Journal of the American Society of Hypertension
Volume 1, Issue 1 , Pages 68-81 , January 2007

Vascular inflammation

  • Valentin Fuster, MD, PhD

      Affiliations

    • Corresponding Author InformationCorresponding author: Valentin Fuster, MD, PhD, The Mount Sinai Medical Center, One Gustave I. Levy Place, 1190 5th Avenue, New York, New York 10029. Tel: 212-241-7911; fax: 212-423-9488.
    • ,
  • Javier Sanz, MD

Received 10 November 2006 ,Accepted 10 November 2006.

References 

  1. Virdis A, Schiffrin EL. Vascular inflammation: a role in vascular disease in hypertension?. Curr Opin Nephrol Hypertens. 2003;12:181–187
  2. Malek AM, Alper SL, Izumo S. Hemodynamic shear stress and its role in atherosclerosis. JAMA. 1999;282:2035–2042
  3. Fuster V, Moreno PR, Fayad ZA, Corti R, Badimon JJ. Atherothrombosis and high-risk plaque: part I: evolving concepts. J Am Coll Cardiol. 2005;46:937–954
  4. Napoli C, de Nigris F, Williams-Ignarro S, Pignalosa O, Sica V, Ignarro LJ. Nitric oxide and atherosclerosis: an update. Nitric Oxide. 2006;15:265–279
  5. Khalil MF, Wagner WD, Goldberg IJ. Molecular interactions leading to lipoprotein retention and the initiation of atherosclerosis. Arterioscler Thromb Vasc Biol. 2004;24:2211–2218
  6. Cheng C, Tempel D, van Haperen R, et al. Atherosclerotic lesion size and vulnerability are determined by patterns of fluid shear stress. Circulation. 2006;113:2744–2753
  7. Hansson GK. Inflammation, atherosclerosis, and coronary artery disease. N Engl J Med. 2005;352:1685–1695
  8. Hansson GK. Immune mechanisms in atherosclerosis. Arterioscler Thromb Vasc Biol. 2001;21:1876–1890
  9. Bjorkbacka H, Kunjathoor VV, Moore KJ, et al. Reduced atherosclerosis in MyD88-null mice links elevated serum cholesterol levels to activation of innate immunity signaling pathways. Nat Med. 2004;10:416–421
  10. Kiechl S, Lorenz E, Reindl M, et al. Toll-like receptor 4 polymorphisms and atherogenesis. N Engl J Med. 2002;347:185–192
  11. Gibson FC, Hong C, Chou H-H, et al. Innate immune recognition of invasive bacteria accelerates atherosclerosis in apolipoprotein E-deficient mice. Circulation. 2004;109:2801–2806
  12. Tobias P, Curtiss LK. Thematic review series: the immune system and atherogenesis (Paying the price for pathogen protection: toll receptors in atherogenesis). J Lipid Res. 2005;46:404–411
  13. de Winther MP, Kanters E, Kraal G, Hofker MH. Nuclear factor kappa-B signaling in atherogenesis. Arterioscler Thromb Vasc Biol. 2005;25:904–914
  14. Valen G, Yan Z-Q, Hansson GK. Nuclear factor kappa-B and the heart. J Am Coll Cardiol. 2001;38:307–314
  15. Chinetti G, Lestavel S, Bocher V, et al. PPAR-alpha and PPAR-gamma activators induce cholesterol removal from human macrophage foam cells through stimulation of the ABCA1 pathway. Nat Med. 2001;7:53–58
  16. Marx N, Sukhova GK, Collins T, Libby P, Plutzky J. PPAR-alpha activators inhibit cytokine-induced vascular cell adhesion molecule-1 expression in human endothelial cells. Circulation. 1999;99:3125–3131
  17. Neve BP, Corseaux D, Chinetti G, et al. PPAR-alpha agonists inhibit tissue factor expression in human monocytes and macrophages. Circulation. 2001;103:207–212
  18. Ricote M, Li AC, Willson TM, Kelly CJ, Glass CK. The peroxisome proliferator-activated receptor-γ is a negative regulator of macrophage activation. Nature. 1998;391:79–82
  19. Moreno PR, Falk E, Palacios IF, Newell JB, Fuster V, Fallon JT. Macrophage infiltration in acute coronary syndromes (Implications for plaque rupture). Circulation. 1994;90:775–778
