Neovascularization of the atherosclerotic plaque: Interplay between atherosclerotic lesion, adventitiaderived microvessels and perivascular fat

Current Opinion in Lipidology

Volumn 26, Issue 5, 2015, Pages 405-411

  Van Hinsbergh, Victor W M ^a   Eringa, Etto C ^a   Daemen, Mat J A P ^b  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^b ACADEMIC MEDICAL CENTER   (Netherlands)

Author keywords

Angiogenesis; Atherosclerosis; Imaging; Perivascular adipose tissue; Vasa vasorum

Indexed keywords

ADIPONECTIN; OXYGEN;

ADIPOSE TISSUE; ADVENTITIA; ANTIANGIOGENIC ACTIVITY; ARTERY PERFUSION; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; DISEASE COURSE; HUMAN; HYPOXIA; IMMUNOHISTOCHEMISTRY; LYMPHANGIOGENESIS; MACROPHAGE; MONOCYTE; NEOVASCULARIZATION (PATHOLOGY); NONHUMAN; NUTRIENT SUPPLY; PERIVASCULAR ADIPOSE TISSUE; PRIORITY JOURNAL; REVIEW; VASA VASORUM; VASCULAR REMODELING; ANIMAL; BLOOD; CELL HYPOXIA; IMMUNOLOGY; MICROVASCULATURE; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; VASCULARIZATION;

ADIPONECTIN; ADIPOSE TISSUE; ADVENTITIA; ANIMALS; ATHEROSCLEROSIS; CELL HYPOXIA; HUMANS; MICROVESSELS; NEOVASCULARIZATION, PATHOLOGIC; OXYGEN; PLAQUE, ATHEROSCLEROTIC;

EID: 84973513794     PISSN: 09579672     EISSN: 14736535     Source Type: Journal    
DOI: 10.1097/MOL.0000000000000210     Document Type: Review

References (90)

