Plaque angiogenesis and its relation to inflammation and atherosclerotic plaque destabilization

Current Opinion in Lipidology

Volumn 27, Issue 5, 2016, Pages 499-506

  De Vries, Margreet R ^a   Quax, Paul H A ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Angiogenesis; Atherosclerosis; Inflammation; Intraplaque hemorrhage; Neovessel maturation

Indexed keywords

ANGIOGENESIS; ANTIANGIOGENIC THERAPY; ATHEROGENESIS; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; BLEEDING; HUMAN; HYPOXIA; INFLAMMATORY CELL; INTRAPLAQUE HEMORRHAGE; NONHUMAN; PRIORITY JOURNAL; REVIEW; VASCULITIS; ANIMAL; CELL HYPOXIA; COMPLICATION; DIAGNOSTIC IMAGING; INFLAMMATION; MOLECULARLY TARGETED THERAPY; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY; PATHOPHYSIOLOGY;

ANIMALS; CELL HYPOXIA; DIAGNOSTIC IMAGING; HUMANS; INFLAMMATION; MOLECULAR TARGETED THERAPY; NEOVASCULARIZATION, PATHOLOGIC; PLAQUE, ATHEROSCLEROTIC;

EID: 84987811322     PISSN: 09579672     EISSN: 14736535     Source Type: Journal    
DOI: 10.1097/MOL.0000000000000339     Document Type: Review

References (109)

1. Bentzon JF, Otsuka F, Virmani R, Falk E. Mechanisms of plaque formation and rupture. Circ Res 2014; 114:1852-1866.
2. Yahagi K, Kolodgie FD, Otsuka F, et al. Pathophysiology of native coronary, vein graft, and in-stent atherosclerosis. Nat Rev Cardiol 2015; 13:79-98.
3. Hansson GK, Libby P, Tabas I. Inflammation and plaque vulnerability. J Intern Med 2015; 278:483-493.
4. Marsch E, Sluimer JC, Daemen MJ. Hypoxia in atherosclerosis and inflammation. Curr Opin Lipidol 2013; 24:393-400.
5. Kolodgie FD, Gold HK, Burke AP, et al. Intraplaque hemorrhage and progression of coronary atheroma. N Engl J Med 2003; 349:2316-2325.
6. Michel JB, Virmani R, Arbustini E, Pasterkamp G. Intraplaque haemorrhages as the trigger of plaque vulnerability. Eur Heart J 2011; 32:1977-1985.
7. Teng Z, Sadat U, Brown AJ, Gillard JH. Plaque hemorrhage in carotid artery disease: pathogenesis, clinical and biomechanical considerations. J Biomech 2014; 47:847-858.
8. Vrijenhoek JE, Den Ruijter HM, De Borst GJ, et al. Sex is associated with the presence of atherosclerotic plaque hemorrhage and modifies the relation between plaque hemorrhage and cardiovascular outcome. Stroke 2013; 44:3318-3323.
9. Mulligan-Kehoe MJ, Simons M. Vasa vasorum in normal and diseased arteries. Circulation 2014; 129:2557-2566.
10. Jain RK. Antiangiogenesis strategies revisited: from starving tumors to alleviating hypoxia. Cancer Cell 2014; 26:605-622.
11. Bjornheden T, Levin M, Evaldsson M, Wiklund O. Evidence of hypoxic areas within the arterial wall in vivo. Arterioscler Thromb Vasc Biol 1999; 19:870- 876.
12. Sluimer JC, Gasc JM, van Wanroij JL, et al. Hypoxia, hypoxia-inducible transcription factor, and macrophages in human atherosclerotic plaques are correlated with intraplaque angiogenesis. J Am Coll Cardiol 2008; 51:1258-1265.
13. Parathath S, Mick SL, Feig JE, et al. Hypoxia is present in murine atherosclerotic plaques and has multiple adverse effects on macrophage lipid metabolism. Circ Res 2011; 109:1141-1152.
