Update on selective treatments targeting neutrophilic inflammation in atherogenesis and atherothrombosis

Thrombosis and Haemostasis

Volumn 111, Issue 4, 2013, Pages 634-646

  Gomes Quinderé, Ana Luíza ^a   Barros Benevides, Norma Maria ^b   Carbone, Federico ^c,d   Mach, François ^c   Vuilleumier, Nicolas ^e   Montecucco, Fabrizio ^d,e  

^a MINISTRY OF EDUCATION OF BRAZIL   (Brazil)

^b FEDERAL UNIVERSITY OF CEARÁ   (Brazil)

^c UNIVERSITY OF GENEVA   (Switzerland)

^d UNIVERSITY OF GENOA   (Italy)

^e GENEVA UNIVERSITY HOSPITALS   (Switzerland)

Author keywords

Atherosclerosis; Inflammation; Neutrophil

Indexed keywords

1 DEOXY 3 (1, 1 DIMETHYLBUTYL) DELTA8 TETRAHYDROCANNABINOL; 3 [3 [[2 CHLORO 3 (TRIFLUOROMETHYL) BENZYL] (2 DIPHENYLETHYL) AMINO] PROPOXY] PHENYLACETIC ACID; CALGRANULIN A; CALGRANULIN B; CARBOXYETHYLGERMANIUM SESQUIOXIDE; CHEMOKINE RECEPTOR CCR1; CHEMOKINE RECEPTOR CCR2; CHEMOKINE RECEPTOR CCR2 ANTAGONIST; CHEMOKINE RECEPTOR CCR5; CHEMOKINE RECEPTOR CCR5 ANTAGONIST; CHEMOKINE RECEPTOR CXCR2; INCLACUMAB; INTERCELLULAR ADHESION MOLECULE 1; MARAVIROC; N [4 [[[6, 7 DIHYDRO 2 (4 METHYLPHENYL) 5H BENZOCYCLOHEPTEN 8 YL] CARBONYL] AMINO] BENZYL] N, N DIMETHYL 2H TETRAHYDROPYRAN 4 AMINIUM CHLORIDE; N [4 [[[6,7 DIHYDRO 2 (4 METHYLPHENYL) 5H BENZOCYCLOHEPTEN 8 YL]CARBONYL]AMINO]BENZYL] N,N DIMETHYL 2H TETRAHYDROPYRAN 4 AMINIUM CHLORIDE; NEUTROPHIL COLLAGENASE; PLERIXAFOR; TLK 19705; UNCLASSIFIED DRUG; VASCULAR CELL ADHESION MOLECULE 1; CELL ADHESION MOLECULE; CHEMOKINE; CHEMOKINE RECEPTOR; MONOCLONAL ANTIBODY;

ATHEROGENESIS; CARDIOVASCULAR RISK; CELL ADHESION; GRANULOPOIESIS; HUMAN; HYPERCOAGULABILITY; HYPERGLYCEMIA; HYPERLIPIDEMIA; IMMUNE RESPONSE; INFLAMMATION; NEUTROPHIL; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REVIEW; THROMBOSIS; VULNERABLE POPULATION; ANIMAL; ATHEROSCLEROSIS; CLINICAL TRIAL (TOPIC); DRUG EFFECTS; DRUG SCREENING; IMMUNOLOGY; MOLECULARLY TARGETED THERAPY; NEUTROPHIL CHEMOTAXIS;

ANIMALS; ANTIBODIES, MONOCLONAL; ATHEROSCLEROSIS; CELL ADHESION MOLECULES; CHEMOKINES; CLINICAL TRIALS AS TOPIC; DRUG EVALUATION, PRECLINICAL; HUMANS; INFLAMMATION; MOLECULAR TARGETED THERAPY; NEUTROPHIL INFILTRATION; NEUTROPHILS; RECEPTORS, CHEMOKINE; THROMBOSIS;

EID: 84897506229     PISSN: 03406245     EISSN: None     Source Type: Journal    
DOI: 10.1160/TH13-08-0712     Document Type: Review

References (127)

