Animal models of atherosclerosis

European Journal of Pharmacology

Volumn 816, Issue , 2017, Pages 3-13

  Emini Veseli, Besa ^a   Perrotta, Paola ^a   De Meyer, Gregory R A ^a   Roth, Lynn ^a   Van der Donckt, Carole ^a   Martinet, Wim ^a   De Meyer, Guido R Y ^a  

^a UNIVERSITY OF ANTWERP   (Belgium)

Author keywords

Animal models; ApoE; Atherosclerosis; LDL receptor; PCSK9; Plaque rupture

Indexed keywords

APOLIPOPROTEIN E; APOLIPOPROTEIN E3; FIBRILLIN 1; LOW DENSITY LIPOPROTEIN RECEPTOR;

ARTICLE; ATHEROGENESIS; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; BLEEDING; CAROTID ATHEROSCLEROSIS; CHOLESTEROL DIET; CHOLESTEROL METABOLISM; FAMILIAL HYPERCHOLESTEROLEMIA; GENETIC MANIPULATION; HEART INFARCTION; HUMAN; NEW ZEALAND WHITE (RABBIT); NONHUMAN; PIG; PRIMATE; PRIORITY JOURNAL; SUDDEN DEATH; WATANABE HERITABLE HYPERLIPIDEMIC RABBIT; WESTERN DIET; ANIMAL; DISEASE MODEL; GENETICS; METABOLISM; PATHOLOGY;

ANIMALS; ATHEROSCLEROSIS; DISEASE MODELS, ANIMAL; PLAQUE, ATHEROSCLEROTIC;

EID: 85018860404     PISSN: 00142999     EISSN: 18790712     Source Type: Journal    
DOI: 10.1016/j.ejphar.2017.05.010     Document Type: Article

References (114)

1. Akram, O.N., Bernier, A., Petrides, F., Wong, G., Lambert, G., Beyond LDL cholesterol, a new role for PCSK9. Arterioscler. Thromb. Vasc. Biol. 30 (2010), 1279–1281.
2. Al-Mashhadi, R.H., Sorensen, C.B., Kragh, P.M., Christoffersen, C., Mortensen, M.B., Tolbod, L.P., Thim, T., Du, Y., Li, J., Liu, Y., Moldt, B., Schmidt, M., Vajta, G., Larsen, T., Purup, S., Bolund, L., Nielsen, L.B., Callesen, H., Falk, E., Mikkelsen, J.G., Bentzon, J.F., Familial hypercholesterolemia and atherosclerosis in cloned minipigs created by DNA transposition of a human PCSK9 gain-of-function mutant. Sci. Transl. Med., 5, 2013 (166ra1).
3. Atkinson, J.B., Hoover, R.L., Berry, K.K., Swift, L.L., Cholesterol-fed heterozygous Watanabe heritable hyperlipidemic rabbits: a new model for atherosclerosis. Atherosclerosis 78 (1989), 123–136.
4. Baumgartner, C., Brandl, J., Münch, G., Ungerer, M., Rabbit models to study atherosclerosis and its complications – transgenic vascular protein expression in vivo. Prog. Biophys. Mol. Biol. 121 (2016), 131–141.
5. Bentzon, J.F., Falk, E., Atherosclerotic lesions in mouse and man: is it the same disease?. Curr. Opin. Lipidol. 21 (2010), 434–440.
6. Berliner, J.A., Navab, M., Fogelman, A.M., Frank, J.S., Demer, L.L., Edwards, P.A., Watson, A.D., Lusis, A.J., Atherosclerosis: basic mechanisms: oxidation, inflammation, and genetics. Circulation 91 (1995), 2488–2496.
7. Bjorklund, M.M., Hollensen, A.K., Hagensen, M.K., Dagnaes-Hansen, F., Christoffersen, C., Mikkelsen, J.G., Bentzon, J.F., Induction of atherosclerosis in mice and hamsters without germline genetic engineering. Circ. Res. 114 (2014), 1684–1689.
8. Bond, A.R., Jackson, C.L., The fat-fed apolipoprotein E knockout mouse brachiocephalic artery in the study of atherosclerotic plaque rupture. J. Biomed. Biotechnol. 2011 (2011), 1–10.
9. Bonthu, S., Heistad, D.D., Chappell, D.A., Lamping, K.G., Faraci, F.M., Atherosclerosis, vascular remodeling, and impairment of endothelium-dependent relaxation in genetically altered hyperlipidemic mice. Arterioscler. Thromb. Vasc. Biol. 17 (1997), 2333–2340.
