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Review Article

Atherosclerotic plaque development and instability: A dual role for VEGF

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Pages 257-264 | Received 11 Apr 2008, Published online: 08 Jul 2009

References

  • Virmani R, Burke AP, Farb A, Kolodgie FD. Pathology of the vulnerable plaque. J Am Coll Cardiol. 2006; 47(8 Suppl)C13–18
  • Hackett D, Davies G, Maseri A. Pre-existing coronary stenoses in patients with first myocardial infarction are not necessarily severe. Eur Heart J. 1988; 9: 1317–23
  • Kovanen PT, Kaartinen M, Paavonen T. Infiltrates of activated mast cells at the site of coronary atheromatous erosion or rupture in myocardial infarction. Circulation. 1995; 92: 1084–8
  • Ribatti D, Levi-Schaffer F, Kovanen PT. Inflammatory angiogenesis in atherogenesis—a double-edged sword. Ann Med. 2008; 40: 606–21
  • Ross R. Atherosclerosis is an inflammatory disease. Am Heart J. 1999; 138: S419–20
  • Ross R, Glomset JA. The pathogenesis of atherosclerosis (first of two parts). N Engl J Med. 1976; 295: 369–77
  • Ross R. The pathogenesis of atherosclerosis—an update. N Engl J Med. 1986; 314: 488–500
  • Ross R. The pathogenesis of atherosclerosis: a perspective for the 1990s. Nature. 1993; 362: 801–9
  • Ross R. George Lyman Duff Memorial Lecture. Atherosclerosis: a problem of the biology of arterial wall cells and their interactions with blood components. Arteriosclerosis. 1981; 1: 293–311
  • Hayden MR, Tyagi SC. Arteriogenesis: angiogenesis within unstable atherosclerotic plaque—interactions with extracellular matrix. Curr Interv Cardiol Rep. 2000; 2: 218–27
  • Hansson GK. Inflammation, atherosclerosis, and coronary artery disease. N Engl J Med. 2005; 352: 1685–95
  • Hartung D, Schafers M, Fujimoto S, Levkau B, Narula N, Kopka K, et al. Targeting of matrix metalloproteinase activation for noninvasive detection of vulnerable atherosclerotic lesions. Eur J Nucl Med Mol Imaging. 2007; 34(Suppl 1)S1–8
  • van der Wal AC, Becker AE, van der Loos CM, Das PK. Site of intimal rupture or erosion of thrombosed coronary atherosclerotic plaques is characterized by an inflammatory process irrespective of the dominant plaque morphology. Circulation. 1994; 89: 36–44
  • Khatri JJ, Johnson C, Magid R, Lessner SM, Laude KM, Dikalov SI, et al. Vascular oxidant stress enhances progression and angiogenesis of experimental atheroma. Circulation. 2004; 109: 520–5
  • Khurana R, Simons M, Martin JF, Zachary IC. Role of angiogenesis in cardiovascular disease: a critical appraisal. Circulation. 2005; 112: 1813–24
  • Virmani R, Kolodgie FD, Burke AP, Finn AV, Gold HK, Tulenko TN, et al. Atherosclerotic plaque progression and vulnerability to rupture: angiogenesis as a source of intraplaque hemorrhage. Arterioscler Thromb Vasc Biol. 2005; 25: 2054–61
  • 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: 155–9
  • Ferrara N. Vascular endothelial growth factor: basic science and clinical progress. Endocr Rev. 2004; 25: 581–611
  • Hicklin DJ, Ellis LM. Role of the vascular endothelial growth factor pathway in tumor growth and angiogenesis. J Clin Oncol. 2005; 23: 1011–27
  • Relf M, LeJeune S, Scott PA, Fox S, Smith K, Leek R, et al. Expression of the angiogenic factors vascular endothelial cell growth factor, acidic and basic fibroblast growth factor, tumor growth factor beta-1, platelet-derived endothelial cell growth factor, placenta growth factor, and pleiotrophin in human primary breast cancer and its relation to angiogenesis. Cancer Res. 1997; 57: 963–9
  • Stimpfl M, Tong D, Fasching B, Schuster E, Obermair A, Leodolter S, et al. Vascular endothelial growth factor splice variants and their prognostic value in breast and ovarian cancer. Clin Cancer Res. 2002; 8: 2253–9