  20. Moreno PR, Murcia AM, Palacios IF, et al. Coronary composition and macrophage infiltration in atherectomy specimens from patients with diabetes mellitus. Circulation. 2000;102:2180–2184
  21. Shah PK, Falk E, Badimon JJ, et al. Human monocyte-derived macrophages induce collagen breakdown in fibrous caps of atherosclerotic plaques (Potential role of matrix-degrading metalloproteinases and implications for plaque rupture). Circulation. 1995;92:1565–1569
  22. Ivan E, Khatri JJ, Johnson C, et al. Expansive arterial remodeling is associated with increased neointimal macrophage foam cell content: the murine model of macrophage-rich carotid artery lesions. Circulation. 2002;105:2686–2691
  23. Moreno PR, Purushothaman KR, Fuster V, O’Connor WN. Intimomedial interface damage and adventitial inflammation is increased beneath disrupted atherosclerosis in the aorta: implications for plaque vulnerability. Circulation. 2002;105:2504–2511
  24. Durand E, Scoazec A, Lafont A, et al. In vivo induction of endothelial apoptosis leads to vessel thrombosis and endothelial denudation: a clue to the understanding of the mechanisms of thrombotic plaque erosion. Circulation. 2004;109:2503–2506
  25. Boyle JJ, Bowyer DE, Weissberg PL, Bennett MR. Human blood-derived macrophages induce apoptosis in human plaque-derived vascular smooth muscle cells by fas-ligand/fas interactions. Arterioscler Thromb Vasc Biol. 2001;21:1402–1407
  26. Toschi V, Gallo R, Lettino M, et al. Tissue factor modulates the thrombogenicity of human atherosclerotic plaques. Circulation. 1997;95:594–599
  27. Moreno PR, Bernardi VH, Lopez-Cuellar J, et al. Macrophages, smooth muscle cells, and tissue factor in unstable angina: implications for cell-mediated thrombogenicity in acute coronary syndromes. Circulation. 1996;94:3090–3097
  28. Hutter R, Valdiviezo C, Sauter BV, et al. Caspase-3 and tissue factor expression in lipid-rich plaque macrophages: evidence for apoptosis as link between inflammation and atherothrombosis. Circulation. 2004;109:2001–2008
  29. Sambola A, Osende J, Hathcock J, et al. Role of risk factors in the modulation of tissue factor activity and blood thrombogenicity. Circulation. 2003;107:973–977
  30. Moreno PR, Purushothaman K-R, Sirol M, Levy AP, Fuster V. Neovascularization in human atherosclerosis. Circulation. 2006;113:2245–2252
  31. Moreno PR, Purushothaman KR, Fuster V, et al. Plaque neovascularization is increased in ruptured atherosclerotic lesions of human aorta: implications for plaque vulnerability. Circulation. 2004;110:2032–2038
  32. O’Brien KD, McDonald TO, Chait A, Allen MD, Alpers CE. Neovascular expression of E-selectin, intercellular adhesion molecule-1, and vascular cell adhesion molecule-1 in human atherosclerosis and their relation to intimal leukocyte content. Circulation. 1996;93:672–682
  33. Kolodgie FD, Gold HK, Burke AP, et al. Intraplaque hemorrhage and progression of coronary atheroma. N Engl J Med. 2003;349:2316–2325
  34. Virmani R, Kolodgie FD, Burke AP, et al. Atherosclerotic plaque progression and vulnerability to rupture: angiogenesis as a source of intraplaque hemorrhage. Arterioscler Thromb Vasc Biol. 2005;25:2054–2061
  35. Kristiansen M, Graversen JH, Jacobsen C, et al. Identification of the haemoglobin scavenger receptor. Nature. 2001;409:198–201
  36. Asleh R, Marsh S, Shilkrut M, et al. Genetically determined heterogeneity in hemoglobin scavenging and susceptibility to diabetic cardiovascular disease. Circ Res. 2003;92:1193–1200