10. Borissoff, J.I., Otten, J.J.T., Heeneman, S., Leenders, P., van Oerle, R., Soehnlein, O., Loubele, S.T.B.G., Hamulyák, K., Hackeng, T.M., Daemen, M.J.A.P., Degen, J.L., Weiler, H., Esmon, C.T., van Ryn, J., Biessen, E.A.L., Spronk, H.M.H., ten Cate, H., Genetic and pharmacological modifications of thrombin formation in apolipoprotein E-deficient mice determine atherosclerosis severity and atherothrombosis onset in a neutrophil-dependent manner. PLoS One, 8, 2013, e55784.
11. Breslow, J.L., Transgenic mouse models of lipoprotein metabolism and atherosclerosis. Proc. Natl. Acad. Sci. U. S. A. 90 (1993), 8314–8318.
12. Brousseau, M.E., Hoeg, J.M., Transgenic rabbits as models for atherosclerosis research. J. Lipid Res. 40 (1999), 365–375.
13. Calara, F., Silvestre, M., Casanada, F., Yuan, N., Napoli, C., Palinski, W., Spontaneous plaque rupture and secondary thrombosis in apolipoprotein E-deficient and LDL receptor-deficient mice. J. Pathol. 195 (2001), 257–263.
14. Caligiuri, G., Levy, B., Pernow, J., Thoren, P., Hansson, G.K., Myocardial infarction mediated by endothelin receptor signaling in hypercholesterolemic mice. Proc. Natl. Acad. Sci. U. S. A. 96 (1999), 6920–6924.
15. Cerrone, M., Noorman, M., Lin, X., Chkourko, H., Liang, F.X., van der Nagel, R., Hund, T., Birchmeier, W., Mohler, P., van Veen, T.A., van Rijen, H.V., Delmar, M., Sodium current deficit and arrhythmogenesis in a murine model of plakophilin-2 haploinsufficiency. Cardiovasc. Res. 95 (2012), 460–468.
16. Chen, Y.C., Bui, A.V., Diesch, J., Manasseh, R., Hausding, C., Rivera, J., Haviv, I., Agrotis, A., Htun, N.M., Jowett, J., Hagemeyer, C.E., Hannan, R.D., Bobik, A., Peter, K., A novel mouse model of atherosclerotic plaque instability for drug testing and mechanistic/therapeutic discoveries using gene and MicroRNA expression profiling. Circ. Res. 113 (2013), 252–265.
17. Curtiss, L.K., Boisvert, W.A., Apolipoprotein E and atherosclerosis. Curr. Opin. Lipidol. 11 (2000), 243–251.
18. Defesche, J.C., Low-density lipoprotein receptor—its structure, function, and mutations. Semin. Vasc. Med. 4 (2004), 5–11.
19. Denis, M., Marcinkiewicz, J., Zaid, A., Gauthier, D., Poirier, S., Lazure, C., Seidah, N.G., Prat, A., Gene inactivation of proprotein convertase subtilisin/kexin type 9 reduces atherosclerosis in mice. Circulation 125 (2012), 894–901.
20. Dietrich, H., Hu, Y., Zou, Y., Huemer, U., Metzler, B., Li, C., Mayr, M., Xu, Q., Rapid development of vein graft atheroma in ApoE-deficient mice. Am. J. Pathol. 157 (2000), 659–669.
21. Fan, J., Watanabe, T., Cholesterol-fed and transgenic rabbit models for the study of atherosclerosis. J. Atheroscler. Thromb. 7 (2000), 26–32.
22. Fan, J., Kitajima, S., Watanabe, T., Xu, J., Zhang, J., Liu, E., Chen, Y.E., Rabbit models for the study of human atherosclerosis: from pathophysiological mechanisms to translational medicine. Pharmacol. Ther. 146 (2015), 104–119.
23. Fulop, T., Larbi, A., Fortun, A., Robert, L., Khalil, A., Elastin peptides induced oxidation of LDL by phagocytic cells. Pathol. Biol. (Paris) 53 (2005), 416–423.
24. Fuster, J.J., Castillo, A.I., Zaragoza, C., Ibáñez, B., Andrés, V., Animal models of atherosclerosis. Prog. Mol. Biol. Transl. Sci. Elsevier BV, 2012, 1–23.
