Advances in imaging angiogenesis and inflammation in atherosclerosis

Summary

Advances in imaging technology have provided powerful tools for dissecting the angiogenic and inflammatory aspects of atherosclerosis. Improved technology along with multi-modal approaches has expanded the utilisation of imaging. Recent advances provide the ability to better define structure and development of angiogenic vessels, identify relationships between inflammatory mediators and the vessel wall, validate biological effects of anti-inflammatory and anti-angiogenic drugs, delivery and/or targeting specific molecules to inflammatory regions of atherosclerotic plaques.

Keywords

Atherosclerosis - inflammation - angiogenesis - imaging

• References

• 1 Sadeghi MM. The pathobiology of the vessel wall: implications for imaging. J Nucl Cardiol 2006; 13: 402-414.
• 2 Landmesser U, Hornig B, Drexler H. Endothelial function: a critical determinant in atherosclerosis?. Circulation 2004; 109: II27-33.
• 3 Hansson GK, Libby P. The immune response in atherosclerosis: a double-edged sword. Nat Rev Immunol 2006; 6: 508-519.
• 4 Hansson GK, Robertson AK, Soderberg-Naucler C. Inflammation and atherosclerosis. Annu Rev Pathol 2006; 1: 297-329.
• 5 Naldini A, Carraro F. Role of inflammatory mediators in angiogenesis. Curr Drug Targets Inflamm Allergy 2005; 4: 3-8.
• 6 Ward JR, Wilson HL, Francis SE, Crossman DC, Sabroe I. Translational mini-review series on immunology of vascular disease: inflammation, infections and Toll-like receptors in cardiovascular disease. Clin Exp Immunol 2009; 156: 386-394.
• 7 O’Brien ER, Garvin MR, Dev R. et al. Angiogenesis in human coronary athero-sclerotic plaques. Am J Pathol 1994; 145: 883-894.
• 8 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.
• 9 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.
• 10 Moulton KS, Heller E, Konerding MA, Flynn E, Palinski W, Folkman J. Angiogenesis inhibitors endostatin or TNP-470 reduce intimal neovascularization and plaque growth in apolipoprotein E-deficient mice. Circulation 1999; 99: 1726-1732.
• 11 Moulton KS, Vakili K, Zurakowski D. et al. Inhibition of plaque neovascularization reduces macrophage accumulation and progression of advanced atherosclerosis. Proc Natl Acad Sci USA 2003; 100: 4736-4741.
• 12 Heistad DD, Marcus ML. Role of vasa vasorum in nourishment of the aorta. Blood Vessels 1979; 16: 225-238.
• 13 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.
• 14 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.
• 15 Kwon HM, Sangiorgi G, Ritman EL. et al. Enhanced coronary vasa vasorum neovascularization in experimental hypercholesterolemia. J Clin Invest 1998; 101: 1551-1556.
• 16 Khurana R, Zhuang Z, Bhardwaj S. et al. Angiogenesis-dependent and independent phases of intimal hyperplasia. Circulation 2004; 110: 2436-2443.
• 17 Kolodgie FD, Gold HK, Burke AP. et al. Intraplaque hemorrhage and progression of coronary atheroma. N Engl J Med 2003; 349: 2316-2325.
• 18 Kolodgie FD, Virmani R, Burke AP. et al. Pathologic assessment of the vulnerable human coronary plaque. Heart 2004; 90: 1385-1391.
• 19 Virmani R, Kolodgie FD, Burke AP, Farb A, Schwartz SM. Lessons from sudden coronary death: a comprehensive morphological classification scheme for athero-sclerotic lesions. Arterioscler Thromb Vasc Biol 2000; 20: 1262-1275.
• 20 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: 443-449.
• 21 Kaartinen M, Penttila A, Kovanen PT. Accumulation of activated mast cells in the shoulder region of human coronary atheroma, the predilection site of atheromatous rupture. Circulation 1994; 90: 1669-1678.
• 22 Nagy JA, Benjamin L, Zeng H, Dvorak AM, Dvorak HF. Vascular permeability, vascular hyperpermeability and angiogenesis. Angiogenesis 2008; 11: 109-119.
• 23 Maiellaro K, Taylor WR. The role of the adventitia in vascular inflammation. Cardiovasc Res 2007; 75: 640-648.
• 24 Cook-Mills JM, Deem TL. Active participation of endothelial cells in inflammation. J Leukoc Biol 2005; 77: 487-495.
• 25 Muller WA. Mechanisms of transendothelial migration of leukocytes. Circ Res 2009; 105: 223-230.