1. O'Brien ER, Garvin MR, Dev R, et al. Angiogenesis in human coronary atherosclerotic plaques. Am J Pathol 1994; 145:883-894.
2. 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.
3. 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.
4. Truijman MTB, Kwee RM, van Hoof RHM, et al. Combined F-18-FDG PET-CT and DCE-MRI to assess inflammation and microvascularization in atherosclerotic plaques. Stroke 2013; 44:3568-3570.
5. Herrmann J, Lerman LO, Mukhopadhyay D, et al. Angiogenesis in atherogenesis. Arterioscler Thromb Vasc Biol 2006; 26:1948-1957.
6. Mulligan-Kehoe MJ, Simons M. Vasa vasorum in normal and diseased arteries. Circulation 2014; 129:2557-2566.
7. Ritman EL, Lerman A. The dynamic vasa vasorum. Cardiovasc Res 2007; 75:649-658.
8. Jaipersad AS, Lip GYH, Silverman S, Shantsila E. The role of monocytes in angiogenesis and atherosclerosis. J Am Coll Cardiol 2014; 63:1-11.
9. Marsch E, Sluimer JC, Daemen MJAP. Hypoxia in atherosclerosis and inflammation. Curr Opin Lipidol 2013; 24:393-400.
10. Sluimer JC, Daemen MJ. Novel concepts in atherogenesis: Angiogenesis and hypoxia in atherosclerosis. J Pathol 2009; 218:7-29.
11. Fraisl P, Mazzone M, Schmidt T, Carmeliet P. Regulation of angiogenesis by oxygen and metabolism. Develop Cell 2009; 16:167-179.
12. Falk E, Nakano M, Bentzon JF, et al. Update on acute coronary syndromes: The pathologists view. Eur Heart J 2013; 34:719-728.
13. Bentzon JF, Otsuka F, Virmani R, Falk E. Mechanisms of plaque formation and rupture. Circ Res 2014; 114:1852-1866.
14. Michel JB, Virmani R, Arbustini E, Pasterkamp G. Intraplaque haemorrhages as the trigger of plaque vulnerability. Eur Heart J 2011; 32:1977-1981.
15. Schoenberger F, Mueller A. On the vascularization of the bovine aortic wall [in German]. Helvetica Physiol Pharmacol Acta 1960; 18:136-150.
16. Bjornheden T, Levin M, Evaldsson M, Wiklund O. Evidence of hypoxic areas within the arterialwall in vivo. Arterioscler ThrombVasc Biol 1999;19:870-876.
17. 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.
18. Mateo J, Izquierdo-Garcia D, Badimon JJ, et al. Noninvasive assessment of hypoxia in rabbit advanced atherosclerosis using F-18-fluoromisonidazole positron emission tomographic imaging. Circ Cardiovasc Imaging 2014; 7:312-320.
19. Semenza GL. Targeting HIF-1 for cancer therapy. Nat Rev Cancer 2003; 3:721-732.
20. Takeda N, Maemura K, Imai Y, et al. Endothelial PAS domain protein 1 gene promotes angiogenesis through the transactivation of both vascular endothelial growth factor and its receptor, Flt-1. Circ Res 2004; 95:146-153.
21. Sukonina V, Lookene A, Olivecrona T, Olivecrona G. Angiopoietin-like protein 4 converts lipoprotein lipase to inactive monomers and modulates lipase activity in adipose tissue. Proc Natl Acad Sci U S A 2006; 103:17450-17455.
22. Potente M, Gerhardt H, Carmeliet P. Basic and therapeutic aspects of angiogenesis. Cell 2011;146:873-887.
23. Tammela T, Alitalo K. Lymphangiogenesis: molecular mechanisms and future promise. Cell 2010; 140:460-476.
24. Ruas JL, Lendahl U, Poellinger L. Modular of vascular gene expression by hypoxia. Curr Opin Lipidol 2007; 18:508-514.
25. Wouters BG, Koritzinsky M. Hypoxia signalling through mTOR and the unfolded protein response in cancer. Nat Rev Cancer 2008; 8:851-864.
26. Hutter R, Speidl WS, Valdiviezo C, et al. Macrophages transmit potent proangiogenic effects of oxLDL in vitro and in vivo involving HIF-1 alpha activation: A novel aspect of angiogenesis in atherosclerosis. J Cardiovasc Translat Res 2013; 6:558-569.
27. Giannarelli C, Alique M, Rodriguez DT, et al. Alternatively spliced tissue factor promotes plaque angiogenesis through the activation of hypoxia-inducible factor-1 alpha and vascular endothelial growth factor signaling. Circulation 2014; 130:1274-1286.
28. Skuli N, Majmundar AJ, Krock BL, et al. Endothelial HIF-2 alpha regulates murine pathological angiogenesis and revascularization processes. J Clin Investig 2012; 122:1427-1443.
29. Jain RK. Antiangiogenesis strategies revisited: from starving tumors to alleviating hypoxia. Cancer Cell 2014; 26:605-622.
30. Tenaglia AN, Peters KG, Sketch MH, Annex BH. Neovascularization in atherectomy specimens from patients with unstable angina: implications for pathogenesis of unstable angina. Am Heart J 1998; 135:10-14.
31. 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.
32. Kerwin WS, O'Brien KD, Ferguson MS, et al. Inflammation in carotid atherosclerotic plaque: A dynamic contrast-enhanced MR imaging study. Radiology 2006; 241:459-468.
33. Calcagno C, Ramachandran S, Izquierdo-Garcia D, et al. The complementary roles of dynamic contrast-enhanced MRI and F-18-fluorodeoxyglucose PET/CT for imaging of carotid atherosclerosis. Eur J Nuclear Med Mol Imaging 2013; 40:1884-1893.