14. van der Valk FM, Sluimer JC, Voo SA, et al. In vivo imaging of hypoxia in atherosclerotic plaques in humans. JACC Cardiovasc Imaging 2015; 8:1340-1341.
15. Yamashita A, Zhao Y, Matsuura Y, et al. Increased metabolite levels of glycolysis and pentose phosphate pathway in rabbit atherosclerotic arteries and hypoxic macrophage. PLoS One 2014; 9:e86426.
16. Tawakol A, Singh P, Mojena M, et al. HIF-1a and PFKFB3 mediate a tight relationship between proinflammatory activation and anerobic metabolism in atherosclerotic macrophages. Arterioscler Thromb Vasc Biol 2015; 35:1463-1471.
17. Crucet M, Wust SJ, Spielmann P, et al. Hypoxia enhances lipid uptake in macrophages: Role of the scavenger receptors Lox1, SRA, and CD36. Atherosclerosis 2013; 229:110-117.
18. Folco EJ, Sukhova GK, Quillard T, Libby P. Moderate hypoxia potentiates interleukin-1b production in activated human macrophages. Circ Res 2014; 115:875-883.
19. Matsuura Y, Yamashita A, Iwakiri T, et al. Vascular wall hypoxia promotes arterial thrombus formation via augmentation of vascular thrombogenicity. Thromb Haemost 2015; 114:158-172.
20. Marsch E, Theelen TL, Demandt JA, et al. Reversal of hypoxia in murine atherosclerosis prevents necrotic core expansion by enhancing efferocytosis. Arterioscler Thromb Vasc Biol 2014; 34:2545-2553.
21. Lijkwan MA, Hellingman AA, Bos EJ, et al. Short hairpin RNA gene silencing of prolyl hydroxylase-2 with a minicircle vector improves neovascularization of hindlimb ischemia. Hum Gene Ther 2014; 25:41-49.
22. Deng W, Feng X, Li X, et al. Hypoxia-inducible factor 1 in autoimmune diseases. Cell Immunol 2016; 303:7-15.
23. van Weel V, de Vries M, Voshol PJ, et al. Hypercholesterolemia reduces collateral artery growth more dominantly than hyperglycemia or insulin resistance in mice. Arterioscler Thromb Vasc Biol 2006; 26:1383-1390.
24. Yao G, Zhang Q, Doeppner TR, et al. LDL suppresses angiogenesis through disruption of the HIF pathway via NF-kappaB inhibition which is reversed by the proteasome inhibitor BSc2118. Oncotarget 2015; 6:30251-30262.
25. Hutter R, Speidl WS, Valdiviezo C, et al. Macrophages transmit potent proangiogenic effects of oxLDL in vitro and in vivo involving HIF-1a activation: A novel aspect of angiogenesis in atherosclerosis. J Cardiovasc Transl Res 2013; 6:558-569.
26. Akhtar S, Hartmann P, Karshovska E, et al. Endothelial hypoxia-inducible factor-1a promotes atherosclerosis and monocyte recruitment by upregulating microRNA-19a. Hypertension 2015; 66:1220-1226.
27. Chaudhari SM, Sluimer JC, Koch M, et al. Deficiency of HIF1a in antigenpresenting cells aggravates atherosclerosis and type 1 T-helper cell responses in mice. Arterioscler Thromb Vasc Biol 2015; 35:2316-2325.
28. Paterson JC. Vascularization and hemorrhage of the intima of arteriosclerotic coronary arteries. Arch Path 1936; 22:313.
29. 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.
30. van Hinsbergh VW, Eringa EC, Daemen MJ. Neovascularization of the atherosclerotic plaque: interplay between atherosclerotic lesion, adventitia- derived microvessels and perivascular fat. Curr Opin Lipidol 2015; 26:405-411.
31. Sluimer JC, Daemen MJ. Novel concepts in atherogenesis: Angiogenesis and hypoxia in atherosclerosis. J Pathol 2009; 218:7-29.