  37. Levy AP, Hochberg I, Jablonski K, et al. Haptoglobin phenotype is an independent risk factor for cardiovascular disease in individuals with diabetes: the strong heart study. J Am Coll Cardiol. 2002;40:1984–1990
  38. Dandona P, Aljada A, Chaudhuri A, Mohanty P, Garg R. Metabolic syndrome: a comprehensive perspective based on interactions between obesity, diabetes, and inflammation. Circulation. 2005;111:1448–1454
  39. Sjoholm A, Nystrom T. Endothelial inflammation in insulin resistance. Lancet. 2005;365:610–612
  40. Pradhan AD, Manson JE, Rifai N, Buring JE, Ridker PM. C-reactive protein, interleukin 6, and risk of developing type 2 diabetes mellitus. JAMA. 2001;286:327–334
  41. Hilgers KF. Monocytes/macrophages in hypertension. J Hypertens. 2002;20:593–596
  42. Diet F, Pratt RE, Berry GJ, Momose N, Gibbons GH, Dzau VJ. Increased accumulation of tissue ACE in human atherosclerotic coronary artery disease. Circulation. 1996;94:2756–2767
  43. Raines EW, Ferri N. Thematic review series: the immune system and atherogenesis. Cytokines affecting endothelial and smooth muscle cells in vascular disease. J Lipid Res. 2005;46:1081–1092
  44. Chae CU, Lee RT, Rifai N, Ridker PM. Blood pressure and inflammation in apparently healthy men. Hypertension. 2001;38:399–403
  45. Abramson JL, Weintraub WS, Vaccarino V. Association between pulse pressure and C-reactive protein among apparently healthy US adults. Hypertension. 2002;39:197–202
  46. Sesso HD, Buring JE, Rifai N, Blake GJ, Gaziano JM, Ridker PM. C-reactive protein and the risk of developing hypertension. JAMA. 2003;290:2945–2951
  47. Smith GD, Lawlor DA, Harbord R, et al. Association of C-reactive protein with blood pressure and hypertension: life course confounding and Mendelian randomization tests of causality. Arterioscler Thromb Vasc Biol. 2005;25:1051–1056
  48. Wang C-H, Li S-H, Weisel RD, et al. C-reactive protein upregulates angiotensin type 1 receptors in vascular smooth muscle. Circulation. 2003;107:1783–1790
  49. Verma S, Li S-H, Badiwala MV, et al. Endothelin antagonism and interleukin-6 inhibition attenuate the proatherogenic effects of C-reactive protein. Circulation. 2002;105:1890–1896
  50. Dzau VJ. Tissue angiotensin and pathobiology of vascular disease: a unifying hypothesis. Hypertension. 2001;37:1047–1052
  51. Schiffrin EL. Vascular endothelin in hypertension. Vascul Pharmacol. 2005;43:19–29
  52. Cunningham KS, Gotlieb AI. The role of shear stress in the pathogenesis of atherosclerosis. Lab Invest. 2005;85:9–23
  53. Tearney GJ, Yabushita H, Houser SL, et al. Quantification of macrophage content in atherosclerotic plaques by optical coherence tomography. Circulation. 2003;107:113–119
  54. Verheye S, De Meyer GR, Van Langenhove G, Knaapen MW, Kockx MM. In vivo temperature heterogeneity of atherosclerotic plaques is determined by plaque composition. Circulation. 2002;105:1596–1601
  55. Davies JR, Rudd JH, Fryer TD, et al. Identification of culprit lesions after transient ischemic attack by combined 18F-fluorodeoxyglucose positron-emission tomography and high-resolution magnetic resonance imaging. Stroke. 2005;36:2642–2647
  56. Rudd JH, Warburton EA, Fryer TD, et al. Imaging atherosclerotic plaque inflammation with 18F-fluorodeoxyglucose positron-emission tomography. Circulation. 2002;105:2708–2711
  57. Weiss CR, Arai AE, Bui MN, et al. Arterial wall MRI characteristics are associated with elevated serum markers of inflammation in humans. J Magn Reson Imaging. 2001;14:698–704