34. Ichibori Y, Nakatani D, Sakata Y, et al. Cardiac allograft vasculopathy progression associated with intraplaque neovascularization. J Am Coll Cardiol 2013; 61:902. 35.
35. Aoki T, Rodriguez-Porcel M, Matsuo Y, et al. Evaluation of coronary adventitial vasa vasorum using 3D optical coherence tomography: Animal and human studies. Atherosclerosis 2015; 239:203-208.
36. Pelisek J, Well G, Reeps C, et al. Neovascularization and angiogenic factors in advanced human carotid artery stenosis. Circ J 2012; 76:1274-1282.
37. 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.
38. Marsch E, Theelen TL, Demandt JAF, et al. Reversal of hypoxia in murine atherosclerosis prevents necrotic core expansion by enhancing efferocytosis. Arterioscler Thromb Vasc Biol 2014; 34:2545-2553.
39. Bot I, Jukema JW, Lankhuizen IM, et al. Atorvastatin inhibits plaque development and adventitial neovascularization in Apo E deficient mice independent of plasma cholesterol levels. Atherosclerosis 2011; 214:295-300.
40. 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.
41. Kwon HM, Sangiorgi G, Ritman EL, et al. Enhanced coronary vasa vasorum neovascularization in experimental hypercholesterolemia. J Clin Investig 1998; 101:1551-1556.
42. Sluimer JC, Kolodgie FD, Bijnens APJJ, 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.
43. Zhu Y, Deng YB, Liu YN, et al. Use of carotid plaque neovascularization at contrast-enhanced US to predict coronary events in patients with coronary artery disease. Radiology 2013; 268:54-60.
44. O'Brien KD, Allen MD, McDonald TO, et al. Vascular cell-Adhesion molecule-1 is expressed in human coronary atherosclerotic plaques: implications for the mode of progression of advanced coronary atherosclerosis. J Clin Investig 1993; 92:945-951.
45. Boyle JJ, Johns M, Kampfer T, et al. Activating transcription factor 1 directs mhem atheroprotective macrophages through coordinated iron handling and foam cell protection. Circ Res 2012; 110:20-33.
46. 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.
47. Langheinrich AC, Michniewicz A, Sedding DG, et al. Correlation of vasa vasorum Neovascularization and plaque progression in aortas of apolipoprotein E-/-/low-density lipoprotein (-/-) double knockout mice. Arterioscler Thromb Vasc Biol 2006; 26:347-352.
48. Drinane M, Mollmark J, Zagorchev L, et al. The antiangiogenic activity of rPAI- 1(23) inhibits vasa vasorum and growth of atherosclerotic plaque. Circ Res 2009; 104:337-345.
49. Khurana R, Moons L, Shafi S, et al. Placental growth factor promotes atherosclerotic intimal thickening and macrophage accumulation. Circulation 2005; 111:2828-2836.
50. Wang YS, Zhou YH, He LP, et al. Gene delivery of soluble vascular endothelial growth factor receptor-1 (sFlt-1) inhibits intra-plaque angiogenesis and suppresses development of atherosclerotic plaque. Clin Exp Med 2011; 11:113-121.
51. Tanaka K, Nagata D, Hirata Y, et al. Augmented angiogenesis in adventitia promotes growth of atherosclerotic plaque in apolipoprotein E-deficient mice. Atherosclerosis 2011; 215:366-373.
52. Kutkut I, Meens MJ, McKee TA, et al. Lymphatic vessels: An emerging actor in atherosclerotic plaque development. Eur J Clin Investig 2015; 45:100-108.
53. Nakano T, Nakashima Y, Yonemitsu Y, et al. Angiogenesis and lymphangiogenesis and expression of lymphangiogenic factors in the atherosclerotic intima of human coronary arteries. Human Pathol 2005; 36:330-340.
54. Drozdz K, Janczak D, Dziegiel P, et al. Adventitial lymphatics of internal carotid artery in healthy and atherosclerotic vessels. Folia Histochem Cytobiol 2008; 46:433-436.
55. Drozdz K, Janczak D, Dziegiel P, et al. Adventitial lymphatics and atherosclerosis. Lymphology 2012; 45:26-33.
56. Martel C, Li WJ, Fulp B, et al. Lymphatic vasculature mediates macrophage reverse cholesterol transport in mice. J Clin Investig 2013; 123:1571-1579.
57. Vuorio T, Jauhiainen S, Yla-Herttuala S. Pro-And antiangiogenic therapy and atherosclerosis with special emphasis on vascular endothelial growth factors. Expert Opin Biol Ther 2012; 12:79-92.
58. Kholova I, Dragneva G, Cermakova P, et al. Lymphatic vasculature is increased in heart valves, ischaemic and inflamed hearts and in cholesterol-rich and calcified atherosclerotic lesions. Eur J Clin Investig 2011; 41:487-497.
59. Grzegorek I, Drozdz K, Chmielewska M, et al. Arterial wall lymphangiogenesis is increased in the human iliac atherosclerotic arteries: involvement of CCR7 receptor. Lymphatic Res Biol 2014; 12:222-231.
60. Issa A, Le TX, Shoushtari AN, et al. Vascular endothelial growth factor-C and C-C chemokine receptor 7 in tumor cell-lymphatic cross-Talk promote invasive phenotype. Cancer Res 2009; 69:349-357.