32. Xu J, Lu X, Shi GP. Vasa vasorum in atherosclerosis and clinical significance. Int J Mol Sci 2015; 16:11574-11608.
33. Kessler K, Borges LF, Ho-Tin-Noe B, et al. Angiogenesis and remodelling in human thoracic aortic aneurysms. Cardiovasc Res 2014; 104:147-159.
34. Herrmann J, Lerman LO, Rodriguez-Porcel M, et al. Coronary vasa vasorum neovascularization precedes epicardial endothelial dysfunction in experimental hypercholesterolemia. Cardiovasc Res 2001; 51:762-766.
35. Manka D, Chatterjee TK, Stoll LL, et al. Transplanted perivascular adipose tissue accelerates injury-induced neointimal hyperplasia: Role of monocyte chemoattractant protein-1. Arterioscler Thromb Vasc Biol 2014; 34:1723- 1730.
36. Fleiner M, Kummer M, Mirlacher M, et al. Arterial neovascularization and inflammation in vulnerable patients: Early and late signs of symptomatic atherosclerosis. Circulation 2004; 110:2843-2850.
37. Eelen G, de Zeeuw P, Simons M, Carmeliet P. Endothelial cell metabolism in normal and diseased vasculature. Circ Res 2015; 116:1231-1244.
38. Celletti FL, Waugh JM, Amabile PG, et al. Vascular endothelial growth factor enhances atherosclerotic plaque progression. Nat Med 2001; 7:425-429.
39. Herkenne S, Paques C, Nivelles O, et al. The interaction of uPAR with VEGFR2 promotes VEGF-induced angiogenesis. Sci Signal 2015; 8:ra117.
40. Carmeliet P, Jain RK. Molecular mechanisms and clinical applications of angiogenesis. Nature 2011; 473:298-307.
41. Jaipersad AS, Lip GY, Silverman S, Shantsila E. The role of monocytes in angiogenesis and atherosclerosis. J Am Coll Cardiol 2014; 63:1-11.
42. Fantin A, Vieira JM, Gestri G, et al. Tissue macrophages act as cellular chaperones for vascular anastomosis downstream of VEGF-mediated endothelial tip cell induction. Blood 2010; 116:829-840.
43. Stapor PC, Sweat RS, Dashti DC, et al. Pericyte dynamics during angiogenesis: new insights from new identities. J Vasc Res 2014; 51:163-174.
44. Stratman AN, Malotte KM, Mahan RD, et al. Pericyte recruitment during vasculogenic tube assembly stimulates endothelial basement membrane matrix formation. Blood 2009; 114:5091-5101.
45. Tattersall IW, Du J, Cong Z, et al. In vitro modeling of endothelial interaction with macrophages and pericytes demonstrates Notch signaling function in the vascular microenvironment. Angiogenesis 2016; 19:201-215.
46. van Dijk CG, Nieuweboer FE, Pei JY, et al. The complex mural cell: pericyte function in health and disease. Int J Cardiol 2015; 190:75-89.
47. Kerr BA, West XZ, Kim YW, et al. Stability and function of adult vasculature is sustained by Akt/Jagged1 signalling axis in endothelium. Nat Commun 2016; 7:10960.
48. Hellstrom M, Gerhardt H, Kalen M, et al. Lack of pericytes leads to endothelial hyperplasia and abnormal vascular morphogenesis. J Cell Biol 2001; 153:543-553.
49. Post S, Peeters W, Busser E, et al. Balance between angiopoietin-1 and angiopoietin-2 is in favor of angiopoietin-2 in atherosclerotic plaques with high microvessel density. J Vasc Res 2008; 45:244-250.
50. Sluimer JC, Kolodgie FD, Bijnens AP, et al. Thin-walled microvessels in human coronary atherosclerotic plaques show incomplete endothelial junctions relevance of compromised structural integrity for intraplaque microvascular leakage. J Am Coll Cardiol 2009; 53:1517-1527.
51. Dunmore BJ, McCarthy MJ, Naylor AR, Brindle NP. Carotid plaque instability and ischemic symptoms are linked to immaturity of microvessels within plaques. J Vasc Surg 2007; 45:155-159.