  58. Kooi ME, Cappendijk VC, Cleutjens KBJM, et al. Accumulation of ultrasmall superparamagnetic particles of iron oxide in human atherosclerotic plaques can be detected by in vivo magnetic resonance imaging. Circulation. 2003;107:2453–2458
  59. Ruehm SG, Corot C, Vogt P, Kolb S, Debatin JF. Magnetic resonance imaging of atherosclerotic plaque with ultrasmall superparamagnetic particles of iron oxide in hyperlipidemic rabbits. Circulation. 2001;103:415–422
  60. Choudhury RP, Fuster V, Fayad ZA. Molecular, cellular, and functional imaging of atherothrombosis. Nat Rev Drug Discov. 2004;3:913–925
  61. Kelly KA, Allport JR, Tsourkas A, Shinde-Patil VR, Josephson L, Weissleder R. Detection of vascular adhesion molecule-1 expression using a novel multimodal nanoparticle. Circ Res. 2005;96:327–336
  62. Deguchi J-o, Aikawa M, Tung C-H. Inflammation in atherosclerosis: visualizing matrix metalloproteinase action in macrophages in vivo. Circulation. 2006;114:55–62
  63. Takaya N, Yuan C, Chu B, et al. Presence of intraplaque hemorrhage stimulates progression of carotid atherosclerotic plaques: a high-resolution magnetic resonance imaging study. Circulation. 2005;111:2768–2775
  64. Kerwin W, Hooker A, Spilker M, et al. Quantitative magnetic resonance imaging analysis of neovasculature volume in carotid atherosclerotic plaque. Circulation. 2003;107:851–856
  65. Sirol M, Purushothaman KR, Moreno PR, et al. Increased neovascularization in advanced lipid-rich atherosclerotic lesions detected by gadofluorine-enhanced magnetic resonance imaging (MRI): implications for plaque vulnerability. Circulation. 2005;112(suppl-II):A1184
  66. Winter PM, Morawski AM, Caruthers SD, et al. Molecular imaging of angiogenesis in early-stage atherosclerosis with alpha(v)beta3-integrin-targeted nanoparticles. Circulation. 2003;108:2270–2274
  67. Smith SC, Anderson JL, Cannon RO, et al. CDC/AHA workshop on markers of inflammation and cardiovascular disease: application to clinical and public health practice: report from the Clinical Practice Discussion Group. Circulation. 2004;110:e550–e553
  68. Tzoulaki I, Murray GD, Lee AJ, Rumley A, Lowe GD, Fowkes FG. C-reactive protein, interleukin-6, and soluble adhesion molecules as predictors of progressive peripheral atherosclerosis in the general population: Edinburgh Artery Study. Circulation. 2005;112:976–983
  69. Zouridakis E, Avanzas P, Arroyo-Espliguero R, Fredericks S, Kaski JC. Markers of inflammation and rapid coronary artery disease progression in patients with stable angina pectoris. Circulation. 2004;110:1747–1753
  70. Blankenberg S, McQueen MJ, Smieja M, et al. Comparative impact of multiple biomarkers and N-terminal pro-brain natriuretic peptide in the context of conventional risk factors for the prediction of recurrent cardiovascular events in the Heart Outcomes Prevention Evaluation (HOPE) study. Circulation. 2006;114:201–208
  71. Verma S, Kuliszewski MA, Li S-H, et al. C-reactive protein attenuates endothelial progenitor cell survival, differentiation, and function: further evidence of a mechanistic link between C-reactive protein and cardiovascular disease. Circulation. 2004;109:2058–2067
  72. Jialal I, Devaraj S, Singh U. C-reactive protein and the vascular endothelium: implications for plaque instability. J Am Coll Cardiol. 2006;47:1379–1381
  73. Timpson NJ, Lawlor DA, Harbord RM, et al. C-reactive protein and its role in metabolic syndrome: Mendelian randomization study. Lancet. 2005;366:1954–1959