1. Roger VL, Go AS, Lloyd-Jones DM, et al. Heart disease and stroke statistics: 2012 update: a report from the American Heart Association. Circulation 2012; 125: e2-e220.
2. Galkina E, Ley K. Immune and inflammatory mechanisms of atherosclerosis. Annu Rev Immunol 2009; 27: 165-197.
3. Hansson GK, Hermansson A. The immune system in atherosclerosis. Nat Immunol 2011; 12: 204-212.
4. Libby P, Ridker PM, Hansson GK. Progress and challenges in translating the biology of atherosclerosis. Nature 2011; 473: 317-325.
5. Soehnlein O. Multiple Roles for Neutrophils in Atherosclerosis. Circ Res 2012; 110: 875-888.
6. Berman JP, Farkouh ME, Rosenson R. Emerging anti-inflammatory drugs for atherosclerosis. Expert Opin Emerg Drugs 2013; 18: 193-205.
7. Koenen RR, Weber C. Therapeutic targeting of chemokines interactions in atherosclerosis. Nat Rev Drug Discov 2010; 9: 141-153.
8. Weber C, Noels H. Atherosclerosis: current pathogenesis and therapeutic options. Nat Med 2011; 17: 1410-1422.
9. Kolaczkowsk E, Kubes P. Neutrophil recruitment and function in health and inflammation. Nat Rev Immunol 2013; 13: 159-175.
10. Mantovani A, Cassatella MA, Costantini C, et al. Neutrophils in the activation and regulation of innate and adaptive immunity. Nat Rev Immunol 2011; 11: 519-531.
11. Borregaard N, Sørensen OE, Theilgaard-Mönch K. Neutrophil granules: a library of innate immunity proteins. Trends Immunol 2007; 28: 340-345.
12. Kougias P, Chai H, Lin PH, et al. Defensins and cathelicidins: neutrophil peptides with roles in inflammation, hyperlipidemia and atherosclerosis. J Cell Mol Med 2005; 9: 3-10.
13. Dyugovskaya L, Polyakov A, Ginsberg D, et al. Molecular pathways of spontaneous and TNF-{alpha}-mediated neutrophil apoptosis under intermittent hypoxia. Am J Respir Cell Mol Biol 2011; 45: 154-162.
14. El Kebir D, József L, Pan W, et al. Myeloperoxidase delays neutrophil apoptosis through CD11b/CD18 integrins and prolongs inflammation. Circ Res 2008; 103: 352-359.
15. Garlichs CD, Eskafi S, Cicha I, et al. Delay of neutrophil apoptosis in acute coronary syndromes. J Leukoc Biol 2004; 75: 828-835.
16. Jaillon S, Galdiero MR, Del Prete D, et al. Neutrophils in innate and adaptive immunity. Semin Immunopathol 2013; 35: 377-394.
17. Montecucco F, Lenglet S, Gayet-Ageron A, et al. Systemic and intraplaque mediators of inflammation are increased in patients symptomatic for ischaemic stroke. Stroke 2010; 41: 1394-1404.
18. Guasti L, Dentali F, Castiglioni L, et al. Neutrophils and clinical outcomes in patients with acute coronary syndromes and/or cardiac revascularization. A systematic review on more than 34,000 subjects. Thromb Haemost 2011; 106: 591-599.
19. Baetta R, Corsini A. Role of polymorphonuclear neutrophils in atherosclerosis: current state and future perspectives. Atherosclerosis 2010; 210: 1-13.
20. Naruko T, Ueda M, Haze K, et al. Neutrophil infiltration of culprit lesions in acute coronary syndromes. Circulation 2002; 106: 2894-2900.
21. Döring Y, Soehnlein O, Drechsler M, et al. Hematopoietic interferon regulatory factor 8-deficiency accelerates atherosclerosis in mice. Arterioscler Thromb Vasc Biol 2012; 32: 1613-1623.
22. 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: 209-217.
23. 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.
24. Soehnlein O, Zernecke A, Eriksson EE, et al. Neutrophil secretion products pave the way for inflammatory monocytes. Blood 2008; 112: 1461-1471.
25. Döring Y, Drechsler M, Wantha S, et al. Lack of neutrophil-derived CRAMP reduces atherosclerosis in mice. Circ Res 2012; 110: 1052-1056.