  • Terman BI, Dougher-Vermazen M, Carrion ME, Dimitrov D, Armellino DC, Gospodarowicz D, et al. Identification of the KDR tyrosine kinase as a receptor for vascular endothelial cell growth factor. Biochem Biophys Res Commun. 1992; 187: 1579–86
  • de Vries C, Escobedo JA, Ueno H, Houck K, Ferrara N, Williams LT. The fms-like tyrosine kinase, a receptor for vascular endothelial growth factor. Science. 1992; 255: 989–91
  • Folkman J. Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat Med. 1995; 1: 27–31
  • Nicosia RF, Nicosia SV, Smith M. Vascular endothelial growth factor, platelet-derived growth factor, and insulin-like growth factor-1 promote rat aortic angiogenesis in vitro. Am J Pathol. 1994; 145: 1023–9
  • Phillips GD, Stone AM, Jones BD, Schultz JC, Whitehead RA, Knighton DR. Vascular endothelial growth factor (rhVEGF165) stimulates direct angiogenesis in the rabbit cornea. In Vivo. 1994; 8: 961–5
  • Tolentino MJ, Miller JW, Gragoudas ES, Chatzistefanou K, Ferrara N, Adamis AP. Vascular endothelial growth factor is sufficient to produce iris neovascularization and neovascular glaucoma in a nonhuman primate. Arch Ophthalmol. 1996; 114: 964–70
  • Gerber HP, Dixit V, Ferrara N. Vascular endothelial growth factor induces expression of the antiapoptotic proteins Bcl-2 and A1 in vascular endothelial cells. J Biol Chem. 1998; 273: 13313–6
  • Gerber HP, McMurtrey A, Kowalski J, Yan M, Keyt BA, Dixit V, et al. Vascular endothelial growth factor regulates endothelial cell survival through the phosphatidylinositol 3'-kinase/Akt signal transduction pathway. Requirement for Flk-1/KDR activation. J Biol Chem. 1998; 273: 30336–43
  • Broxmeyer HE, Cooper S, Li ZH, Lu L, Song HY, Kwon BS, et al. Myeloid progenitor cell regulatory effects of vascular endothelial cell growth factor. Int J Hematol. 1995; 62: 203–15
  • Dvorak HF, Brown LF, Detmar M, Dvorak AM. Vascular permeability factor/vascular endothelial growth factor, microvascular hyperpermeability, and angiogenesis. Am J Pathol. 1995; 146: 1029–39
  • Dvorak HF, Harvey VS, Estrella P, Brown LF, McDonagh J, Dvorak AM. Fibrin containing gels induce angiogenesis. Implications for tumor stroma generation and wound healing. Lab Invest. 1987; 57: 673–86
  • Murata T, Ishibashi T, Inomata H. Immunohistochemical detection of extravasated fibrinogen (fibrin) in human diabetic retina. Graefes Arch Clin Exp Ophthalmol. 1992; 230: 428–31
  • Paul SA, Simons JW, Mabjeesh NJ. HIF at the crossroads between ischemia and carcinogenesis. J Cell Physiol. 2004; 200: 20–30
  • Kumamoto M, Nakashima Y, Sueishi K. Intimal neovascularization in human coronary atherosclerosis: its origin and pathophysiological significance. Hum Pathol. 1995; 26: 450–6
  • Dor Y, Porat R, Keshet E. Vascular endothelial growth factor and vascular adjustments to perturbations in oxygen homeostasis. Am J Physiol Cell Physiol. 2001; 280: C1367–74
  • Semenza GL. Expression of hypoxia-inducible factor 1: mechanisms and consequences. Biochem Pharmacol. 2000; 59: 47–53
  • North S, Moenner M, Bikfalvi A. Recent developments in the regulation of the angiogenic switch by cellular stress factors in tumors. Cancer Lett. 2005; 218: 1–14
  • Namiki A, Brogi E, Kearney M, Kim EA, Wu T, Couffinhal T, et al. Hypoxia induces vascular endothelial growth factor in cultured human endothelial cells. J Biol Chem. 1995; 270: 31189–95
  • de Boer OJ, van der Wal AC, Teeling P, Becker AE. Leucocyte recruitment in rupture prone regions of lipid-rich plaques: a prominent role for neovascularization?. Cardiovasc Res. 1999; 41: 443–9
  • O'Brien KD, Allen MD, McDonald TO, Chait A, Harlan JM, Fishbein D, 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 Invest. 1993; 92: 945–51
  • 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: 672–82
  • Moreno PR, Fuster V. New aspects in the pathogenesis of diabetic atherothrombosis. J Am Coll Cardiol. 2004; 44: 2293–300