52. Hellings WE, Peeters W, Moll FL, et al. Composition of carotid atherosclerotic plaque is associated with cardiovascular outcome: A prognostic study. Circulation 2010; 121:1941-1950.
53. Habib A, Finn AV. The role of iron metabolism as a mediator of macrophage inflammation and lipid handling in atherosclerosis. Front Pharmacol 2014; 5:195.
54. Boyle JJ, Harrington HA, Piper E, et al. Coronary intraplaque hemorrhage evokes a novel atheroprotective macrophage phenotype. Am J Pathol 2009; 174:1097-1108.
55. Finn AV, Nakano M, Polavarapu R, et al. Hemoglobin directs macrophage differentiation and prevents foam cell formation in human atherosclerotic plaques. J Am Coll Cardiol 2012; 59:166-177.
56. Boyle JJ. Heme and haemoglobin direct macrophage Mhem phenotype and counter foam cell formation in areas of intraplaque haemorrhage. Curr Opin Lipidol 2012; 23:453-461.
57. Newby AC. Proteinases and plaque rupture: unblocking the road to translation. Curr Opin Lipidol 2014; 25:358-366.
58. Willems S, Vink A, Bot I, et al. Mast cells in human carotid atherosclerotic plaques are associated with intraplaque microvessel density and the occurrence of future cardiovascular events. Eur Heart J 2013; 34:3699-3706.
59. Shi GP, Bot I, Kovanen PT. Mast cells in human and experimental cardiometabolic diseases. Nat Rev Cardiol 2015; 12:643-658.
60. Aplin AC, Ligresti G, Fogel E, et al. Regulation of angiogenesis, mural cell recruitment and adventitial macrophage behavior by Toll-like receptors. Angiogenesis 2014; 17:147-161.
61. Langer HF, Chung KJ, Orlova VV, et al. Complement-mediated inhibition of neovascularization reveals a point of convergence between innate immunity and angiogenesis. Blood 2010; 116:4395-4403.
62. Stark K, Eckart A, Haidari S, et al. Capillary and arteriolar pericytes attract innate leukocytes exiting through venules and 'instruct' them with patternrecognition and motility programs. Nat Immunol 2013; 14:41-51.
63. Vestweber D. How leukocytes cross the vascular endothelium. Nat Rev Immunol 2015; 15:692-704.
64. Gerhardt T, Ley K. Monocyte trafficking across the vessel wall. Cardiovasc Res 2015; 107:321-330.
65. Tabas I, Bornfeldt KE. Macrophage phenotype and function in different stages of atherosclerosis. Circ Res 2016; 118:653-667.
66. Jetten N, Verbruggen S, Gijbels MJ, et al. Anti-inflammatory M2, but not proinflammatory M1 macrophages promote angiogenesis in vivo. Angiogenesis 2014; 17:109-118.
67. Barbay V, Houssari M, Mekki M, et al. Role of M2-like macrophage recruitment during angiogenic growth factor therapy. Angiogenesis 2015; 18:191-200.
68. de Souza Junior DA, Santana AC, da Silva EZ, et al. The role of mast cell specific chymases and tryptases in tumor angiogenesis. Biomed Res Int 2015; 2015:142359.
69. de Vries MR, Niessen HW, Lowik CW, et al. Plaque rupture complications in murine atherosclerotic vein grafts can be prevented by TIMP-1 overexpression. PLoS One 2012; 7:e47134.
70. de Vries MR, Wezel A, Schepers A, et al. Complement factor C5a as mast cell activator mediates vascular remodelling in vein graft disease. Cardiovasc Res 2013; 97:311-320.
71. Wezel A, de Vries MR, Maassen JM, et al. Deficiency of the TLR4 analogue RP105 aggravates vein graft disease by inducing a pro-inflammatory response. Sci Rep 2016; 6:24248.
72. Silvestre-Roig C, de Winther MP, Weber C, et al. Atherosclerotic plaque destabilization: mechanisms, models, and therapeutic strategies. Circ Res 2014; 114:214-226.