25. Gencer, B., Kronenberg, F., Stroes, E.S., Mach, F., Lipoprotein(a): the revenant. Eur. Heart J., 2017.
26. Getz, G.S., Reardon, C.A., Apoprotein E as a lipid transport and signaling protein in the blood, liver, and artery wall. J. Lipid Res. 50:Suppl (2009), S156–S161.
27. Getz, G.S., Reardon, C.A., Animal models of atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 32 (2012), 1104–1115.
28. Gijbels, M.J., van der Cammen, M., van der Laan, L.J., Emeis, J.J., Havekes, L.M., Hofker, M.H., Kraal, G., Progression and regression of atherosclerosis in APOE3-Leiden transgenic mice: an immunohistochemical study. Atherosclerosis 143 (1999), 15–25.
29. Goettsch, C., Hutcheson, J.D., Hagita, S., Rogers, M.A., Creager, M.D., Pham, T., Choi, J., Mlynarchik, A.K., Pieper, B., Kjolby, M., Aikawa, M., Aikawa, E., A single injection of gain-of-function mutant PCSK9 adeno-associated virus vector induces cardiovascular calcification in mice with no genetic modification. Atherosclerosis 251 (2016), 109–118.
30. Gough, P.J., Gomez, I.G., Wille, P.T., Raines, E.W., Macrophage expression of active MMP-9 induces acute plaque disruption in apoE-deficient mice. J. Clin. Invest. 116 (2006), 59–69.
31. Hartvigsen, K., Binder, C.J., Hansen, L.F., Rafia, A., Juliano, J., Horkko, S., Steinberg, D., Palinski, W., Witztum, J.L., Li, A.C., A diet-induced hypercholesterolemic murine model to study atherogenesis without obesity and metabolic syndrome. Arterioscler. Thromb. Vasc. Biol. 27 (2007), 878–885.
32. Hobbs, H.H., Russell, D.W., Brown, M.S., Goldstein, J.L., The LDL receptor locus in familial hypercholesterolemia: mutational analysis of a membrane protein. Annu. Rev. Genet. 24 (1990), 133–170.
33. Hu, J.H., Du, L., Chu, T., Otsuka, G., Dronadula, N., Jaffe, M., Gill, S.E., Parks, W.C., Dichek, D.A., Overexpression of urokinase by plaque macrophages causes histological features of plaque rupture and increases vascular matrix metalloproteinase activity in aged apolipoprotein E-null mice. Circulation 121 (2010), 1637–1644.
34. Huang, Y., Teng, Z., Sadat, U., He, J., Graves, M.J., Gillard, J.H., In vivo MRI-based simulation of fatigue process: a possible trigger for human carotid atherosclerotic plaque rupture. BioMed. Eng. OnLine, 12, 2013, 36.
35. Ishibashi, S., Brown, M.S., Goldstein, J.L., Gerard, R.D., Hammer, R.E., Herz, J., Hypercholesterolemia in low density lipoprotein receptor knockout mice and its reversal by adenovirus-mediated gene delivery. J. Clin. Invest. 92 (1993), 883–893.
36. Ishibashi, S., Goldstein, J.L., Brown, M.S., Herz, J., Burns, D.K., Massive xanthomatosis and atherosclerosis in cholesterol-fed low density lipoprotein receptor-negative mice. J. Clin. Invest. 93 (1994), 1885–1893.
37. Ishibashi, S., Herz, J., Maeda, N., Goldstein, J.L., Brown, M.S., The two-receptor model of lipoprotein clearance: tests of the hypothesis in “knockout” mice lacking the low density lipoprotein receptor, apolipoprotein E, or both proteins. Proc. Natl. Acad. Sci. U. S. A. 91 (1994), 4431–4435.
38. Jawien, J., Nastalek, P., Korbut, R., Mouse models of experimental atherosclerosis. J. Physiol. Pharmacol. 55 (2004), 503–517.
39. Jin, Sx, Shen, Lh, Nie, P., Yuan, W., Hu, Lh, Li, Dd, Chen, Xj, Zhang, Xk, He, B., Endogenous renovascular hypertension combined with low shear stress induces plaque rupture in apolipoprotein E-deficient mice. Arterioscler. Thromb. Vasc. Biol. 32 (2012), 2372–2379.
40. Judge, D.P., Dietz, H.C., Marfan's syndrome. Lancet 366 (2005), 1965–1976.
41. Judge, D.P., Biery, N.J., Keene, D.R., Geubtner, J., Myers, L., Huso, D.L., Sakai, L.Y., Dietz, H.C., Evidence for a critical contribution of haploinsufficiency in the complex pathogenesis of Marfan syndrome. J. Clin. Invest. 114 (2004), 172–181.
