markers for progressive atherosclerosis in APOE and APOECD40L mice. Clin Exp Immunol 2008; 154: 264-9.
140. Bavendiek U, Zirlik A, LaClair S, MacFarlane L, Libby P, Schönbeck U. Atherogenesis in mice does not require CD40 ligand from bone marrow-derived cells. Arterioscler Thromb Vasc Biol 2005; 25: 1244-9.
141. Lievens D, Zernecke A, Seijkens T et al. Platelet CD40L mediates thrombotic and inflammatory processes in atherosclerosis. Blood 2010; 116: 4317-27.
142. Lutgens E, Lievens D, Beckers L et al. Deficient CD40-TRAF6 signaling in leukocytes prevents atherosclerosis by skewing the immune response toward an antiinflammatory profile. J Exp Med 2010; 207: 391-404.
143. Zirlik A, Maier C, Gerdes N et al. CD40 ligand mediates inflammation independently of CD40 by interaction with Mac-1. Circulation 2007; 115: 1571-80.
144. Missiou A, Köstlin N, Varo N et al. Tumor necrosis factor receptor-associated factor 1 (TRAF1) deficiency attenuates atherosclerosis in mice by impairing monocyte recruitment to the vessel wall. Circulation 2010; 121: 2033-44.
145. Missiou A, Rudolf P, Stachon P et al. TRAF5 deficiency accelerates atherogenesis in mice by increasing inflammatory cell recruitment and foam cell formation. Circ Res 2010; 107: 757-66.
146. Stachon P, Missiou A, Walter C et al. Tumor necrosis factor receptor associated factor 6 is not required for atherogenesis in mice and does not associate with atherosclerosis in humans. PLoS One 2010; 5: e11589.
147. Polykratis A, van Loo G, Xanthoulea S, Hellmich M, Pasparakis M. Conditional targeting of tumor necrosis factor receptor-associated factor 6 reveals opposing functions of Toll-like receptor signaling in endothelial and myeloid cells in a mouse model of atherosclerosis. Circulation 2012; 126: 1739-51.
148. Ahonen C, Manning E, Erickson LD et al. The CD40-TRAF6 axis controls affinity maturation and the generation of long-lived plasma cells. Nat Immunol 2002; 3: 451-6.
149. Song Z, Jin R, Yu S et al. CD40 is essential in the upregulation of TRAF proteins and NF-kappaB-dependent proinflammatory gene expression after arterial injury. PLoS One 2011; 6: e23239.
150. Song Z, Jin R, Yu S, Nanda A, Granger DN, Li G. Crucial role of CD40 signaling in vascular wall cells in neointimal formation and vascular remodeling after vascular interventions. Arterioscler Thromb Vasc Biol 2012; 32: 50-64.
151. Zarzycka B, Seijkens T, Nabuurs S et al. Discovery of small molecule CD40-TRAF6 inhibitors. J Chem Inf Mod 2015; 55: 294-307.
152. Chatzigeorgiou A, Seijkens T, Zarzycka B et al. Blocking CD40-TRAF6 signaling is a therapeutic target in obesity-associated insulin resistance. Proc Natl Acad Sci USA 2014; 111: 2686-91.
153. van den Berg SM, Seijkens TTP, Kusters PJH et al. Blocking CD40-Traf6 interactions by small molecule inhibitor 6860766 ameliorates the complications of diet induced obesity in mice. Int J Obes (Lond) 2015; doi: 10.1038/ijo.2014.198. [Epub ahead of print].
154. Wang X, Ria M, Kelmenson PM et al. Positional identification of TNFSF4, encoding OX40 ligand, as a gene that influences atherosclerosis susceptibility. Nat Genet 2005; 37: 365-72.
155. van Wanrooij EJA, van Puijvelde GHM, de Vos P, Yagita H, van Berkel TJC, Kuiper J. Interruption of the Tnfrsf4/Tnfsf4 (OX40/OX40L) pathway attenuates atherogenesis in low-density lipoprotein receptor-deficient mice. Arterioscler Thromb Vasc Biol 2007; 27: 204-10.
156. Foks AC, van Puijvelde GHM, Bot I et al. Interruption of the OX40-OX40 ligand pathway in LDL receptor-deficient mice causes regression of atherosclerosis. J Immunol 2013; 191: 4573-80.
157. Jeon HJ, Choi J-H, Jung I-H et al. CD137 (4-1BB) deficiency reduces atherosclerosis in hyperlipidemic mice. Circulation 2010; 121: 1124-33.