  74. Koh KK, Quon MJ, Han SH, et al. Additive beneficial effects of fenofibrate combined with atorvastatin in the treatment of combined hyperlipidemia. J Am Coll Cardiol. 2005;45:1649–1653
  75. Esposito K, Marfella R, Ciotola M, et al. Effect of a Mediterranean-style diet on endothelial dysfunction and markers of vascular inflammation in the metabolic syndrome: a randomized trial. JAMA. 2004;292:1440–1446
  76. Esposito K, Pontillo A, Di Palo C, et al. Effect of weight loss and lifestyle changes on vascular inflammatory markers in obese women: a randomized trial. JAMA. 2003;289:1799–1804
  77. Hutter R, Carrick FE, Valdiviezo C, et al. Vascular endothelial growth factor regulates reendothelialization and neointima formation in a mouse model of arterial injury. Circulation. 2004;110:2430–2435
  78. Walter DH, Rittig K, Bahlmann FH, et al. Statin therapy accelerates re-endothelialization: a novel effect involving mobilization and incorporation of bone marrow-derived endothelial progenitor cells. Circulation. 2002;105:3017–3024
  79. Rauscher FM, Goldschmidt-Clermont PJ, Davis BH, et al. Aging, progenitor cell exhaustion, and atherosclerosis. Circulation. 2003;108:457–463
  80. Vasa M, Fichtlscherer S, Aicher A, et al. Number and migratory activity of circulating endothelial progenitor cells inversely correlate with risk factors for coronary artery disease. Circ Res. 2001;89:E1–E7
  81. Werner N, Kosiol S, Schiegl T, et al. Circulating endothelial progenitor cells and cardiovascular outcomes. N Engl J Med. 2005;353:999–1007
  82. Arnaud C, Burger F, Steffens S, et al. Statins reduce interleukin-6-induced C-reactive protein in human hepatocytes: new evidence for direct antiinflammatory effects of statins. Arterioscler Thromb Vasc Biol. 2005;25:1231–1236
  83. Laufs U, La Fata V, Plutzky J, Liao JK. Upregulation of endothelial nitric oxide synthase by HMG CoA reductase inhibitors. Circulation. 1998;97:1129–1135
  84. Wibaut-Berlaimont V, Randi AM, Mandryko V, Lunnon MW, Haskard DO, Naoumova RP. Atorvastatin affects leukocyte gene expression in dyslipidemia patients: in vivo regulation of hemostasis, inflammation, and apoptosis. J Thromb Haemost. 2005;3:677–685
  85. Albert MA, Danielson E, Rifai N, Ridker PM PRINCE Investigators. Effect of statin therapy on C-reactive protein l levels: the Pravastatin Inflammation/CRP Evaluation (PRINCE): a randomized trial and cohort study. JAMA. 2001;286:64–70
  86. Ridker PM, Rifai N, Pfeffer MA, Sacks F, Braunwald E The Cholesterol and Recurrent Events (CARE) Investigators. Long-term effects of pravastatin on plasma concentration of C-reactive protein. Circulation. 1999;100:230–235
  87. Ridker PM, Cannon CP, Morrow D, et al. C-reactive protein levels and outcomes after statin therapy. N Engl J Med. 2005;352:20–28
  88. Robinson JG, Smith B, Maheshwari N, Schrott H. Pleiotropic effects of statins: benefit beyond cholesterol reduction? A meta-regression analysis. J Am Coll Cardiol. 2005;46:1855–1862
  89. Corti R, Fuster V, Fayad ZA, et al. Lipid lowering by simvastatin induces regression of human atherosclerotic lesions: two years’ follow-up by high-resolution noninvasive magnetic resonance imaging. Circulation. 2002;106:2884–2887
  90. Badimon JJ, Badimon L, Fuster V. Regression of atherosclerotic lesions by high density lipoprotein plasma fraction in the cholesterol-fed rabbit. J Clin Invest. 1990;85:1234–1241