42. Kapourchali, F.R., Surendiran, G., Chen, L., Uitz, E., Bahadori, B., Moghadasian, M.H., Animal models of atherosclerosis. World J. Clin. Cases 2 (2014), 126–132.
43. Karper, J.C., de Vries, M.R., van den Brand, B.T., Hoefer, I.E., Fischer, J.W., Jukema, J.W., Niessen, H.W.M., Quax, P.H.A., Toll-like receptor 4 is involved in human and mouse vein graft remodeling, and local gene silencing reduces vein graft disease in hypercholesterolemic APOE*3Leiden mice. Arterioscler. Thromb. Vasc. Biol. 31 (2011), 1033–1040.
44. Kaspar, B.K., Roth, D.M., Lai, N.C., Drumm, J.D., Erickson, D.A., McKirnan, M.D., Hammond, H.K., Myocardial gene transfer and long-term expression following intracoronary delivery of adeno-associated virus. J. Gene Med. 7 (2005), 316–324.
45. Kielty, C.M., Sherratt, M.J., Shuttleworth, C.A., Elastic fibres. J. Cell Sci. 115 (2002), 2817–2828.
46. Knowles, J.W., Maeda, N., Genetic modifiers of atherosclerosis in mice. Arterioscler. Thromb. Vasc. Biol. 20 (2000), 2336–2345.
47. Kockx, M.M., Cromheeke, K.M., Knaapen, M.W., Bosmans, J.M., De Meyer, G.R.Y., Herman, A.G., Bult, H., Phagocytosis and macrophage activation associated with hemorrhagic microvessels in human atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 23 (2003), 440–446.
48. Koenig, W., Khuseyinova, N., Biomarkers of atherosclerotic plaque instability and rupture. Arterioscler. Thromb. Vasc. Biol. 27 (2007), 15–26.
49. Konstantinov, I.E., Jankovic, G.M., Alexander I. Ignatowski: a pioneer in the study of atherosclerosis. Tex. Heart Inst. J. 40 (2013), 246–249.
50. Lardenoye, J.H., Delsing, D.J., de Vries, M.R., Deckers, M.M., Princen, H.M., Havekes, L.M., van Hinsbergh, V.W., van Bockel, J.H., Quax, P.H., Accelerated atherosclerosis by placement of a perivascular cuff and a cholesterol-rich diet in ApoE*3Leiden transgenic mice. Circ. Res. 87 (2000), 248–253.
51. Lardenoye, J.H.P., De Vries, M.R., Grimbergen, J.M., Havekes, L.M., Knaapen, M.W., Kockx, M.M., van Hinsbergh, V.W., van Bockel, J.H., Quax, P.H., Inhibition of accelerated atherosclerosis in vein grafts by placement of external stent in ApoE*3-Leiden transgenic mice. Arterioscler. Thromb. Vasc. Biol. 22 (2002), 1433–1438.
52. Lardenoye, J.H.P., de Vries, M.R., Löwik, C.W., Xu, Q., Dhore, C.R., Cleutjens, J.P., van Hinsbergh, V.W., van Bockel, J.H., Quax, P.H., Accelerated atherosclerosis and calcification in vein grafts: a study in APOE*3 Leiden transgenic mice. Circ. Res. 91 (2002), 577–584.
53. Lawn, R.M., Wade, D.P., Hammer, R.E., Chiesa, G., Verstuyft, J.G., Rubin, E.M., Atherogenesis in transgenic mice expressing human apolipoprotein(a). Nature 360 (1992), 670–672.
54. Lee, Y.T., Lin, H.Y., Chan, Y.W., Li, K.H., To, O.T., Yan, B.P., Liu, T., Li, G., Wong, W.T., Keung, W., Tse, G., Mouse models of atherosclerosis: a historical perspective and recent advances. Lipids Health Dis., 16, 2017, 12.
55. Li, J., Tumanut, C., Gavigan, J.A., Huang, W.J., Hampton, E.N., Tumanut, R., Suen, K.F., Trauger, J.W., Spraggon, G., Lesley, S.A., Liau, G., Yowe, D., Harris, J.L., Secreted PCSK9 promotes LDL receptor degradation independently of proteolytic activity. Biochem. J. 406 (2007), 203–207.
56. Libby, P., Mechanisms of acute coronary syndromes and their implications for therapy. N. Engl. J. Med. 368 (2013), 2004–2013.
