Plaque neovascularization: Defense mechanisms, betrayal, or a war in progress

Annals of the New York Academy of Sciences

Volumn 1254, Issue 1, 2012, Pages 7-17

  Moreno, Pedro R ^a   Purushothaman, Meeranani ^a   Purushothaman, K Raman ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Angiogenesis; Atherosclerosis; Hypoxia; Neovascularization

Indexed keywords

APOLIPOPROTEIN E; BEVACIZUMAB; BILIVERDIN; CARBON MONOXIDE; CD163 ANTIGEN; CHEMOKINE RECEPTOR CCR7; FERROUS ION; FUMAGILLIN; HAPTOGLOBIN; HEME OXYGENASE 1; HEMOGLOBIN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; HYPOCHOLESTEROLEMIC AGENT; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; NANOPARTICLE; PEGAPTANIB; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PLATELET DERIVED GROWTH FACTOR; RANIBIZUMAB; SUNITINIB; TRANSFORMING GROWTH FACTOR BETA1; VASCULOTROPIN;

ANGIOGENESIS; ARTICLE; ATHEROMA; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; BLEEDING; CARDIOMYOPATHY; CARDIOVASCULAR RISK; DIABETES MELLITUS; DISEASE COURSE; DNA POLYMORPHISM; DRUG DELIVERY SYSTEM; ERYTHROCYTE MEMBRANE; GENOTYPE; HUMAN; HYPERCHOLESTEROLEMIA; HYPERTENSION; HYPOXIA; INFLAMMATION; NECROSIS; NEOVASCULARIZATION (PATHOLOGY); NONHUMAN; OXIDATIVE STRESS; THROMBOTIC THROMBOCYTOPENIC PURPURA;

EID: 84860481730     PISSN: 00778923     EISSN: 17496632     Source Type: Book Series    
DOI: 10.1111/j.1749-6632.2012.06497.x     Document Type: Article

References (98)

1. Fishman, G.I., S.S. Chugh, J.P. Dimarco, et al 2010. Sudden cardiac death prediction and prevention: report from a National Heart, Lung, and Blood Institute and Heart Rhythm Society Workshop. Circulation 122: 2335-2348.
2. Roger, V.L., A.S. Go, D.M. Lloyd-Jones, et al 2012. Executive summary:heart disease and stroke statistics-2012 update: a report from the American Heart Association. Circulation 125: 188-197.
3. Zemplenyi, T., D.W. Crawford & M.A. Cole 1989. Adaptation to arterial wall hypoxia demonstrated in vivo with oxygen microcathodes. Atherosclerosis 76: 173-179.
4. Fang, S. & P. Salven 2010. Stem cells in tumor angiogenesis. J. Mol. Cell. Cardiol. 50: 290-295.
5. Potente, M., H. Gerhardt & P. Carmeliet 2011. Basic and therapeutic aspects of angiogenesis. Cell 146: 873-887.
6. Arroyo, A.G. & M.L. Iruela-Arispe 2010. Extracellular matrix, inflammation, and the angiogenic response. Cardiovasc. Res. 86: 226-235.
7. Folkman, J. 2007. Angiogenesis: an organizing principle for drug discovery? Nat. Rev. Drug Discov. 6: 273-286.
8. Sluimer, J.C. & M.J. Daemen 2009. Novel concepts in atherogenesis: angiogenesis and hypoxia in atherosclerosis. J. Pathol. 218: 7-29.
9. Leppanen, O., T. Bjornheden, M. Evaldsson, et al 2006. ATP depletion in macrophages in the core of advanced rabbit atherosclerotic plaques in vivo. Atherosclerosis 188: 323-330.
10. Sluimer, J.C., J.M. Gasc, J.L. van Wanroij, et al 2008. Hypoxia, hypoxia-inducible transcription factor, and macrophages in human atherosclerotic plaques are correlated with intraplaque angiogenesis. J. Am. Coll. Cardiol. 51: 1258-1265.