26. Wantha S, Alard JE, Megens RT, et al. Neutrophil-derived cathelicidin promotes adhesion of classical monocytes. Circ Res 2013; 112: 792-801.
27. Soehnlein O, Wantha S, Simsekyilmaz S, et al. Neutrophil-derived cathelicidin protects from neointimal hyperplasia. Sci Transl Med 2011; 3: 103ra98.
28. Soehnlein O, Swirski FK. Hypercholesterolemia links hematopoiesis with atherosclerosis. Trends Endocrinol Metab 2013; 24: 129-136.
29. Drechsler M, Megens RT, van Zandvoort M, et al. Hyperlipidemia-triggered neutrophilia promotes early atherosclerosis. Circulation 2010; 122: 1837-1845.
30. Rotzius P, Thams S, Soehnlein O, et al. Distinct infiltration of neutrophils in lesion shoulders in ApoE-/-mice. Am J Pathol 2010; 177: 493-500.
31. Alipour A, van Oostrom AJ, Izraeljan A, et al. Leukocyte activation by triglyceride-rich lipoproteins. Arterioscler Thromb Vasc Biol 2008; 28: 792-797.
32. van Oostrom AJ, Plokker HW, van Asbeck BS, et al. Effects of rosuvastatin on postprandial leukocytes in mildly hyperlipidemic patients with premature coronary sclerosis. Atherosclerosis 2006; 185: 331-339.
33. Mazor R, Shurtz-Swirski R, Farah R, et al. Primed polymorphonuclear leukocytes constitute a possible link between inflammation and oxidative stress in hyperlipidemic patients. Atherosclerosis 2008; 197: 937-943.
34. Croce K, Gao H, Wang Y, et al. Myeloid-related protein-8/14 is critical for the biological response to vascular injury. Circulation 2009; 120: 427-436.
35. Nagareddy PR, Murphy AJ, Stirzaker RA, et al. Hyperglycemia promotes myelopoiesis and impairs the resolution of atherosclerosis. Cell Metab 2013; 17: 695-708.
36. Ghasemzadeh M, Hosseini E. Platelet-leukocyte crosstalk: Linking proinflammatory responses to procoagulant state. Thromb Res 2013; 131: 191-197.
37. Massberg S, Grahl L, von Bruehl ML, et al. Reciprocal coupling of coagulation and innate immunity via neutrophil serine proteases. Nat Med 2010; 16: 887-896.
38. Borissoff JI, Otten JJ, Heeneman S, et al. Genetic and pharmacological modifications of thrombin formation in apolipoprotein e-deficient mice determine atherosclerosis severity and atherothrombosis onset in a neutrophil-dependent manner. PLoS One 2013; 8: e55784.
39. Megens RT, Vijayan S, Lievens D, et al. Presence of luminal neutrophil extracellular traps in atherosclerosis. Thromb Haemost 2012; 107: 597-598.
40. de Boer OJ, Li X, Teeling P, et al. Neutrophils, neutrophil extracellular traps and interleukin-17 associate with the organisation of thrombi in acute myocardial infarction. Thromb Haemost 2013; 109: 290-297.
41. Timár CI, Lorincz AM, Ligeti E. Changing world of neutrophils. Pflugers Arch 2013; Epub ahead of print.
42. Branzk N, Papayannopoulos V. Molecular mechanisms regulating NETosis in infection and disease. Semin Immunopathol 2013; 35: 513-530.
43. Drechsler M, Döring Y, Megens RT, et al. Neutrophilic granulocytes-promiscuous accelerators of atherosclerosis. Thromb Haemost 2011; 106: 839-848.
44. Bradley MN, Hong C, Chen M, et al. Ligand activation of LXR beta reverses atherosclerosis and cellular cholesterol overload in mice lacking LXR alpha and apoE. J Clin Invest 2007; 117: 2337-2346.
45. Montecucco F, Di Marzo V, da Silva RF, et al. The activation of the cannabinoid receptor type 2 reduces neutrophilic protease-mediated vulnerability in atherosclerotic plaques. Eur Heart J 2012; 33: 846-856.