57. Lusis, A.J., Atherosclerosis. Nature 407 (2000), 233–241.
58. Lutgens, E., Daemen, M., Kockx, M., Doevendans, P., Hofker, M., Havekes, L., Wellens, H., de Muinck, E.D., Atherosclerosis in APOE*3-Leiden transgenic mice: from proliferative to atheromatous stage. Circulation 99 (1999), 276–283.
59. van den Maagdenberg, A.M., Hofker, M.H., Krimpenfort, P.J., de Bruijn, I., van Vlijmen, B., van der Boom, H., Havekes, L.M., Frants, R.R., Transgenic mice carrying the apolipoprotein E3-Leiden gene exhibit hyperlipoproteinemia. J. Biol. Chem. 268 (1993), 10540–10545.
60. Mahley, R., Apolipoprotein E: cholesterol transport protein with expanding role in cell biology. Science 240 (1988), 622–630.
61. Marais, A.D., Familial hypercholesterolaemia. Clin. Biochem. Rev. 25 (2004), 49–68.
62. Mariko, B., Pezet, M., Escoubet, B., Bouillot, S., Andrieu, J.-P., Starcher, B., Quaglino, D., Jacob, M.-P., Huber, P., Ramirez, F., Faury, G., Fibrillin-1 genetic deficiency leads to pathological ageing of arteries in mice. J. Pathol. 224 (2011), 33–44.
63. Medley, T.L., Cole, T.J., Gatzka, C.D., Wang, W.Y., Dart, A.M., Kingwell, B.A., Fibrillin-1 genotype is associated with aortic stiffness and disease severity in patients with coronary artery disease. Circulation 105 (2002), 810–815.
64. Meir, K.S., Leitersdorf, E., Atherosclerosis in the apolipoprotein E-deficient mouse: a decade of progress. Arterioscler. Thromb. Vasc. Biol. 24 (2004), 1006–1014.
65. Moulton, K.S., Olsen, B.R., Sonn, S., Fukai, N., Zurakowski, D., Zeng, X., Loss of collagen XVIII enhances neovascularization and vascular permeability in atherosclerosis. Circulation 110 (2004), 1330–1336.
66. Nakashima, Y., Plump, A.S., Raines, E.W., Breslow, J.L., Ross, R., ApoE-deficient mice develop lesions of all phases of atherosclerosis throughout the arterial tree. Arterioscler. Thromb. Vasc. Biol. 14 (1994), 133–140.
67. Ni, M., Chen, W.Q., Zhang, Y., Animal models and potential mechanisms of plaque destabilisation and disruption. Heart 95 (2009), 1393–1398.
68. Niimi, M., Yang, D., Kitajima, S., Ning, B., Wang, C., Li, S., Liu, E., Zhang, J., Eugene Chen, Y., Fan, J., ApoE knockout rabbits: a novel model for the study of human hyperlipidemia. Atherosclerosis 245 (2016), 187–193.
69. Ning, B., Wang, X., Yu, Y., Waqar, A.B., Yu, Q., Koike, T., Shiomi, M., Liu, E., Wang, Y., Fan, J., High-fructose and high-fat diet-induced insulin resistance enhances atherosclerosis in Watanabe heritable hyperlipidemic rabbits. Nutr. Metab. (Lond. ), 12, 2015.
70. Niu, Y., Shen, B., Cui, Y., Chen, Y., Wang, J., Wang, L., Kang, Y., Zhao, X., Si, W., Li, W., Xiang, Andy, P., Zhou, J., Guo, X., Bi, Y., Si, C., Hu, B., Dong, G., Wang, H., Zhou, Z., Li, T., Tan, T., Pu, X., Wang, F., Ji, S., Zhou, Q., Huang, X., Ji, W., Sha, J., Generation of gene-modified cynomolgus monkey via Cas9/RNA-mediated gene targeting in one-cell embryos. Cell 156 (2014), 836–843.
71. de Nooijer, R., Verkleij, C.J., von der Thüsen, J.H., Jukema, J.W., van der Wall, E.E., van Berkel, T.J., Baker, A.H., Biessen, E.A., Lesional overexpression of matrix metalloproteinase-9 Promotes intraplaque hemorrhage in advanced lesions but not at earlier stages of atherogenesis. Arterioscler. Thromb. Vasc. Biol. 26 (2005), 340–346.
72. Piedrahita, J.A., Zhang, S.H., Hagaman, J.R., Oliver, P.M., Maeda, N., Generation of mice carrying a mutant apolipoprotein E gene inactivated by gene targeting in embryonic stem cells. PNAS 89 (1992), 4471–4475.