11. Bahadori, B., E. Uitz, A. Mayer, et al 2010. Polymorphisms of the hypoxia-inducible factor 1 gene and peripheral artery disease. Vasc. Med. 15: 371-374.
12. Carmeliet, P. & R.K. Jain 2011. Molecular mechanisms and clinical applications of angiogenesis. Nature 473: 298-307.
13. Majmundar, A.J., W.J. Wong & M.C. Simon 2010. Hypoxia-inducible factors and the response to hypoxic stress. Mol. Cell. 40: 294-309.
14. Semenza, G.L. 2007. Life with oxygen. Science 318: 62-64.
15. Wenger, R.H. & M. Gassmann 1997. Oxygen(es) and the hypoxia-inducible factor-1. Biol. Chem. 378: 609-616.
16. Mazzone, M., D. Dettori, R. Leite de Oliveira, et al 2009. Heterozygous deficiency of PHD2 restores tumor oxygenation and inhibits metastasis via endothelial normalization. Cell 136: 839-851.
17. Hutter, R., V. Fuster, B. Sauter, C. Valdiviezo, et al 2006. In vitro and in vivo evidence for hypoxia inducible factor 1-alpha expression in macrophages as link between vascular inflammation and angiogenesis. Circulation 114: II 284-II 285.
18. Moreno, P.R., J. Sanz & V. Fuster 2009. Promoting mechanisms of vascular health: circulating progenitor cells, angiogenesis, and reverse cholesterol transport. J. Am. Coll. Cardiol. 53: 2315-2323.
19. Heistad, D.D., M.L. Armstrong & M.L. Marcus 1981. Hyperemia of the aortic wall in atherosclerotic monkeys. Circ. Res. 48: 669-675.
20. Moreno, P.R., K.R. Purushothaman, E. Zias, et al 2006. Neovascularization in human atherosclerosis. Curr. Mol. Med. 6: 457-477.
21. Moreno, P.R., K.R. Purushothaman V. Fuster, et al 2002. Intimomedial interface damage and adventitial inflammation is increased beneath disrupted atherosclerosis in the aorta: implications for plaque vulnerability. Circulation 105: 2504-2511.
22. Moreno, P.R., K.R. Purushothaman, V. Fuster, et al 2004. Plaque neovascularization is increased in ruptured atherosclerotic lesions of human aorta: implications for plaque vulnerability. Circulation 110: 2032-2038.
23. Moreno, P.R., K.R. Purushothaman, M. Sirol, et al 2006. Neovascularization in human atherosclerosis. Circulation 113: 2245-2252.
24. Peters, S.A., S. Dogan, R. Meijer, et al 2011. The use of plaque score measurements to assess changes in atherosclerotic plaque burden induced by lipid-lowering therapy over time: the METEOR study. J. Atheroscler. Thromb. 18: 784-795.
25. Nicholls, S.J., C.M. Ballantyne, P.J. Barter, et al 2011. Effect of two intensive statin regimens on progression of coronary disease. N. Engl. J. Med. 365: 2078-2087.
26. Bot, I., J.W. Jukema, I.M. Lankhuizen, et al 2010. Atorvastatin inhibits plaque development and adventitial neovascularization in ApoE deficient mice independent of plasma cholesterol levels. Atherosclerosis 214: 295-300.
27. Nicholls, S.J., J.M. Borgman, S.E. Nissen, et al 2011. Impact of statins on progression of atherosclerosis: rationale and design of SATURN (study of coronary atheroma by intravascular ultrasound: effect of rosuvastatin versus atorvastatin). Curr. Med. Res. Opin. 27: 1119-1129.
28. Feig, J.E., Y. Shang, N. Rotllan, et al 2011. Statins promote the regression of atherosclerosis via activation of the CCR7-dependent emigration pathway in macrophages. PLoS ONE 6: e28534.
29. Tabas, I. 2010 Macrophage death and defective inflammation resolution in atherosclerosis. Nat. Rev. Immunol. 10: 36-46.