46. Charo IF, Taub R. Anti-inflammatory therapeutics for the treatment of atherosclerosis. Nat Rev Drug Discov 2011; 10: 365-376.
47. Björkbacka H, Fredrikson GN, Nilsson J. Emerging biomarkers and intervention targets for immune-modulation of atherosclerosis-a review of the experimental evidence. Atherosclerosis 2013; 227: 9-17.
48. Wolf D, Hohmann JD, Wiedemann A, et al. Binding of CD40L to Mac-1's I-domain involves the EQLKKSKTL motif and mediates leukocyte recruitment and atherosclerosis--but does not affect immunity and thrombosis in mice. Circ Res 2011; 109: 1269-1279.
49. Park JG, Ryu SY, Jung IH, et al. Evaluation of VCAM-1 antibodies as therapeutic agent for atherosclerosis in apolipoprotein E-deficient mice. Atherosclerosis 2013; 226: 356-363.
50. Briz V, Poveda E, Soriano V. HIV entry inhibitors: mechanisms of action and resistance pathways. J Antimicrob Chemother 2006; 57: 619-627.
51. van Wanrooij EJ, 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: 2642-2647.
52. Veillard NR, Kwak B, Pelli G, et al. Antagonism of RANTES receptors reduces atherosclerotic plaque formation in mice. Circ Res 2004; 94: 253-261.
53. Jubeli E, Moine L, Vergnaud-Gauduchon J, et al. E-selectin as a target for drug delivery and molecular imaging. J Control Release 2012; 158: 194-206.
54. 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.
55. 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: 906-911.
56. Okamoto M, Fuchigami M, Suzuki T, et al. A novel C-C chemokine receptor 2 antagonist prevents progression of albuminuria and atherosclerosis in mouse models. Biol Pharm Bull 2012; 35: 2069-2074.
57. Yamashita T, Kawashima S, Ozaki M, et al. Propagermanium reduces atherosclerosis in apolipoprotein E knockout mice via inhibition of macrophage infiltration. Arterioscler Thromb Vasc Biol 2002; 22: 969-974.
58. Koenen RR, Weber C. Chemokines: established and novel targets in atherosclerosis. EMBO Mol Med 2011; 3: 713-725.
59. 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: 2114-2124.
60. Copin JC, da Silva RF, Fraga-Silva RA, et al. Treatment with Evasin-3 reduces atherosclerotic vulnerability for ischaemic stroke, but not brain injury in mice. J Cereb Blood Flow Metab 2013; 33: 490-498.
61. Montecucco F, Lenglet S, Braunersreuther V, et al. Single administration of the CXC chemokine-binding protein Evasin-3 during ischaemia prevents myocardial reperfusion injury in mice. Arterioscler Thromb Vasc Biol 2010; 30: 1371-1377.
62. Levin N, Bischoff ED, Daige CL, et al. Macrophage liver X receptor is required for antiatherogenic activity of LXR agonists. Arterioscler Thromb Vasc Biol 2005; 25: 135-142.
63. Katz A, Udata C, Ott E, et al. Safety, pharmacokinetics, and pharmacodynamics of single doses of LXR-623, a novel liver X-receptor agonist, in healthy participants. J Clin Pharmacol 2009; 49: 643-649.
64. Quinet EM, Basso MD, Halpern AR, et al. LXR ligand lowers LDL cholesterol in primates, is lipid neutral in hamster, and reduces atherosclerosis in mouse. J Lipid Res 2009; 50: 2358-2370.
65. Giannarelli C, Cimmino G, Connolly TM, et al. Synergistic effect of liver X receptor activation and simvastatin on plaque regression and stabilization: an magnetic resonance imaging study in a model of advanced atherosclerosis. Eur Heart J 2012; 33: 264-273.
66. Kling D, Stucki C, Kronenberg S, et al. Pharmacological control of platelet-leukocyte interactions by the human anti-P-selectin antibody inclacumab-preclinical and clinical studies. Thromb Res 2013; 131: 401-410.