• 26 Janabi M, Yamashita S, Hirano K. et al. Oxidized LDL-induced NF-kappa B activation and subsequent expression of proinflammatory genes are defective in monocyte-derived macrophages from CD36-deficient patients. Arterioscler Thromb Vasc Biol 2000; 20: 1953-1960.
• 27 Virella G, Lopes-Virella MF. Atherogenesis and the humoral immune response to modified lipoproteins. Atherosclerosis 2008; 200: 239-246.
• 28 Galkina E, Ley K. Immune and inflammatory mechanisms of atherosclerosis (*). Annu Rev Immunol 2009; 27: 165-197.
• 29 Shi Y, O’Brien JE, Fard A, Mannion JD, Wang D, Zalewski A. Adventitial myofibroblasts contribute to neointimal formation in injured porcine coronary arteries. Circulation 1996; 94: 1655-1664.
• 30 Shi Y, Pieniek M, Fard A, O’Brien J, Mannion JD, Zalewski A. Adventitial remodeling after coronary arterial injury. Circulation 1996; 93: 340-348.
• 31 Wilcox JN, Waksman R, King SB, Scott NA. The role of the adventitia in the arterial response to angioplasty: the effect of intravascular radiation. Int J Radiat Oncol Biol Phys 1996; 36: 789-796.
• 32 Clowes AW, Schwartz SM. Significance of quiescent smooth muscle migration in the injured rat carotid artery. Circ Res 1985; 56: 139-145.
• 33 Houtkamp MA, de Boer OJ, van der Loos CM, van der Wal AC, Becker AE. Adventitial infiltrates associated with advanced atherosclerotic plaques: structural organization suggests generation of local humoral immune responses. J Pathol 2001; 193: 263-269.
• 34 Moos MP, John N, Grabner R. et al. The lamina adventitia is the major site of immune cell accumulation in standard chow-fed apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol 2005; 25: 2386-2391.
• 35 Marxen M, Thornton MM, Chiarot CB. et al. MicroCT scanner performance and considerations for vascular specimen imaging. Med Phys 2004; 31: 305-313.
• 36 Kwon HM, Sangiorgi G, Ritman EL. et al. Adventitial vasa vasorum in balloon-injured coronary arteries: visualization and quantitation by a microscopic three-dimensional computed tomography technique. J Am Coll Cardiol 1998; 32: 2072-2079.
• 37 Kennel SJ, Davis IA, Branning J, Pan H, Kabalka GW, Paulus MJ. High resolution computed tomography and MRI for monitoring lung tumor growth in mice undergoing radioimmunotherapy: correlation with histology. Med Phys 2000; 27: 1101-1107.
• 38 Gossl M, Malyar NM, Rosol M, Beighley PE, Ritman EL. Impact of coronary vasa vasorum functional structure on coronary vessel wall perfusion distribution. Am J Physiol Heart Circ Physiol 2003; 285: H2019-2026.
• 39 Gossl M, Rosol M, Malyar NM. et al. Functional anatomy and hemodynamic characteristics of vasa vasorum in the walls of porcine coronary arteries. Anat Rec A Discov Mol Cell Evol Biol 2003; 272: 526-537.
• 40 Kampschulte M, Brinkmann A, Stieger P. et al. Quantitative CT imaging of the spatio-temporal distribution patterns of vasa vasorum in aortas of apoE(-/-)/ LDL(-/-) double knockout mice. Atherosclerosis 2010; 212: 444-450.
• 41 McQuade P, Knight LC, Welch MJ. Evaluation of 64Cu- and 125I-radiolabeled bitistatin as potential agents for targeting alpha v beta 3 integrins in tumor angio-genesis. Bioconjug Chem 2004; 15: 988-996.
• 42 Wang H, Cai W, Chen K. et al. A new PET tracer specific for vascular endothelial growth factor receptor 2. Eur J Nucl Med Mol Imaging 2007; 34: 2001-2010.
• 43 Wu Y, Zhang X, Xiong Z. et al. micro-PET imaging of glioma integrin {alpha}v{beta}3 expression using (64)Cu-labeled tetrameric RGD peptide. J Nucl Med 2005; 46: 1707-1718.
• 44 Calcagno C, Cornily JC, Hyafil F. et al. Detection of neovessels in atherosclerotic plaques of rabbits using dynamic contrast enhanced MRI and 18 F-FDG PET. Arterioscler Thromb Vasc Biol 2008; 28: 1311-1317.
• 45 Tahara N, Kai H, Ishibashi M. et al. Simvastatin attenuates plaque inflammation: evaluation by fluorodeoxyglucose positron emission tomography. J Am Coll Cardiol 2006; 48: 1825-1831.
• 46 Evans WH, Karnovsky ML. The biochemical basis of phagocytosis. IV. Some aspects of carbohydrate metabolism during phagocytosis. Biochemistry 1962; 1: 159-166.