30. Williams, K.J., J.E. Feig & E.A. Fisher 2007. Cellular and molecular mechanisms for rapid regression of atherosclerosis: from bench top to potentially achievable clinical goal. Curr. Opin. Lipidol. 18: 443-450.
31. Williams, K.J., J.E. Feig & E.A. Fisher 2008. Rapid regression of atherosclerosis: insights from the clinical and experimental literature. Nat. Clin. Pract. Cardiovasc. Med. 5: 91-102.
32. Moore, K.J. & I. Tabas 2011. Macrophages in the pathogenesis of atherosclerosis. Cell 145: 341-355.
33. Chinetti-Gbaguidi, G., M. Baron, M.A. Bouhlel, et al 2011. Human atherosclerotic plaque alternative macrophages display low cholesterol handling but high phagocytosis because of distinct activities of the PPARgamma and LXRalpha pathways. Circ. Res. 108: 985-995.
34. Potteaux, S., E.L. Gautier, S.B. Hutchison, et al 2011. Suppressed monocyte recruitment drives macrophage removal from atherosclerotic plaques of Apoe-/- mice during disease regression. J. Clin. Invest. 121: 2025-2036.
35. Randolph, G.J. 2011. Immunology. No need to coax monocytes. Science 332: 1268-1269.
36. Chung, A.S., J. Lee & N. Ferrara 2010. Targeting the tumour vasculature: insights from physiological angiogenesis. Nat. Rev. Cancer 10: 505-514.
37. Folkman, J. & K. Camphausen 2001. Cancer. What does radiotherapy do to endothelial cells? Science 293: 227-228.
38. Folkman, J. & P. A. D'Amore 1996. Blood vessel formation: what is its molecular basis? Cell 87: 1153-1155.
39. Purushothaman, K.R., D. Echeverri, V. Fuster, et al 2003. Neovascularization, inflammation and intra-plaque hemorrhage are increased in advanced human atherosclerosis from patients with diabetes mellitus. Circulation 108: 459.
40. Kockx, M.M., C.K.M. Knaapen, M.W. Bosmans, et al 2003. Phagocytosis and macrophage activation associated with hemorrhagic microvessels in human atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 23: 440-446.
41. Kolodgie, F.D., H.K. Gold, A.P. Burke, et al 2003. Intraplaque hemorrhage and progression of coronary atheroma. N. Engl. J. Med. 349: 2316-2325.
42. Nagy, J.A. & D.R. Senger 2005. VEGF-A, cytoskeletal dynamics, and the pathological vascular phenotype. Exp. Cell. Res. 312: 538-548.
43. Arbustini, E., P. Morbini, A.M. D'Armini, et al 2002. Plaque composition in plexogenic and thromboembolic pulmonary hypertension: the critical role of thrombotic material in pultaceous core formation. Heart 88: 177-182.
44. Takaya, N., C. Yuan, B. Chu, et al. 2005. Presence of intraplaque hemorrhage stimulates progression of carotid atherosclerotic plaques: a high-resolution magnetic resonance imaging study. Circulation 111: 2768-2775.
45. Takaya, N., C. Yuan, B. Chu, et al 2006. Association between carotid plaque characteristics and subsequent ischemic cerebrovascular events: a prospective assessment with MRI-initial results. Stroke 37: 818-823.
46. Gutierrez, J., S.W. Ballinger, V.M. Darley-Usmar, et al 2006. Free radicals, mitochondria, and oxidized lipids: the emerging role in signal transduction in vascular cells. Circ. Res. 99: 924-932.
47. Thomas, C., M.M. Mackey, A.A. Diaz, et al 2009. Hydroxyl radical is produced via the Fenton reaction in submitochondrial particles under oxidative stress: implications for diseases associated with iron accumulation. Redox Rep. 14: 102-108.