67. Barthel SR, Gavino JD, Descheny L, Dimitroff CJ. Targeting selectins and selectin ligands in inflammation and cancer. Expert Opin Ther Targets 2007; 11: 1473-1491.
68. Rozenberg I, Sluka SH, Mocharla P, et al. Deletion of L-selectin increases atherosclerosis development in ApoE-/-mice. PLoS One 2011; 6: e21675.
69. Ludwig RJ, Schön MP, Boehncke WH. P-selectin: a common therapeutic target for cardiovascular disorders, inflammation and tumour metastasis. Expert Opin Ther Targets 2007; 11: 1103-1117.
70. Wedepohl S, Beceren-Braun F, Riese S, et al. L-Selectin-A dynamic regulator of leukocyte migration. Eur J Cell Biol 2012; 91: 257-264.
71. Johnson-Tidey RR, McGregor JL, Taylor PR, et al. Increase in the adhesion molecule P-selectin in endothelium overlying atherosclerotic plaques. Coexpression with intercellular adhesion molecule-1. Am J Pathol 1994; 144: 952-961.
72. Molenaar TJM, Twisk J, de Haas SAM, et al. P-selectin as a candidate target in atherosclerosis. Biochem Pharmacol 2003; 66: 859-866.
73. Bourdillon MC, Randon J, Barek L, et al. Reduced atherosclerotic lesion size in P-selectin deficient apolipoprotein E-knockout mice fed a chow but not a fat diet. J Biomed Biotechnol 2006; 2006: 49193.
74. Dong ZM, Chapman SM, Brown AA, et al. The combined role of P-and E-selectins in atherosclerosis. J Clin Invest 1998; 102: 145-152.
75. van Leeuwen M, Gijbels MJ, Duijvestijn A, et al. Accumulation of myeloperoxidase-positive neutrophils in atherosclerotic lesions in LDLR-/-mice. Arterioscler Thromb Vasc Biol 2008; 28: 84-89.
76. Huo Y, Xia L. P-selectin glycoprotein ligand-1 plays a crucial role in the selective recruitment of leukocytes into the atherosclerotic arterial wall. Trends Cardiovasc Med 2009; 19: 140-145.
77. Japp AG, Chelliah R, Tattersall L, et al. Effect of PSI-697, a novel P-selectin inhibitor, on platelet-monocyte aggregate formation in humans. J Am Heart Assoc 2013; 2: e006007.
78. Cerletti C, Tamburrelli C, Izzi B, et al. Platelet-leukocyte interactions in thrombosis. Thromb Res 2012; 129: 263-266.
79. Patko Z, Csaszar A, Acsady G, et al. Roles of Mac-1 and glycoprotein IIb/IIIaintegrins in leukocyte-platelet aggregate formation: stabilization by Mac-1 and inhibition by GpIIb/IIIa blockers. Platelets 2012; 23: 368-375.
80. Luo W, Wang H, Öhman MK, et al. P-selectin glycoprotein ligand-1 deficiency leads to cytokine resistance and protection against atherosclerosis in apolipoprotein E deficient mice. Atherosclerosis 2012; 220: 110-117.
81. Duchatelle V, Kritikou EA, Tardif JC. Clinical value of drugs targeting inflammation for the management of coronary artery disease. Can J Cardiol 2012; 28: 678-686.
82. Phillips JW, Barringhaus KG, Sanders JM, et al. Single injection of P-selectin or P-selectin glycoprotein ligand-1 monoclonal antibody blocks neointima formation after arterial injury in apolipoprotein E-deficient mice. Circulation 2003; 107: 2244-2249.
83. Høye AM, Couchman JR, Wewer UM, et al. The newcomer in the integrin family: integrin α9 in biology and cancer. Adv Biol Regul 2012; 52: 326-339.
84. Hajishengallis G, Chavakis T. Endogenous modulators of inflammatory cell recruitment. Trends Immunol 2013; 34: 1-6.
85. Park JG, Ryu SY, Jung IH, et al. Evaluation of VCAM-1 antibodies as therapeutic agent for atherosclerosis in apolipoprotein E-deficient mice. Atherosclerosis 2013; 226: 356-363.
86. Iiyama K, Hajra L, Iiyama M, et al. Patterns of vascular cell adhesion molecule-1 and intercellular adhesion molecule-1 expression in rabbit and mouse atherosclerotic lesions and at sites predisposed to lesion formation. Circ Res 1999; 85: 199-207.
