Assessment of unstable atherosclerosis in mice

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 27, Issue 4, 2007, Pages 714-720

  Jackson, Christopher L ^a,e   Bennett, Martin R ^b   Biessen, Erik A L ^c   Johnson, Jason L ^a   Krams, Rob ^d  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c LEIDEN UNIVERSITY   (Netherlands)

^d VU UNIVERSITY AMSTERDAM   (Netherlands)

^e BRISTOL ROYAL INFIRMARY   (United Kingdom)

Author keywords

Animal models; ApoE knockout mouse; Plaque rupture; Vascular histopathology

Indexed keywords

APOLIPOPROTEIN E; LOW DENSITY LIPOPROTEIN RECEPTOR;

ARTERY INJURY; ARTERY INTIMA PROLIFERATION; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; ATHEROSCLEROTIC PLAQUE RUPTURE; BLEEDING; BRACHIOCEPHALIC TRUNK; ENDOTHELIAL DYSFUNCTION; HUMAN; HYPERCHOLESTEROLEMIA; KNOCKOUT MOUSE; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; REVIEW; THROMBOSIS;

ANIMALS; ATHEROSCLEROSIS; DISEASE MODELS, ANIMAL; HEMORRHAGE; MICE; MICE, TRANSGENIC; RUPTURE, SPONTANEOUS; TERMINOLOGY;

EID: 34247266792     PISSN: 10795642     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.ATV.0000261873.86623.e1     Document Type: Review

References (57)