  • Moulton KS, Vakili K, Zurakowski D, Soliman M, Butterfield C, Sylvin E, et al. Inhibition of plaque neovascularization reduces macrophage accumulation and progression of advanced atherosclerosis. Proc Natl Acad Sci U S A. 2003; 100: 4736–41
  • Lessner SM, Prado HL, Waller EK, Galis ZS. Atherosclerotic lesions grow through recruitment and proliferation of circulating monocytes in a murine model. Am J Pathol. 2002; 160: 2145–55
  • Zhao Q, Egashira K, Inoue S, Usui M, Kitamoto S, Ni W, et al. Vascular endothelial growth factor is necessary in the development of arteriosclerosis by recruiting/activating monocytes in a rat model of long-term inhibition of nitric oxide synthesis. Circulation. 2002; 105: 1110–5
  • Vlassara H, Fuh H, Donnelly T, Cybulsky M. Advanced glycation endproducts promote adhesion molecule (VCAM-1, ICAM-1) expression and atheroma formation in normal rabbits. Mol Med. 1995; 1: 447–56
  • Wuttge DM, Sirsjo A, Eriksson P, Stemme S. Gene expression in atherosclerotic lesion of ApoE deficient mice. Mol Med. 2001; 7: 383–92
  • Sengoelge G, Fodinger M, Skoupy S, Ferrara I, Zangerle C, Rogy M, et al. Endothelial cell adhesion molecule and PMNL response to inflammatory stimuli and AGE-modified fibronectin. Kidney Int. 1998; 54: 1637–51
  • Pakala R, Watanabe T, Benedict CR. Induction of endothelial cell proliferation by angiogenic factors released by activated monocytes. Cardiovasc Radiat Med. 2002; 3: 95–101
  • McCarthy MJ, Loftus IM, Thompson MM, Jones L, London NJ, Bell PR, et al. Angiogenesis and the atherosclerotic carotid plaque: an association between symptomatology and plaque morphology. J Vasc Surg. 1999; 30: 261–8
  • Tenaglia AN, Buda AJ, Wilkins RG, Barron MK, Jeffords PR, Vo K, et al. Levels of expression of P-selectin, E-selectin, and intercellular adhesion molecule-1 in coronary atherectomy specimens from patients with stable and unstable angina pectoris. Am J Cardiol. 1997; 79: 742–7
  • Celletti FL, Waugh JM, Amabile PG, Brendolan A, Hilfiker PR, Dake MD. Vascular endothelial growth factor enhances atherosclerotic plaque progression. Nat Med. 2001; 7: 425–9
  • Luttun A, Tjwa M, Moons L, Wu Y, Angelillo-Scherrer A, Liao F, et al. Revascularization of ischemic tissues by PlGF treatment, and inhibition of tumor angiogenesis, arthritis and atherosclerosis by anti-Flt1. Nat Med. 2002; 8: 831–40
  • Schmeisser A, Christoph M, Augstein A, Marquetant R, Kasper M, Braun-Dullaeus RC, et al. Apoptosis of human macrophages by Flt-4 signaling: implications for atherosclerotic plaque pathology. Cardiovasc Res. 2006; 71: 774–84
  • Kockx MM, Cromheeke KM, Knaapen MW, Bosmans JM, De Meyer GR, Herman AG, et al. Phagocytosis and macrophage activation associated with hemorrhagic microvessels in human atherosclerosis. Arterioscler Thromb Vasc Biol. 2003; 23: 440–6
  • Ben-Av P, Crofford LJ, Wilder RL, Hla T. Induction of vascular endothelial growth factor expression in synovial fibroblasts by prostaglandin E and interleukin-1: a potential mechanism for inflammatory angiogenesis. FEBS Lett. 1995; 372: 83–7
  • Cohen T, Nahari D, Cerem LW, Neufeld G, Levi BZ. Interleukin 6 induces the expression of vascular endothelial growth factor. J Biol Chem. 1996; 271: 736–41
  • Asahara T, Chen D, Tsurumi Y, Kearney M, Rossow S, Passeri J, et al. Accelerated restitution of endothelial integrity and endothelium-dependent function after phVEGF165 gene transfer. Circulation. 1996; 94: 3291–302
  • Walter DH, Cejna M, Diaz-Sandoval L, Willis S, Kirkwood L, Stratford PW, et al. Local gene transfer of phVEGF-2 plasmid by gene-eluting stents: an alternative strategy for inhibition of restenosis. Circulation. 2004; 110: 36–45
  • Pels K, Deiner C, Coupland SE, Noutsias M, Sutter AP, Schultheiss HP, et al. Effect of adventitial VEGF(165) gene transfer on vascular thickening after coronary artery balloon injury. Cardiovasc Res. 2003; 60: 664–72