87. Lomakina EB, Waugh RE. Adhesion between human neutrophils and immobilized endothelial ligand vascular cell adhesion molecule 1: divalent ion effects. Biophys J 2009; 96: 276-284.
88. Pick R, Brechtefeld D, Walzog B. Intraluminal crawling versus interstitial neutrophil migration during inflammation. Mol Immunol 2013; 55: 70-75.
89. Zirlik A, Maier C, Gerdes N, et al. CD40 ligand mediates inflammation independently of CD40 by interaction with Mac-1. Circulation 2007; 115: 1571-1580.
90. Hassan GS, Merhi Y, Mourad W. CD40 ligand: a neo-inflammatory molecule in vascular diseases. Immunobiology 2012; 217: 521-532.
91. Cybulsky MI, Iiyama K, Li H, et al. A major role for VCAM-1, but not ICAM-1, in early atherosclerosis. J Clin Invest 2001; 107: 1255-1262.
92. Blanchet X, Langer M, Weber C, et al. Touch of chemokines. Front Immunol 2012; 3: 175.
93. Grommes J, Alard JE, Drechsler M, et al. Disruption of platelet-derived chemokine heteromers prevents neutrophil extravasation in acute lung injury. Am J Respir Crit Care Med 2012; 185: 628-636.
94. Grommes J, Drechsler M, Soehnlein O. CCR5 and FPR1 Mediate Neutrophil Recruitment in Endotoxin-Induced Lung Injury. J Innate Immun 2013; Epub ahead of print.
95. 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: 373-379.
96. Baba M, Nishimura O, Kanzaki N, et al. A small-molecule, nonpeptide CCR5 antagonist with highly potent and selective anti-HIV-1 activity. Proc Natl Acad Sci USA 1999; 96: 5698-5703.
97. Allegretti M, Cesta MC, Garin A, et al. Current status of chemokine receptor inhibitors in development. Immunol Lett 2012; 145: 68-78.
98. Koelink PJ, Overbeek SA, Braber S, de et al. Targeting chemokine receptors in chronic inflammatory diseases: an extensive review. Pharmacol Ther 2012; 133: 1-18.
99. ChemoCentryx Announces Completion of Target Enrolment of CCX140 Phase II Clinical Trial in Diabetic Nephropathy. Company On Track to Report 12-Week Interim Data in Third Quarter of 2013. Available at: http://ir.chemocentryx. com/releasedetail.cfm?ReleaseID=772390. Accessed June 19, 2013.
100. Déruaz M, Frauenschuh A, Alessandri AL, et al. Ticks produce highly selective chemokine binding proteins with antiinflammatory activity. J Exp Med 2008; 205: 2019-2031.
101. Braunersreuther V, Montecucco F, Pelli G, et al. Treatment with the CC chemokine-binding protein Evasin-4 improves post-infarction myocardial injury and survival in mice. Thromb Haemost 2013; 110: 807-825.
102. Lei ZB, Zhang Z, Jing Q, Qin YW, Pei G, Cao BZ, Li XY. OxLDL upregulates CXCR2 expression in monocytes via scavenger receptors and activation of p38 mitogen-activated protein kinase. Cardiovasc Res 2002; 53: 524-532.
103. 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: 1385-1395.
104. 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: 471-481.
105. Oral H, Kanzler I, Tuchscheerer N, et al. CXC chemokine KC fails to induce neutrophil infiltration and neoangiogenesis in a mouse model of myocardial infarction. J Mol Cell Cardiol 2013; 60: 1-7.
106. Liehn EA, Kanzler I, Konschalla S, et al. Compartmentalized protective and detrimental effects of endogenous macrophage migration-inhibitory factor mediated by CXCR2 in a mouse model of myocardial ischaemia/reperfusion. Arterioscler Thromb Vasc Biol 2013; 33: 2180-2186.
107. Garin A, Proudfoot AE. Chemokines as targets for therapy. Exp Cell Res 2011; 317: 602-612.