48. Cutler, R.G. 2005. Oxidative stress profiling: part I. Its potential importance in the optimization of human health. Ann. N. Y. Acad. Sci. 1055: 93-135.
49. Rother, R.P., L. Bell, P. Hillmen, et al 2005. The clinical sequelae of intravascular hemolysis and extracellular plasma hemoglobin: a novel mechanism of human disease. JAMA 293: 1653-1662.
50. Kristiansen, M., J.H. Graverson, C. Jacobson, et al 2001. Identification of hemoglobin scavenger receptor. Nature 409: 198-201.
51. Langlois, M.R. & J.R. Delanghe 1996. Biological and clinical significance of haptoglobin polymorphism in humans. Clin. Chem. 42: 1589-1600.
52. Melamed-Frank, M., O. Lache, B.I. Enav, et al 2001. Structure-function analysis of the antioxidant properties of haptoglobin. Blood 98: 3693-3698.
53. Guetta, J., M. Strauss, N.S. Levy, et al 2007. Haptoglobin genotype modulates the balance of Th1/Th2 cytokines produced by macrophages exposed to free hemoglobin. Atherosclerosis 191: 48-53.
54. Levy, A.P., J.E. Levy, S. Kalet-Litman, et al 2007. Haptoglobin genotype is a determinant of iron, lipid peroxidation, and macrophage accumulation in the atherosclerotic plaque. Arterioscler. Thromb. Vasc. Biol. 27: 134-140.
55. Asleh, R., S. Marsh, M. Shilkrut, et al 2003. Genetically determined heterogeneity in hemoglobin scavenging and susceptibility to diabetic cardiovascular disease. Circ. Res. 92: 1193-1200.
56. Levy, A.P.A. Roguin, I. Hochberg, et al 2000. Haptoglobin phenotype and vascular complications in patients with diabetes. N. Engl. J. Med. 343: 969-970.
57. Suleiman, M.D. Aronson, R. Asleh, et al 2005. Haptoglobin polymorphism predicts 30-day mortality and heart failure in patients with diabetes and acute myocardial infarction. Diabetes 54: 2802-2806.
58. Levy, A.P., I. Hochberg, K. Jablonski, et al 2002. Haptoglobin phenotype is an independent risk factor for cardiovascular disease in individuals with diabetes: the Strong Heart Study. J. Am. Coll. Cardiol. 40: 1984-1990.
59. Schaer C.A., F. Vallelian, A. Imhof, et al 2007. CD163-expressing monocytes constitute an endotoxin-sensitive Hb clearance compartment within the vascular system. J. Leucocyte Biol. 82: 106-110.
60. Schaer, C.A., G. Schoedon, A. Imhof, et al 2006. Constitutive endocytosis of CD163 mediates hemoglobin-heme uptake and determines the noninflammatory and protective transcriptional response of macrophages to hemoglobin. Circ. Res. 99: 943-950.
61. Schaer, D.J. 2002. The macrophage hemoglobin scavenger receptor CD163 as a genetically determined disease modifying pathway in atherosclerosis. Atherosclerosis 163: 199-201.
62. Philippidis, P., J.C. Mason, B.J. Evans, et al 2004. Hemoglobin scavenger receptor CD163 mediates interleukin-10 release and heme oxygenase-1 synthesis: antiinflammatory monocyte-macrophage responses in vitro, in resolving skin blisters in vivo, and after cardiopulmonary bypass surgery. Circ. Res. 94: 119-126.
63. Schaer, D., F.S. Boretti, A. Hongegger, et al 2001. Molecular cloning and characterization of the mouse CD163 homologue, a highly glucocorticoid-inducible member of the scavenger receptor cysteine-rich family. Immunogenetics 53: 170-177.
64. Siow, R.C., H. Sato, & G.E. Mann 1999. Heme oxygenase-carbon monoxide signalling pathway in atherosclerosis:anti-atherogenic actions of bilirubin and carbon monoxide? Cardiovasc. Res. 41: 385-394.