158. Olofsson PS, Söderström LA, Wågsäter D et al. CD137 is expressed in human atherosclerosis and promotes development of plaque inflammation in hypercholesterolemic mice. Circulation 2008; 117: 1292-301.
159. Foks AC, Bot I, Frodermann V et al. Interference of the CD30-CD30L pathway reduces atherosclerosis development. Arterioscler Thromb Vasc Biol 2012; 32: 2862-8.
160. Moreland L, Bate G, Kirkpatrick P. Abatacept. Nat Rev Drug Discov 2006; 5: 185-6.
161. Genovese MC, Becker J-C, Schiff M et al. Abatacept for rheumatoid arthritis refractory to tumor necrosis factor alpha inhibition. N Engl J Med 2005; 353: 1114-23.
162. Vincenti F, Dritselis A, Kirkpatrick P. Belatacept. Nat Rev Drug Discovery 2011; 10: 655-6.
163. ® reduces lipopolysaccharide-mediated inflammation in human atherosclerotic lesions. Drug Des Devel Ther 2014; 8: 447-57.
164. Sugamura K, Ishii N, Weinberg AD. Therapeutic targeting of the effector T-cell co-stimulatory molecule OX40. Nat Rev Immunol 2004; 4: 420-31.
165. Peters AL, Stunz LL, Bishop GA. CD40 and autoimmunity: the dark side of a great activator. Semin Immunol 2009; 21: 293-300.
166. Liossis S-NC, Sfikakis PP. Costimulation blockade in the treatment of rheumatic diseases. BioDrugs 2004; 18: 95-102.
167. Kanmaz T, Fechner JJH, Torrealba J et al. Monotherapy with the novel human anti-CD154 monoclonal antibody ABI793 in rhesus monkey renal transplantation model. Transplantation 2004; 77: 914-20.
168. André P, Prasad KSS, Denis CV et al. CD40L stabilizes arterial thrombi by a beta3 integrin-dependent mechanism. Nat Med 2002; 8: 247-52.
169. Kasran A, Boon L, Wortel CH et al. Safety and tolerability of antagonist anti-human CD40 Mab ch5D12 in patients with moderate to severe Crohn's disease. Aliment Pharmacol Ther 2005; 22: 111-22.
170. Beatty GL, Torigian DA, Chiorean EG et al. A phase I study of an agonist CD40 monoclonal antibody (CP-870, 893) in combination with gemcitabine in patients with advanced pancreatic ductal adenocarcinoma. Clin Cancer Res 2013; 19: 6286-95.
171. Beatty GL, Chiorean EG, Fishman MP et al. CD40 agonists alter tumor stroma and show efficacy against pancreatic carcinoma in mice and humans. Science 2011; 331: 1612-6.
172. Hassan SB, Sørensen JF, Olsen BN, Pedersen AE. Anti-CD40-mediated cancer immunotherapy: an update of recent and ongoing clinical trials. Immunopharmacol Immunotoxicol 2014; 36: 96-104.
173. de Vos S, Forero-Torres A, Ansell SM et al. A phase II study of dacetuzumab (SGN-40) in patients with relapsed diffuse large B-cell lymphoma (DLBCL) and correlative analyses of patient-specific factors. J Hematol Oncol 2014; 7: 44.
174. Byrd JC, Kipps TJ, Flinn IW et al. Phase I study of the anti-CD40 humanized monoclonal antibody lucatumumab (HCD122) in relapsed chronic lymphocytic leukemia. Leuk Lymphoma 2012; 53: 2136-42.
175. Bensinger W, Maziarz RT, Jagannath S et al. A phase 1 study of lucatumumab, a fully human anti-CD40 antagonist monoclonal antibody administered intravenously to patients with relapsed or refractory multiple myeloma. Br J Haematol 2012; 159: 58-66.
176. Fanale M, Assouline S, Kuruvilla J et al. Phase IA/II, multicentre, open-label study of the CD40 antagonistic monoclonal antibody lucatumumab in adult patients with advanced non-Hodgkin or Hodgkin lymphoma. Br J Haematol 2014; 164: 258-65.
177. Akhtar S, Gremse F, Kiessling F, Weber C, Schober A. CXCL12 promotes the stabilization of atherosclerotic lesions mediated by smooth muscle progenitor cells in Apoe-deficient mice. Arterioscler Thromb Vasc Biol 2013; 33: 679-86.