• 47 Weisdorf DJ, Craddock PR, Jacob HS. Granulocytes utilize different energy sources for movement and phagocytosis. Inflammation 1982; 6: 245-256.
• 48 Shepherd PR, Kahn BB. Glucose transporters and insulin action--implications for insulin resistance and diabetes mellitus. N Engl J Med 1999; 341: 248-257.
• 49 Nahrendorf M, Zhang H, Hembrador S. et al. Nanoparticle PET-CT imaging of macrophages in inflammatory atherosclerosis. Circulation 2008; 117: 379-387.
• 50 Sadeghi MM, Glover DK, Lanza GM, Fayad ZA, Johnson LL. Imaging atherosclerosis and vulnerable plaque. J Nucl Med 51 (Suppl. 01) 51S-65S.
• 51 Achenbach S, Moselewski F, Ropers D. et al. Detection of calcified and noncalcified coronary atherosclerotic plaque by contrast-enhanced, submillimeter multidetector spiral computed tomography: a segment-based comparison with intravascular ultrasound. Circulation 2004; 109: 14-17.
• 52 Hoffmann U, Moselewski F, Cury RC. et al. Predictive value of 16-slice multidetector spiral computed tomography to detect significant obstructive coronary artery disease in patients at high risk for coronary artery disease: patient-versus segment-based analysis. Circulation 2004; 110: 2638-2643.
• 53 Leber AW, Becker A, Knez A. et al. Accuracy of 64-slice computed tomography to classify and quantify plaque volumes in the proximal coronary system: a comparative study using intravascular ultrasound. J Am Coll Cardiol 2006; 47: 672-677.
• 54 Leber AW, Knez A, Becker A. et al. Accuracy of multidetector spiral computed tomography in identifying and differentiating the composition of coronary athero-sclerotic plaques: a comparative study with intracoronary ultrasound. J Am Coll Cardiol 2004; 43: 1241-1247.
• 55 Leber AW, Knez A, von Ziegler F. et al. Quantification of obstructive and non-obstructive coronary lesions by 64-slice computed tomography: a comparative study with quantitative coronary angiography and intravascular ultrasound. J Am Coll Cardiol 2005; 46: 147-154.
• 56 Viles-Gonzalez JF, Poon M, Sanz J. et al. In vivo 16-slice, multidetector-row computed tomography for the assessment of experimental atherosclerosis: comparison with magnetic resonance imaging and histopathology. Circulation 2004; 110: 1467-1472.
• 57 Hyafil F, Cornily JC, Feig JE. et al. Noninvasive detection of macrophages using a nanoparticulate contrast agent for computed tomography. Nat Med 2007; 13: 636-641.
• 58 Hyafil F, Cornily JC, Rudd JH, Machac J, Feldman LJ, Fayad ZA. Quantification of inflammation within rabbit atherosclerotic plaques using the macrophage-specific CT contrast agent N1177: a comparison with 18F-FDG PET/CT and histology. J Nucl Med 2009; 50: 959-965.
• 59 Van Herck JL, De Meyer GR, Martinet W. et al. Multi-slice computed tomography with N1177 identifies ruptured atherosclerotic plaques in rabbits. Basic Res Cardiol 2010; 105: 51-59.
• 60 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.
• 61 Yankeelov TE, Gore JC. Dynamic Contrast Enhanced Magnetic Resonance Imaging in Oncology: Theory, Data Acquisition, Analysis, and Examples. Curr Med Imaging Rev 2009; 3: 91-107.
• 62 Tofts PS, Brix G, Buckley DL. et al. Estimating kinetic parameters from dynamic contrast-enhanced T(1)-weighted MRI of a diffusable tracer: standardized quantities and symbols. J Magn Reson Imaging 1999; 10: 223-232.
• 63 Tofts PS, Kermode AG. Measurement of the blood-brain barrier permeability and leakage space using dynamic MR imaging. 1. Fundamental concepts. Magn Reson Med 1991; 17: 357-367.
• 64 Winter PM, Caruthers SD, Lanza GM, Wickline SA. Quantitative cardiovascular magnetic resonance for molecular imaging. J Cardiovasc Magn Reson 2010; 12: 62.
• 65 Sirol M, Itskovich VV, Mani V. et al. Lipid-rich atherosclerotic plaques detected by gadofluorine-enhanced in vivo magnetic resonance imaging. Circulation 2004; 109: 2890-2896.
• 66 Caruthers SD, Cyrus T, Winter PM, Wickline SA, Lanza GM. Anti-angiogenic perfluorocarbon nanoparticles for diagnosis and treatment of atherosclerosis. Wiley Interdiscip Rev Nanomed Nanobiotechnol 2009; 1: 311-323.