73. Plump, A.S., Breslow, J.L., Apolipoprotein E and the apolipoprotein E-deficient mouse. Annu. Rev. Nutr. 15 (1995), 495–518.
74. Plump, A.S., Lum, P.Y., Genomics and cardiovascular drug development. J. Am. Coll. Cardiol. 53 (2009), 1089–1100.
75. Plump, A.S., Smith, J.D., Hayek, T., Aalto-Setälä, K., Walsh, A., Verstuyft, J.G., Rubin, E.M., Breslow, J.L., Severe hypercholesterolemia and atherosclerosis in apolipoprotein E-deficient mice created by homologous recombination in ES cells. Cell 71 (1992), 343–353.
76. Rademakers, T., Douma, K., Hackeng, T.M., Post, M.J., Sluimer, J.C., Daemen, M.J.A.P., Biessen, E.A.L., Heeneman, S., van Zandvoort, M.A.M.J., Plaque-associated vasa vasorum in aged apolipoprotein E-deficient mice exhibit proatherogenic functional features in vivo. Arterioscler. Thromb. Vasc. Biol. 33 (2013), 249–256.
77. Raffetto, J.D., Khalil, R.A., Matrix metalloproteinases and their inhibitors in vascular remodeling and vascular disease. Biochem. Pharmacol. 75 (2008), 346–359.
78. Rattazzi, M., Bennett, B.J., Bea, F., Kirk, E.A., Ricks, J.L., Speer, M., Schwartz, S.M., Giachelli, C.M., Rosenfeld, M.E., Calcification of advanced atherosclerotic lesions in the innominate arteries of ApoE-deficient mice: potential role of chondrocyte-like cells. Arterioscler. Thromb. Vasc. Biol. 25 (2005), 1420–1425.
79. Reddick, R.L., Zhang, S.H., Maeda, N., Atherosclerosis in mice lacking apo E. evaluation of lesional development and progression [publishederratum appears in Arterioscler Thromb 1994 may; 14(5):839]. Arterioscler. Thromb. Vasc. Biol. 14 (1994), 141–147.
80. Roche-Molina, M., Sanz-Rosa, D., Cruz, F.M., Garcia-Prieto, J., Lopez, S., Abia, R., Muriana, F.J., Fuster, V., Ibanez, B., Bernal, J.A., Induction of sustained hypercholesterolemia by single adeno-associated virus-mediated gene transfer of mutant hPCSK9. Arterioscler. Thromb. Vasc. Biol. 35 (2015), 50–59.
81. Ross, R., Cell biology of atherosclerosis. Annu Rev. Physiol. 57 (1995), 791–804.
82. Roth, L., Rombouts, M., Schrijvers, D.M., Lemmens, K., De Keulenaer, G.W., Martinet, W., De Meyer, G.R.Y., Chronic intermittent mental stress promotes atherosclerotic plaque vulnerability, myocardial infarction and sudden death in mice. Atherosclerosis 242 (2015), 288–294.
83. Roth, L., Van Dam, D., Van der Donckt, C., Schrijvers, D.M., Lemmens, K., Van Brussel, I., De Deyn, P.P., Martinet, W., De Meyer, G.R.Y., Impaired gait pattern as a sensitive tool to assess hypoxic brain damage in a novel mouse model of atherosclerotic plaque rupture. Physiol. Behav. 139 (2015), 397–402.
84. Roth, L., Rombouts, M., Schrijvers, D.M., Martinet, W., De Meyer, G.R.Y., Cholesterol-independent effects of atorvastatin prevent cardiovascular morbidity and mortality in a mouse model of atherosclerotic plaque rupture. Vasc. Pharmacol. 80 (2016), 50–58.
85. Sakakura, K., Nakano, M., Otsuka, F., Ladich, E., Kolodgie, F.D., Virmani, R., Pathophysiology of atherosclerosis plaque progression. Heart Lung Circ. 22 (2013), 399–411.
86. Sasaki, T., Kuzuya, M., Nakamura, K., Cheng, X.W., Shibata, T., Sato, K., Iguchi, A., A simple method of plaque rupture induction in apolipoprotein E-deficient mice. Arterioscler. Thromb. Vasc. Biol. 26 (2006), 1304–1309.
87. Schwartz, S.M., Galis, Z.S., Rosenfeld, M.E., Falk, E., Plaque Rupture in Humans and Mice. Arterioscler. Thromb. Vasc. Biol. 27 (2007), 705–713.