65. Lin, Q., S. Weis, G. Yang, et al 2007. Heme oxygenase-1 protein localizes to nucleus and activates transcription factors important in oxidative stress. J. Biol. Chemistry. 282: 20621-20633.
66. Hoekstra, K.A., D.V. Godin, J. Kurtu, et al 2003. Heme oxygenase and antioxidant status in cultured aortic endothelial cells isolated from atherosclerosis- susceptible and -resistant Japanese quail. Mol. Cell. Biochem. 252: 253-262.
67. Ahmad, F.K., Z. He & G.L. King 2005. Molecular targets of diabetic cardiovascular complications. Curr. Drug Targets. 6: 487-494.
68. Meerarani, P., A.P. Levy, K.R. Purushothaman, et al 2008. Down-regulation of Heme oxygenase-1 gene expression is associated with decreased ferritin and increased iron deposition in diabetic atherosclerotic plaques. Diabetes 57: A944-A179.
69. Moreno, P.R. & V. Fuster 2004. New aspects in the pathogenesis of diabetic atherothrombosis. J. Am. Coll. Cardiol. 44: 2293-2300.
70. Purushothaman, K.R., P. Meerarani, P. Muntner, et al 2011. Inflammation, neovascularization and intra-plaque hemorrhage are associated with increased reparative collagen content: implication for plaque progression in diabetic atherosclerosis. Vasc. Med. 16: 103-108.
71. Lu, M., M. Kuroki, S. Amano, et al 1998. Advanced glycation end products increase retinal vascular endothelial growth factor expression. J. Clin. Invest. 101: 1219-1224.
72. Chala, E., C. Manes, H. Lliades, et al 2006. Insulin resistance, growth factors and cytokine levels in overweight women with breast cancer before and after chemotherapy. Hormones (Athens). 5: 137-146.
73. Hirata, C., K. Nakano, N. Nakamura, et al 1997. Advanced glycation end products induce expression of vascular endothelial growth factor by retinal Muller cells. Biochem. Biophys. Res. Commun. 236: 712-715.
74. Asleh, R., J. Guetta, S. Kalet-Litman, et al 2005. Haptoglobin genotype- and diabetes-dependent differences in iron-mediated oxidative stress in vitro and in vivo. Circ. Res. 96: 435-441.
75. Moreno, P.R., K.R. Purushothaman, P. Meerarani, et al 2008. Haptoglobin genotype is a major determinant of the amount of iron in the human atherosclerotic plaque. J. Am. Coll. Cardiol. 52: 1049-1051.
76. Moulton, K.S., E. Heller, M.A Konerding, et al 1999. Angiogenesis inhibitors endostatin or TNP-470 reduce intimal neovascularization and plaque growth in apolipoprotein E-deficient mice. Circulation 99: 1726-1732.
77. Crawford, Y. & N. Ferrara 2009. VEGF inhibition: insights from preclinical and clinical studies. Cell Tissue Res. 335: 261-269.
78. Ferrara, N., K.J. Hillan, H.P. Gerber, et al 2004. Discovery and development of bevacizumab, an anti-VEGF antibody for treating cancer. Nat. Rev. Drug Discov. 3: 391-400.
79. Ryan, A.M., D.B. Eppler, K.E. Hagler, et al 1999. Preclinical safety evaluation of rhuMAbVEGF, an antiangiogenic humanized monoclonal antibody. Toxicol. Pathol. 27: 78-86.
80. Jain, R.K. 2001. Normalizing tumor vasculature with anti-angiogenic therapy: a new paradigm for combination therapy. Nat. Med. 7: 987-989.
81. Jain, R.K. 2005. Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy. Science 307: 58-62.
82. Batchelor, T.T., A.G. Sorenson, E. di Tomaso, et al 2007. AZD2171, a pan-VEGF receptor tyrosine kinase inhibitor, normalizes tumor vasculature and alleviates edema in glioblastoma patients. Cancer Cell 11: 83-95.