• 67 Kooi ME, Cappendijk VC, Cleutjens KB. et al. Accumulation of ultrasmall super-paramagnetic particles of iron oxide in human atherosclerotic plaques can be detected by in vivo magnetic resonance imaging. Circulation 2003; 107: 2453-2458.
• 68 Kerwin WS, O’Brien KD, Ferguson MS, Polissar N, Hatsukami TS, Yuan C. Inflammation in carotid atherosclerotic plaque: a dynamic contrast-enhanced MR imaging study. Radiology 2006; 241: 459-468.
• 69 Kerwin WS, Oikawa M, Yuan C, Jarvik GP, Hatsukami TS. MR imaging of adventitial vasa vasorum in carotid atherosclerosis. Magn Reson Med 2008; 59: 507-514.
• 70 Mestas J, Ley K. Monocyte-endothelial cell interactions in the development of atherosclerosis. Trends Cardiovasc Med 2008; 18: 228-232.
• 71 Lindner JR. Molecular imaging of myocardial and vascular disorders with ultra-sound. JACC Cardiovasc Imaging 2010; 3: 204-211.
• 72 Lindner JR. Contrast ultrasound molecular imaging of inflammation in cardiovascular disease. Cardiovasc Res 2009; 84: 182-189.
• 73 Lindner JR. Contrast ultrasound molecular imaging: harnessing the power of bubbles. Cardiovasc Res 2009; 83: 615-616.
• 74 Hak S, Reitan NK, Haraldseth O, de Lange Davies C. Intravital microscopy in window chambers: a unique tool to study tumor angiogenesis and delivery of nanoparticles. Angiogenesis 2010; 13: 113-130.
• 75 Koehl GE, Gaumann A, Geissler EK. Intravital microscopy of tumor angiogenesis and regression in the dorsal skin fold chamber: mechanistic insights and preclinical testing of therapeutic strategies. Clin Exp Metastasis 2009; 26: 329-344.
• 76 Fukumura D, Jain RK. Imaging angiogenesis and the microenvironment. APMIS 2008; 116: 695-715.
• 77 Chang K, Francis SA, Aikawa E. et al. Pioglitazone Suppresses Inflammation In Vivo in Murine Carotid Atherosclerosis. Novel Detection by Dual-Target Fluorescence Molecular Imaging. Arterioscler Thromb Vasc Biol 2010; 30: 1933-1939.
• 78 Kato S, Amano H, Ito Y. et al. Effect of erythropoietin on angiogenesis with the increased adhesion of platelets to the microvessels in the hind-limb ischemia model in mice. J Pharmacol Sci 2010; 112: 167-175.
• 79 Kisucka J, Chauhan AK, Patten IS. et al. Peroxiredoxin1 prevents excessive endothelial activation and early atherosclerosis. Circ Res 2008; 103: 598-605.
• 80 McClelland S, Gawaz M, Kennerknecht E. et al. Contribution of cyclooxygenase-1 to thromboxane formation, platelet-vessel wall interactions and atherosclerosis in the ApoE null mouse. Atherosclerosis 2009; 202: 84-91.
• 81 Rotzius P, Soehnlein O, Kenne E. et al. ApoE(-/-)/lysozyme M(EGFP/EGFP) mice as a versatile model to study monocyte and neutrophil trafficking in atherosclerosis. Atherosclerosis 2009; 202: 111-118.
• 82 Rhee SG, Kang SW, Jeong W, Chang TS, Yang KS, Woo HA. Intracellular messenger function of hydrogen peroxide and its regulation by peroxiredoxins. Curr Opin Cell Biol 2005; 17: 183-189.
• 83 Missiou A, Rudolf P, Stachon P. et al. TRAF5 Deficiency Accelerates Atherogenesis in Mice by Increasing Inflammatory Cell Recruitment and Foam Cell Formation. Circ Res 2010; 107: 757-766.
• 84 Ohman MK, Wright AP, Wickenheiser KJ, Luo W, Russo HM, Eitzman DT. Monocyte chemoattractant protein-1 deficiency protects against visceral fat-induced atherosclerosis. Arterioscler Thromb Vasc Biol 2010; 30: 1151-1158.
• 85 Kiessling F, Razansky D, Alves F. Anatomical and microstructural imaging of angiogenesis. Eur J Nucl Med Mol Imaging 2010; 37 (Suppl. 01) S4-19.
• 86 Tozer GM, Ameer-Beg SM, Baker J. et al. Intravital imaging of tumour vascular networks using multiphoton fluorescence microscopy. Adv Drug Deliv Rev 2005; 57: 135-152.