88. Sehayek, E., Shefer, S., Nguyen, L.B., Ono, J.G., Merkel, M., Breslow, J.L., Apolipoprotein E regulates dietary cholesterol absorption and biliary cholesterol excretion: studies in C57BL/6 apolipoprotein E knockout mice. PNAS 97 (2000), 3433–3437.
89. Shim, J., Al-Mashhadi, R.H., Sorensen, C.B., Bentzon, J.F., Large animal models of atherosclerosis—new tools for persistent problems in cardiovascular medicine. J. Pathol. 238 (2016), 257–266.
90. Silvestre-Roig, C., de Winther, M.P., Weber, C., Daemen, M.J., Lutgens, E., Soehnlein, O., Atherosclerotic plaque destabilization. Circ. Res. 114 (2014), 214–226.
91. Slager, C.J., Wentzel, J.J., Gijsen, F.J.H., Thury, A., van der Wal, A.C., Schaar, J.A., Serruys, P.W., The role of shear stress in the destabilization of vulnerable plaques and related therapeutic implications. Nat. Clin. Pract. Cardiovasc. Med. 2 (2005), 456–464.
92. Sluimer, J.C., Kolodgie, F.D., Bijnens, A.P.J.J., Maxfield, K., Pacheco, E., Kutys, B., Duimel, H., Frederik, P.M., van Hinsbergh, V.W.M., Virmani, R., Daemen, M.J.A.P., Thin-walled microvessels in human coronary atherosclerotic plaques show incomplete endothelial junctions. J. Am. Coll. Cardiol. 53 (2009), 1517–1527.
93. Smith, J.D., Breslow, J.L., The emergence of mouse models of atherosclerosis and their relevance to clinical research. J. Intern. Med. 242 (1997), 99–109.
94. Suhy, D.A., Kao, S.C., Mao, T., Whiteley, L., Denise, H., Souberbielle, B., Burdick, A.D., Hayes, K., Wright, J.F., Lavender, H., Roelvink, P., Kolykhalov, A., Brady, K., Moschos, S.A., Hauck, B., Zelenaia, O., Zhou, S., Scribner, C., High, K.A., Renison, S.H., Corbau, R., Safe, long-term hepatic expression of anti-HCV shRNA in a nonhuman primate model. Mol. Ther. 20 (2012), 1737–1749.
95. Tabas, I., García-Cardeña, G., Owens, G.K., Recent insights into the cellular biology of atherosclerosis. J. Cell Biol. 209 (2015), 13–22.
96. Van der Donckt, C., Roth, L., Vanhoutte, G., Blockx, I., Bink, D.I., Ritz, K., Pintelon, I., Timmermans, J.P., Bauters, D., Martinet, W., Daemen, M.J., Verhoye, M., De Meyer, G.R.Y., Fibrillin-1 impairment enhances blood–brain barrier permeability and xanthoma formation in brains of apolipoprotein E-deficient mice. Neuroscience 295 (2015), 11–22.
97. Van der Donckt, C., Van Herck, J.L., Schrijvers, D.M., Vanhoutte, G., Verhoye, M., Blockx, I., Van Der Linden, A., Bauters, D., Lijnen, H.R., Sluimer, J.C., Roth, L., Van Hove, C.E., Fransen, P., Knaapen, M.W., Hervent, A.S., De Keulenaer, G.W., Bult, H., Martinet, W., Herman, A.G., De Meyer, G.R.Y., Elastin fragmentation in atherosclerotic mice leads to intraplaque neovascularization, plaque rupture, myocardial infarction, stroke, and sudden death. Eur. Heart J. 36 (2015), 1049–1058.
98. Van Herck, J.L., De Meyer, G.R.Y., Martinet, W., Van Hove, C.E., Foubert, K., Theunis, M.H., Apers, S., Bult, H., Vrints, C.J., Herman, A.G., Impaired fibrillin-1 function promotes features of plaque instability in apolipoprotein E-deficient mice. Circulation 120 (2009), 2478–2487.
99. van Vlijmen, B.J., van den Maagdenberg, A.M., Gijbels, M.J., van der Boom, H., HogenEsch, H., Frants, R.R., Hofker, M.H., Havekes, L.M., Diet-induced hyperlipoproteinemia and atherosclerosis in apolipoprotein E3-Leiden transgenic mice. J. Clin. Invest 93 (1994), 1403–1410.