73. van der Heiden K, Hoogendoorn A, Daemen MJ, Gijsen FJ. Animal models for plaque rupture: A biomechanical assessment. Thromb Haemost 2016; 115:501-508.
74. Matoba T, Sato K, Egashira K. Mouse models of plaque rupture. Curr Opin Lipidol 2013; 24:419-425.
75. Hartwig H, Silvestre-Roig C, Hendrikse J, et al. Atherosclerotic plaque destabilization in mice: A comparative study. PLoS One 2015; 10:e0141019.
76. Moulton KS, Heller E, Konerding MA, et al. Angiogenesis inhibitors endostatin or TNP-470 reduce intimal neovascularization and plaque growth in apolipoprotein E-deficient mice. Circulation 1999; 99:1726-1732.
77. 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.
78. Van der Donckt C, Van Herck JL, Schrijvers DM, et al. Elastin fragmentation in atherosclerotic mice leads to intraplaque neovascularization, plaque rupture, myocardial infarction, stroke, and sudden death. Eur Heart J 2015; 36:1049-1058.
79. Roth L, Rombouts M, Schrijvers DM, et al. Chronic intermittent mental stress promotes atherosclerotic plaque vulnerability, myocardial infarction and sudden death in mice. Atherosclerosis 2015; 242:288-294.
80. Roth L, Rombouts M, Schrijvers DM, et al. Cholesterol-independent effects of atorvastatin prevent cardiovascular morbidity and mortality in a mouse model of atherosclerotic plaque rupture. Vascul Pharmacol 2016; 80:50-58.
81. Yazdani SK, Farb A, Nakano M, et al. Pathology of drug-eluting versus baremetal stents in saphenous vein bypass graft lesions. JACC Cardiovasc Interv 2012; 5:666-674.
82. de Vries MR, Simons KH, Jukema JW, et al. Vein graft failure: from pathophysiology to clinical outcomes. Nat Rev Cardiol 2016; doi:10.1038/nrcardio.2016.76. [Epub ahead of print].
83. Kutkut I, Meens MJ, McKee TA, et al. Lymphatic vessels: An emerging actor in atherosclerotic plaque development. Eur J Clin Invest 2015; 45:100-108.
84. Yang Y, Oliver G. Development of the mammalian lymphatic vasculature. J Clin Invest 2014; 124:888-897.
85. Vuorio T, Nurmi H, Moulton K, et al. Lymphatic vessel insufficiency in hypercholesterolemic mice alters lipoprotein levels and promotes atherogenesis. Arterioscler Thromb Vasc Biol 2014; 34:1162-1170.
86. Aspelund A, Robciuc MR, Karaman S, et al. Lymphatic system in cardiovascular medicine. Circ Res 2016; 118:515-530.
87. Rantakari P, Auvinen K, Jappinen N, et al. The endothelial protein PLVAP in lymphatics controls the entry of lymphocytes and antigens into lymph nodes. Nat Immunol 2015; 16:386-396.
88. Wan W, Lionakis MS, Liu Q, et al. Genetic deletion of chemokine receptor Ccr7 exacerbates atherogenesis in ApoE-deficient mice. Cardiovasc Res 2013; 97:580-588.
89. Taher M, Nakao S, Zandi S, et al. Phenotypic transformation of intimal and adventitial lymphatics in atherosclerosis: A regulatory role for soluble VEGF receptor 2. FASEB J 2016; 30:2490-2499.
90. Mohanta SK, Yin C, Peng L, et al. Artery tertiary lymphoid organs contribute to innate and adaptive immune responses in advanced mouse atherosclerosis. Circ Res 2014; 114:1772-1787.
91. Srikakulapu P, Hu D, Yin C, et al. Artery tertiary lymphoid organs control multilayered territorialized atherosclerosis B-cell responses in aged ApoE-/-mice. Arterioscler Thromb Vasc Biol 2016; 36:1174-1185.
92. Hu D, Mohanta SK, Yin C, et al. Artery tertiary lymphoid organs control aorta immunity and protect against atherosclerosis via vascular smooth muscle cell lymphotoxin b receptors. Immunity 2015; 42:1100-1115.