  • Fortuin FD, Vale P, Losordo DW, Symes J, DeLaria GA, Tyner JJ, et al. One-year follow-up of direct myocardial gene transfer of vascular endothelial growth factor-2 using naked plasmid deoxyribonucleic acid by way of thoracotomy in no-option patients. Am J Cardiol. 2003; 92: 436–9
  • Losordo DW, Vale PR, Hendel RC, Milliken CE, Fortuin FD, Cummings N, et al. Phase 1/2 placebo-controlled, double-blind, dose-escalating trial of myocardial vascular endothelial growth factor 2 gene transfer by catheter delivery in patients with chronic myocardial ischemia. Circulation. 2002; 105: 2012–8
  • Tio RA, Tan ES, Jessurun GA, Veeger N, Jager PL, Slart RH, et al. PET for evaluation of differential myocardial perfusion dynamics after VEGF gene therapy and laser therapy in end-stage coronary artery disease. J Nucl Med. 2004; 45: 1437–43
  • Laitinen M, Hartikainen J, Hiltunen MO, Eränen J, Kiviniemi M, Närvänen O, et al. Catheter-mediated vascular endothelial growth factor gene transfer to human coronary arteries after angioplasty. Hum Gene Ther. 2000; 11: 263–70
  • Kastrup, J, Jørgensen, E, Rück, A, Tägil, K, Glogar, D, Ruzyllo, W,.; Euroinject One Group, et al. Direct intramyocardial plasmid vascular endothelial growth factor-A165 gene therapy in patients with stable severe angina pectoris A randomized double-blind placebo-controlled study: the Euroinject One trial. J Am Coll Cardiol. 2005;45:982–8.
  • Tio RA, Wijpkema JS, Tan ES, Asselbergs FW, Hospers GA, Jessurun GA, et al. Functional characteristics of coronary vasomotor function following intramyocardial gene therapy with naked DNA encoding for vascular endothelial growth factor165. Endothelium. 2005; 12: 103–6
  • Petrovan RJ, Kaplan CD, Reisfeld RA, Curtiss LK. DNA vaccination against VEGF receptor 2 reduces atherosclerosis in LDL receptor-deficient mice. Arterioscler Thromb Vasc Biol. 2007; 27: 1095–100
  • Leppänen P, Koota S, Kholová I, Koponen J, Fieber C, Eriksson U, et al. Gene transfers of vascular endothelial growth factor-A, vascular endothelial growth factor-B, vascular endothelial growth factor-C, and vascular endothelial growth factor-D have no effects on atherosclerosis in hypercholesterolemic low-density lipoprotein-receptor/apolipoprotein B48-deficient mice. Circulation. 2005; 112: 1347–52
  • Stefanadis C, Toutouzas K, Stefanadi E, Lazaris A, Patsouris E, Kipshidze N. Inhibition of plaque neovascularization and intimal hyperplasia by specific targeting vascular endothelial growth factor with bevacizumab-eluting stent: an experimental study. Atherosclerosis. 2007; 195: 269–76
  • Lucerna M, Zernecke A, de Nooijer R, de Jager SC, Bot I, van der Lans C, et al. Vascular endothelial growth factor-A induces plaque expansion in ApoE knock-out mice by promoting de novo leukocyte recruitment. Blood. 2007; 109: 122–9
  • Hildebrandt HA, Goessl M, Mannheim D, Versari D, Herrmann J, Spendlove D, et al. Differential distribution of vasa vasorum in different vascular beds in humans. Atherosclerosis. 2008; 199: 47–54
  • O'Brien ER, Garvin MR, Dev R, Stewart DK, Hinohara T, Simpson JB, et al. Angiogenesis in human coronary atherosclerotic plaques. Am J Pathol. 1994; 145: 883–94
  • Couffinhal T, Kearney M, Witzenbichler B, Chen D, Murohara T, Losordo DW, et al. Vascular endothelial growth factor/vascular permeability factor (VEGF/VPF) in normal and atherosclerotic human arteries. Am J Pathol. 1997; 150: 1673–85
  • Jain RK, Finn AV, Kolodgie FD, Gold HK, Virmani R. Antiangiogenic therapy for normalization of atherosclerotic plaque vasculature: a potential strategy for plaque stabilization. Nat Clin Pract Cardiovasc Med. 2007; 4: 491–502
  • Winter PM, Morawski AM, Caruthers SD, Fuhrhop RW, Zhang H, Williams TA, et al. Molecular imaging of angiogenesis in early-stage atherosclerosis with alpha(v)beta3-integrin-targeted nanoparticles. Circulation. 2003; 108: 2270–4

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