100. VanderLaan, P.A., Reardon, C.A., Getz, G.S., Site specificity of atherosclerosis: site-selective responses to atherosclerotic modulators. Arterioscler. Thromb. Vasc. Biol. 24 (2004), 12–22.
101. Véniant, M.M., Withycombe, S., Young, S.G., Lipoprotein size and atherosclerosis susceptibility in Apoe-/- and Ldlr-/- mice. Arterioscler. Thromb. Vasc. Biol. 21 (2001), 1567–1570.
102. Véniant, M.M., Sullivan, M.A., Kim, S.K., Ambroziak, P., Chu, A., Wilson, M.D., Hellerstein, M.K., Rudel, L.L., Walzem, R.L., Young, S.G., Defining the atherogenicity of large and small lipoproteins containing apolipoprotein B100. J. Clin. Invest. 106 (2000), 1501–1510.
103. Virmani, R., Kolodgie, F.D., Burke, A.P., Finn, A.V., Gold, H.K., Tulenko, T.N., Wrenn, S.P., Narula, J., Atherosclerotic plaque progression and vulnerability to rupture: angiogenesis as a source of intraplaque hemorrhage. Arterioscler. Thromb. Vasc. Biol. 25 (2005), 2054–2061.
104. von der Thusen, J.H., van Berkel, T.J., Biessen, E.A., Induction of rapid atherogenesis by perivascular carotid collar placement in apolipoprotein E-deficient and low-density lipoprotein receptor-deficient mice. Circulation 103 (2001), 1164–1170.
105. von der Thusen, J.H., van Vlijmen, B.J.M., Hoeben, R.C., Kockx, M.M., Havekes, L.M., van Berkel, T.J.C., Biessen, E.A.L., Induction of atherosclerotic plaque rupture in apolipoprotein E-/- mice after adenovirus-mediated transfer of p53. Circulation 105 (2002), 2064–2070.
106. de Vries, M.R., Simons, K.H., Jukema, J.W., Braun, J., Quax, P.H.A., Vein graft failure: from pathophysiology to clinical outcomes. Nat. Rev. Cardiol. 13 (2016), 451–470.
107. Watanabe, Y., Serial inbreeding of rabbits with hereditary hyperlipidemia (WHHL-rabbit). Atherosclerosis 36 (1980), 261–268.
108. Williams, H., Characteristics of intact and ruptured atherosclerotic plaques in brachiocephalic arteries of apolipoprotein E knockout mice. Arterioscler. Thromb. Vasc. Biol. 22 (2002), 788–792.
109. Witting, P.K., Pettersson, K., Ostlund-Lindqvist, A.M., Westerlund, C., Eriksson, A.W., Stocker, R., Inhibition by a coantioxidant of aortic lipoprotein lipid peroxidation and atherosclerosis in apolipoprotein E and low density lipoprotein receptor gene double knockout mice. FASEB J. 13 (1999), 667–675.
110. Ylä-Herttuala, S., Bentzon, J.F., Daemen, M., Falk, E., Garcia-Garcia, H.M., Herrmann, J., Hoefer, I., Jukema, J.W., Krams, R., Kwak, B.R., Marx, N., Naruszewicz, M., Newby, A., Pasterkamp, G., Serruys, P.W.J.C., Waltenberger, J., Weber, C., Tokgözoglu, L., Stabilisation of atherosclerotic plaques. Thromb. Haemost. 106 (2011), 1–19.
111. Zadelaar, S., Kleemann, R., Verschuren, L., de Vries-Van der Weij, J., van der Hoorn, J., Princen, H.M., Kooistra, T., Mouse models for atherosclerosis and pharmaceutical modifiers. Arterioscler. Thromb. Vasc. Biol. 27 (2007), 1706–1721.
112. Zhang, S.H., Reddick, R.L., Piedrahita, J.A., Maeda, N., Spontaneous hypercholesterolemia and arterial lesions in mice lacking apolipoprotein E. Science 258 (1992), 468–471.
113. Zou, Y., Dietrich, H., Hu, Y., Metzler, B., Wick, G., Xu, Q., Mouse model of venous bypass graft arteriosclerosis. Am. J. Pathol. 153 (1998), 1301–1310.
114. Zsebo, K., Yaroshinsky, A., Rudy, J.J., Wagner, K., Greenberg, B., Jessup, M., Hajjar, R.J., Long-term effects of AAV1/SERCA2a gene transfer in patients with severe heart failure: analysis of recurrent cardiovascular events and mortality. Circ. Res. 114 (2014), 101–108.