93. Magnoni M, Ammirati E, Camici PG. Noninvasive molecular imaging of vulnerable atherosclerotic plaques. J Cardiol 2015; 65:261-269.
94. Alonso A, Artemis D, Hennerici MG. Molecular imaging of carotid plaque vulnerability. Cerebrovasc Dis 2015; 39:5-12.
95. Tarkin JM, Dweck MR, Evans NR, et al. Imaging atherosclerosis. Circ Res 2016; 118:750-769.
96. Bourantas CV, Jaffer FA, Gijsen FJ, et al. Hybrid intravascular imaging: Recent advances, technical considerations, and current applications in the study of plaque pathophysiology. Eur Heart J 2016. [Epub ahead of print].
97. Calcagno C, Lobatto ME, Dyvorne H, et al. Three-dimensional dynamic contrast-enhanced MRI for the accurate, extensive quantification of microvascular permeability in atherosclerotic plaques. NMR Biomed 2015; 28:1304-1314.
98. Alie N, Eldib M, Fayad ZA, et al. Inflammation, atherosclerosis, and coronary artery disease: PET/CT for the evaluation of atherosclerosis and inflammation. Clin Med Insights Cardiol 2014; 8:13-21.
99. Yoo JS, Lee J, Jung JH, et al. SPECT/CT imaging of high-risk atherosclerotic plaques using integrin-binding RGD dimer peptides. Sci Rep 2015; 5:11752.
100. Kim S, Lee MW, Kim TS, et al. Intracoronary dual-modal optical coherence tomography-near-infrared fluorescence structural-molecular imaging with a clinical dose of indocyanine green for the assessment of high-risk plaques and stent-Associated inflammation in a beating coronary artery. Eur Heart J 2016. [Epub ahead of print].
101. Taqueti VR, Di Carli MF, Jerosch-Herold M, et al. Increased microvascularization and vessel permeability associate with active inflammation in human atheromata. Circ Cardiovasc Imaging 2014; 7:920-929.
102. Zhang R, Pan D, Cai X, et al. alphaVbeta3-Targeted copper nanoparticles incorporating an Sn 2 lipase-labile fumagillin prodrug for photoacoustic neovascular imaging and treatment. Theranostics 2015; 5:124-133.
103. Wang K, Pan D, Schmieder AH, et al. Atherosclerotic neovasculature MR imaging with mixed manganese-gadolinium nanocolloids in hyperlipidemic rabbits. Nanomedicine 2015; 11:569-578.
104. Belliere J, Martinez de Lizarrondo S, Choudhury RP, et al. Unmasking silent endothelial activation in the cardiovascular system using molecular magnetic resonance imaging. Theranostics 2015; 5:1187-1202.
105. Jain RK, Finn AV, Kolodgie FD, et al. Antiangiogenic therapy for normalization of atherosclerotic plaque vasculature: A potential strategy for plaque stabilization. Nat Clin Pract Cardiovasc Med 2007; 4:491-502.
106. Winnik S, Lohmann C, Siciliani G, et al. Systemic VEGF inhibition accelerates experimental atherosclerosis and disrupts endothelial homeostasis: implications for cardiovascular safety. Int J Cardiol 2013; 168:2453- 2461.
107. Heist RS, Duda DG, Sahani DV, et al. Improved tumor vascularization after anti-VEGF therapy with carboplatin and nab-paclitaxel associates with survival in lung cancer. Proc Natl Acad Sci U S A 2015; 112:1547-1552.
108. Peterson TE, Kirkpatrick ND, Huang Y, et al. Dual inhibition of Ang-2 and VEGF receptors normalizes tumor vasculature and prolongs survival in glioblastoma by altering macrophages. Proc Natl Acad Sci U S A 2016; 113:4470-4475.
109. Kelly-Goss MR, Sweat RS, Stapor PC, et al. Targeting pericytes for angiogenic therapies. Microcirculation 2014; 21:345-357.