  91. Nissen SE, Tsunoda T, Tuzcu EM, et al. Effect of recombinant ApoA-I Milano on coronary atherosclerosis in patients with acute coronary syndromes: a randomized controlled trial. JAMA. 2003;290:2292–2300
  92. Rong JX, Li J, Reis ED, et al. Elevating high-density lipoprotein cholesterol in apolipoprotein E-deficient mice remodels advanced atherosclerotic lesions by decreasing macrophage and increasing smooth muscle cell content. Circulation. 2001;104:2447–2452
  93. Suc I, Escargueil-Blanc I, Troly M, Salvayre R, Negre-Salvayre A. HDL and apoA prevent cell death of endothelial cells induced by oxidized LDL. Arterioscler Thromb Vasc Biol. 1997;17:2158–2166
  94. Nicholls SJ, Dusting GJ, Cutri B, et al. Reconstituted high-density lipoproteins inhibit the acute pro-oxidant and proinflammatory vascular changes induced by a periarterial collar in normocholesterolemic rabbits. Circulation. 2005;111:1543–1550
  95. Duffy D, Rader DJ. Emerging therapies targeting high-density lipoprotein metabolism and reverse cholesterol transport. Circulation. 2006;113:1140–1150
  96. Zambon A, Gervois P, Pauletto P, Fruchart J-C, Staels B. Modulation of hepatic inflammatory risk markers of cardiovascular diseases by PPAR-alpha activators: clinical and experimental evidence. Arterioscler Thromb Vasc Biol. 2006;26:977–986
  97. Haffner SM, Greenberg AS, Weston WM, Chen H, Williams K, Freed MI. Effect of rosiglitazone treatment on nontraditional markers of cardiovascular disease in patients with type 2 diabetes mellitus. Circulation. 2002;106:679–684
  98. Pasceri V, Wu HD, Willerson JT, Yeh ETH. Modulation of vascular inflammation in vitro and in vivo by peroxisome proliferator-activated receptor-gamma activators. Circulation. 2000;101:235–238
  99. Fliser D, Buchholz K, Haller H EUropean Trial on Olmesartan and Pravastatin in Inflammation and Atherosclerosis Investigators. Antiinflammatory effects of angiotensin II subtype 1 receptor blockade in hypertensive patients with microinflammation. Circulation. 2004;110:1103–1107
  100. Kuster GM, Kotlyar E, Rude MK, et al. Mineralocorticoid receptor inhibition ameliorates the transition to myocardial failure and decreases oxidative stress and inflammation in mice with chronic pressure overload. Circulation. 2005;111:420–427
  101. Ridker PM, Danielson E, Rifai N, Glynn RJ, for the Val MI. Valsartan, blood pressure reduction, and C-reactive protein: primary report of the Val-MARC trial. Hypertension. 2006;48:73–79
  102. Schieffer B, Bunte C, Witte J, et al. Comparative effects of AT1-antagonism and angiotensin-converting enzyme inhibition on markers of inflammation and platelet aggregation in patients with coronary artery disease. J Am Coll Cardiol. 2004;44:362–368
  103. Ridker PM, Cushman M, Stampfer MJ, Tracy RP, Hennekens CH. Inflammation, aspirin, and the risk of cardiovascular disease in apparently healthy men. N Engl J Med. 1997;336:973–979
  104. Moulton KS, Vakili K, Zurakowski D, et al. Inhibition of plaque neovascularization reduces macrophage accumulation and progression of advanced atherosclerosis. Proc Natl Acad Sci U S A. 2003;100:4736–4741
  105. Simons M. Angiogenesis: where do we stand now?. Circulation. 2005;111:1556–1566
  106. Moreno PR, Fuster V. New aspects in the pathogenesis of diabetic atherothrombosis. J Am Coll Cardiol. 2004;44:2293–2300

 Conflict of interest: none.

PII: S1933-1711(06)00002-7

doi: 10.1016/j.jash.2006.11.005

Journal of the American Society of Hypertension
Volume 1, Issue 1 , Pages 68-81 , January 2007

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