108. Stanke-Labesque F, Pépin JL, de Jouvencel T, et al. Leukotriene B4 pathway activation and atherosclerosis in obstructive sleep apnea. J Lipid Res 2012; 53: 1944-1951.
109. Li RC, Haribabu B, Mathis SP, Kim J, Gozal D. Leukotriene B4 receptor-1 mediates intermittent hypoxia-induced atherogenesis. Am J Respir Crit Care Med 2011; 184: 124-131.
110. Hoyer FF, Albrecht L, Nickenig G, Müller C. Selective inhibition of leukotriene receptor BLT-2 reduces vascular oxidative stress and improves endothelial function in ApoE-/-mice. Mol Cell Biochem 2012; 359: 25-31.
111. Hlawaty H, Jacob MP, 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: 518-524.
112. Egger G, Burda A, Obernosterer A, et al. Blood polymorphonuclear leukocyte activation in atherosclerosis: effects of aspirin. Inflammation 2001; 25: 129-135.
113. Chakraborti T, Mandal A, Mandal M, et al. Complement activation in heart diseases. Role of oxidants. Cell Signal 2000; 12: 607-617.
114. Veneskoski M, Turunen SP, Kummu O, et al. Specific recognition of malondialdehyde and malondialdehyde acetaldehyde adducts on oxidized LDL and apoptotic cells by complement anaphylatoxin C3a. Free Radic Biol Med 2011; 51: 834-843.
115. Manthey HD, Thomas AC, Shiels IA, et al. Complement C5a inhibition reduces atherosclerosis in ApoE-/-mice. FASEB J 2011; 25: 2447-2455.
116. Kupreishvili K, Baidoshvili A, ter Weeme M, et al. Degeneration and atherosclerosis inducing increased deposition of type IIA secretory phospholipase A2, C-reactive protein and complement in aortic valves cause neutrophilic granulocyte influx. J Heart Valve Dis 2011; 20: 29-36.
117. Kinkade K, Streeter J, Miller FJ. Inhibition of NADPH oxidase by apocynin attenuates progression of atherosclerosis. Int J Mol Sci 2013; 14: 17017-17028.
118. Gray SP, Di Marco E, Okabe J, et al. NADPH oxidase 1 plays a key role in diabetes mellitus-accelerated atherosclerosis. Circulation 2013; 127: 1888-1902.
119. Hosokawa T, Kumon Y, Kobayashi T, et al. Neutrophil infiltration and oxidantproduction in human atherosclerotic carotid plaques. Histol Histopathol 2011; 26: 1-11.
120. Lenglet S, Mach F, Montecucco F. Role of matrix metalloproteinase-8 in atherosclerosis. Mediators Inflamm 2013; 2013: 659282.
121. Lenglet S, Thomas A, Soehnlein O, et al. Fatty acid amide hydrolase deficiency enhances intraplaque neutrophil recruitment in atherosclerotic mice. Arterioscler Thromb Vasc Biol 2013; 33: 215-223.
122. Saragusti AC, Ortega MG, Cabrera JL, et al. Inhibitory effect of quercetin on matrix metalloproteinase 9 activity molecular mechanism and structure-activity relationship of the flavonoid-enzyme interaction. Eur J Pharmacol 2010; 644: 138-145.
123. Rival Y, Benéteau N, Chapuis V, et al. Cardiovascular drugs inhibit MMP-9 activity from human THP-1 macrophages. DNA Cell Biol 2004; 23: 283-292.
124. Jakobsson T, Treuter E, Gustafsson JÅ, et al. Liver X receptor biology and pharmacology: new pathways, challenges and opportunities. Trends Pharmacol Sci 2012; 33: 394-404.
125. Hong C, Kidani Y, A-Gonzalez N, et al. Coordinate regulation of neutrophil homeostasis by liver X receptors in mice. J Clin Invest 2012; 122: 337-347.
126. Tangirala RK, Bischoff ED, Joseph SB, et al. Identification of macrophage liver X receptors as inhibitors of atherosclerosis. Proc Natl Acad Sci USA 2002; 99: 11896-11901.
127. Teupser D, Kretzschmar D, Tennert C, et al. Effect of macrophage overexpression of murine liver X receptor-alpha (LXR-alpha) on atherosclerosis in LDL-receptor deficient mice. Arterioscler Thromb Vasc Biol 2008; 28: 2009-2015.