83. Bottomley, A., C. Coens, F. Efficace, et al 2007. Symptoms and patient-reported well-being: do they predict survival in malignant pleural mesothelioma? A prognostic factor analysis of EORTC-NCIC 08983: randomized phase III study of cisplatin with or without raltitrexed in patients with malignant pleural mesothelioma. J. Clin. Oncol. 25: 5770-5776.
84. Willett, C.G., Y. Boucher, E. di Tomaso, et al 2004. Direct evidence that the VEGF-specific antibody bevacizumab has antivascular effects in human rectal cancer. Nat. Med. 10: 145-147.
85. Willett, C.G., Y. Boucher, D.G. Duda, et al 2005. Surrogate markers for antiangiogenic therapy and dose-limiting toxicities for bevacizumab with radiation and chemotherapy: continued experience of a phase I trial in rectal cancer patients. J. Clin. Oncol. 23: 8136-8139.
86. Winter, P.M., A.M. Neubauer, S.D. Caruthers, et al 2006. Endothelial alpha(v)beta3 integrin-targeted fumagillin nanoparticles inhibit angiogenesis in atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 26: 2103-2109.
87. Vaklavas, C., D. Lenihan, R. Kurzrock, et al 2010 Anti-vascular endothelial growth factor therapies and cardiovascular toxicity: what are the important clinical markers to target? Oncologist 15: 130-141.
88. Gerber, H.P., A.K. Malik, G.P. Solar, et al 2002. VEGF regulates haematopoietic stem cell survival by an internal autocrine loop mechanism. Nature 417: 954-958.
89. Heissig, B., K. Hattori, S. Dias, et al 2002. Recruitment of stem and progenitor cells from the bone marrow niche requires MMP-9 mediated release of kit-ligand. Cell 109: 625-637.
90. Ruzinova, M.B., R.A. Schoer, W. Gerald, et al 2003. Effect of angiogenesis inhibition by Id loss and the contribution of bone-marrow-derived endothelial cells in spontaneous murine tumors. Cancer Cell 4: 277-289.
91. Browder, T.C., E. Butterfield, B.M. Kraling, et al 2000. Antiangiogenic scheduling of chemotherapy improves efficacy against experimental drug-resistant cancer. Cancer Res. 60: 1878-1886.
92. Klement, G., S. Baruchel, J. Rak, et al 2000. Continuous low-dose therapy with vinblastine and VEGF receptor-2 antibody induces sustained tumor regression without overt toxicity. J. Clin. Invest. 105: R15-R24.
93. Sweeney, C.J., K.D. Miller, S.E. Sissons, et al 2001. The antiangiogenic property of docetaxel is synergistic with a recombinant humanized monoclonal antibody against vascular endothelial growth factor or 2-methoxyestradiol but antagonized by endothelial growth factors. Cancer Res. 61: 3369-3372.
94. Jain, R.K., A.V. Finn, F.D. Kolodgie, et al 2007. Antiangiogenic therapy for normalization of atherosclerotic plaque vasculature: a potential strategy for plaque stabilization. Nat. Clin. Pract. Cardiovasc. Med. 4: 491-502.
95. Hausenloy, D.J. & D.M. Yellon 2008. Targeting residual cardiovascular risk: raising high-density lipoprotein cholesterol levels. Heart 94: 706-714.
96. Rubba, P. 2007. Effects of atorvastatin on the different phases of atherogenesis. Drugs 67(Suppl. 1): 17-27.
97. Wilson, S.H., J. Herrmann, L.O. Lerman, et al 2002. Simvastatin preserves the structure of coronary adventitial vasa vasorum in experimental hypercholesterolemia independent of lipid lowering. Circulation 105: 415-418.
98. Park, H.J., D. Kong, L. Iruela-Arispe, et al 2002. 3-hydroxy-3-methylglutaryl coenzyme A reductase inhibitors interfere with angiogenesis by inhibiting the geranylgeranylation of RhoA. Circ. Res. 91: 143-150.