61. 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.
62. 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.
63. Kampschulte M, Gunkel I, Stieger P, et al. Thalidomide influences atherogenesis in aortas of ApoE(-/-)/LDLR-/- double knockout mice: A nano-CT study. Int J Cardiovasc Imaging 2014; 30:795-802.
64. Mollmark JI, Park AJH, Kim J, et al. Fibroblast growth factor-2 is required for vasa vasorum plexus stability in hypercholesterolemic mice. Arterioscler Thromb Vasc Biol 2012; 32:2644-2651.
65. 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.
66. Ropert S, Vignaux O, Mir O, Goldwasser F. VEGF pathway inhibition by anticancer agent sunitinib and susceptibility to atherosclerosis plaque disruption. Investig New Drugs 2011; 29:1497-1499.
67. Mourad JJ, des Guetz G, Debbabi H, Levy BI. Blood pressure rise following angiogenesis inhibition by bevacizumab. A crucial role for microcirculation. Ann Oncol 2008; 19:927-934 .
68. van der Veldt AAM, de Boer MP, Boven E, et al. Reduction in skin microvascular density and changes in vessel morphology in patients treated with sunitinib. Anti-Cancer Drugs 2010; 21:439-446.
69. Schirmer SH, Fledderus JO, Bot PTG, et al. Interferon-beta signaling is enhanced in patients with insufficient coronary collateral artery development and inhibits arteriogenesis in mice. Circ Res 2008; 102:1286-1294.
70. 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.
71. Obrien KD, Mcdonald TO, Chait A, et al. 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.
72. Kumar AHS, Martin K, TurnerEC, et al. Role ofCX(3)CR1receptor inmonocyte/macrophage driven neovascularization. PLoS One 2013; 8:e57230.
73. Datta M, Via LE, Kamoun WS, et al. Antivascular endothelial growth factor treatment normalizes tuberculosis granuloma vasculature and improves small molecule delivery. Proc Natl Acad Sci U S A 2015; 112:1827-1832.
74. 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.
75. Takaoka M, Nagata D, Kihara S, et al. Periadventitial adipose tissue plays a critical role in vascular remodeling. Circ Res 2009; 105:906-911.
76. Ouchi N, Parker JL, Lugus JJ, Walsh K. Adipokines in inflammation and metabolic disease. Nat Rev Immunol 2011; 11:85-97.
77. Meijer RI, Serne EH, Smulders YM, et al. Perivascular adipose tissue and its role in type 2 diabetes and cardiovascular disease. Curr Diab Rep 2011; 11:211-217.
78. Yudkin JS, Eringa E, Stehouwer CDA. 'Vasocrine' signalling from perivascular fat: A mechanism linking insulin resistance to vascular disease. Lancet 2005; 365:1817-1820.
79. Greenstein AS, Khavandi K, Withers SB, et al. Local inflammation and hypoxia abolish the protective anticontractile properties of perivascular fat in obese patients. Circulation 2009; 119:1661-1670.
80. Rittig K, Dolderer JH, Balletshofer B, et al. The secretion pattern of perivascular fat cells is different from that of subcutaneous and visceral fat cells. Diabetologia 2012; 55:1514-1525.
81. Eringa EC, Bakker W, van Hinsbergh VWM. Paracrine regulation of vascular tone, inflammation and insulin sensitivity by perivascular adipose tissue. Vasc Pharmacol 2012; 56:204-209.
82. Henrichot E, Juge-Aubry CE, Pernin AS, et al. Production of chemokines by perivascular adipose tissue: A role in the pathogenesis of atherosclerosis? Arterioscler Thromb Vasc Biol 2005; 25:2594-2599.
83. Takaoka M, Suzuki H, Shioda S, et al. Endovascular injury induces rapid phenotypic changes in perivascular adipose tissue. Arterioscler Thromb Vasc Biol 2010; 30:1576-1582.
84. Meijer RI, Bakker W, Alta CLAF, et al. Perivascular adipose tissue control of insulin-induced vasoreactivity in muscle is impaired in db/db mice. Diabetes 2013; 62:590-598.
85. Withers SB, Bussey CE, Saxton SN, et al. Mechanisms of adiponectinassociated perivascular function in vascular disease. Arterioscler Thromb Vasc Biol 2014; 34:1637-1642.
86. 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.
87. Chang L, Villacorta L, Li RX, et al. Loss of perivascular adipose tissue on peroxisome proliferator-Activated receptor-gamma deletion in smooth muscle cells impairs intravascular thermoregulation and enhances atherosclerosis. Circulation 2012; 126:1067-1078.
88. Meijer RI, Serne EH, Krokmaz I, et al. Insulin-induced changes in skeletal muscle microvascular perfusion are dependent upon perivascular adipose tissue in women. Diabetologia 2015 [Epub ahead of print]. doi:10.1007/s00125-015-3606-8.
89. Moreno PR, Fuster V. New aspects in the pathogenesis of diabetic atherothrombosis. J Am Coll Cardiol 2004; 44:2293-2300.
90. Rensing KL, von der Thusen JH, Weijers EM, et al. Endothelial insulin receptor expression in human atherosclerotic plaques: Linking micro-And macrovascular disease in diabetes? Atherosclerosis 2012; 222:208- 215.