1. Thompson JS. Atheromata in an inbred strain of mice. J Atheroscler Res. 1969;10:113-122.
2. Roberts A, Thompson JS. Genetic factors in the development of atheroma and on serum total cholesterol levels in inbred mice and their hybrids. Prog Biochem Pharmacol. 1977;13:298-305.
3. Paigen B, Morrow A, Brandon C, Mitchell D, Holmes P. Variation in susceptibility to atherosclerosis among inbred strains of mice. Atherosclerosis. 1985;57:65-73.
4. Paigen B, Morrow A, Holmes PA, Mitchell D, Williams RA. Quantitative assessment of atherosclerotic lesions in mice. Atherosclerosis. 1987;68:231-240.
5. Nishina PM, Verstuyft J, Paigen B. Synthetic low and high fat diets for the study of atherosclerosis in the mouse. J Lipid Res. 1990;31:859-869.
6. Plump AS, Smith JD, Hayek T, Aalto-Setala K, Walsh A, Verstuyft JG, Rubin EM, Breslow JL. Severe hypercholesterolemia and atherosclerosis in apolipoprotein E-deficient mice created by homologous recombination in ES cells. Cell. 1992;71:343-353.
7. Nakashima Y, Plump AS, Raines EW, Breslow JL, Ross R. ApoE-deficient mice develop lesions of all phases of atherosclerosis throughout the arterial tree. Arterioscler Thromb. 1994;14:133-140.
8. Ishibashi S, Goldstein JL, Brown MS, Herz J, Burns DK. Massive xanthomatosis and atherosclerosis in cholesterol-fed low density lipoprotein receptor-negative mice. J Clin Invest. 1994;93:188518-188593.
9. Rosenfeld ME, Polinsky P, Virmani R, Kauser K, Rubanyi G, Schwartz SM. Advanced atherosclerotic lesions in the innominate artery of the apoE knockout mouse. Arterioscler Thromb Vasc Biol. 2000;20:2587-2592.
10. Johnson JL, Jackson CL. The apolipoprotein E knockout mouse: an animal model of atherosclerotic plaque rupture. Atherosclerosis. 2001;154:399-406.
11. 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. 2001;195:257-263.
12. Virmani R, Kolodgie FD, Burke AP, Farb A, Schwartz SM. Lessons from sudden coronary death: a comprehensive morphological classification scheme for atherosclerotic lesions. Arterioscler Thromb Vasc Biol. 2000;20:1262-1275.
13. Burke AP, Kolodgie FD, Farb A, Weber DK, Malcom GT, Smialek J, Virmani R. Healed plaque ruptures and sudden coronary death: evidence that subclinical rupture has a role in plaque progression. Circulation. 2001;103:934-940.
14. Clark E, Graef I, Chasis H. Thrombosis of the aorta and coronary arteries: with special reference to the fibrinoid lesions. Arch Pathol. 1936;22:183-212.
15. Tsakiris DA, Scudder L, Hodivala-Dilke K, Hynes RO, Coller BS. Hemostasis in the mouse (Mus musculus): a review. Thromb Haemost. 1999;81:177-188.
16. Zhu Y, Carmeliet P, Fay WP. Plasminogen activator inhibitor-1 is a major determinant of arterial thrombolysis resistance. Circulation. 1999;99:3050-3055.
17. Bouma BN, Meijers JC. Thrombin-activatable fibrinolysis inhibitor (TAFI, plasma procarboxypeptidase B, procarboxypeptidase R, procarboxypeptidase U). J Thromb Haemost. 2003;1:1566-1574.
18. te Velde EA, Wagenaar GT, Reijerkerk A, Roose-Girma M, Borel Rinkes IH, Voest EE, Bouma BN, Gebbink MF, Meijers JC. Impaired healing of cutaneous wounds and colonic anastomoses in mice lacking thrombin-activatable fibrinolysis inhibitor. J Thromb Haemost. 2003;1:2087-2096.
19. Takano M, Inami S, Ishibashi F, Okamatsu K, Seimiya K, Ohba T, Sakai S, Mizuno K. Angioscopic follow-up study of coronary ruptured plaques in nonculprit lesions. J Am Coll Cardiol. 2005;45:652-658.
20. Friedman M. Pathogenesis of Coronary Artery Disease. McGraw-Hill, New York (1969), 176.
21. Breslow JL. Mouse models of atherosclerosis. Science. 1996;272:685-688.
22. Lusis AJ. Atherosclerosis. Nature. 2000;407:233-241.
23. Macdougall ED, Kramer F, Polinsky P, Barnhart S, Askari B, Johansson F, Varon R, Rosenfeld ME, Oka K, Chan L, Schwartz SM, Bornfeldt KE. Aggressive very low-density lipoprotein (VLDL) and LDL lowering by gene transfer of the VLDL receptor combined with a low-fat diet regimen induces regression and reduces macrophage content in advanced atherosclerotic lesions in LDL receptor-deficient mice. Am J Pathol. 2006;168:2064-2073.
24. Johnson JL, Baker AH, Oka K, Chan L, Newby AC, Jackson CL, George SJ. Suppression of atherosclerotic plaque progression and instability by tissue inhibitor of metalloproteinase-2: involvement of macrophage migration and apoptosis. Circulation. 2006;113:2435-2444.
25. Cilingiroglu M, Oh JH, Sugunan B, Kemp NJ, Kim J, Lee S, Zaatari HN, Escobedo D, Thomsen S, Milner TE, Feldman MD. Detection of vulnerable plaque in a murine model of atherosclerosis with optical coherence tomography. Catheter Cardiovasc Interv. 2006;67:915-923.
26. Rodgers KJ, Watkins DJ, Miller AL, Chan PY, Karanam S, Brissette WH, Long CJ, Jackson CL. Destabilizing role of cathepsin S in murine atherosclerotic plaques. Arterioscler Thromb Vasc Biol. 2006;26:851-856.
27. Li G, Sanders JM, Phan ET, Ley K, Sarembock IJ. Arterial macrophages and regenerating endothelial cells express P-selectin in atherosclerosis-prone apolipoprotein E-deficient mice. Am J Pathol. 2005;167:1511-1518.
28. Johnson JL, George SJ, Newby AC, Jackson CL. Divergent effects of matrix metalloproteinases 3, 7, 9, and 12 on atherosclerotic plaque stability in mouse brachiocephalic arteries. Proc Natl Acad Sci U S A. 2005;102:15575-15580.
29. Moos MP, John N, Grabner R, Nossmann S, Gunther B, Vollandt R, Funk CD, Kaiser B, Habenicht AJ. 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.
30. Mayer LP, Dyer CA, Eastgard RL, Hoyer PB, Banka CL. Atherosclerotic lesion development in a novel ovary-intact mouse model of perimenopause. Arterioscler Thromb Vasc Biol. 2005;25:1910-1916.
31. Jones GT, Jiang F, McCormick SP, Dusting GJ. Elastic lamina defects are an early feature of aortic lesions in the apolipoprotein E knockout mouse. J Vasc Res. 2005;42:237-246.
32. Rattazzi M, Bennett BJ, Bea F, Kirk EA, Ricks JL, Speer M, Schwartz SM, Giachelli CM, Rosenfeld ME. Calcification of advanced atherosclerotic lesions in the innominate arteries of ApoE-deficient mice: potential role of chondrocyte-like cells. Arterioscler Thromb Vasc Biol. 2005;25:1420-1425.
33. Johnson J, Carson K, Williams H, Karanam S, Newby A, Angelini G, George S, Jackson C. Plaque rupture after short periods of fat feeding in the apolipoprotein E-knockout mouse: model characterization and effects of pravastatin treatment. Circulation. 2005;111:1422-1430.
34. Mercer J, Figg N, Stoneman V, Braganza D, Bennett MR. Endogenous p53 protects vascular smooth muscle cells from apoptosis and reduces atherosclerosis in ApoE knockout mice. Circ Res. 2005;96:667-674.
35. Teupser D, Pavlides S, Tan M, Gutierrez-Ramos JC, Kolbeck R, Breslow JL. Major reduction of atherosclerosis in fractalkine (CX3CL1)-deficient mice is at the brachiocephalic artery, not the aortic root. Proc Natl Acad Sci U S A. 2004;101:17795-17800.
36. -/- mice ex vivo. J Magn Reson Imaging. 2004;20:981-989.
37. Park TS, Panek RL, Mueller SB, Hanselman JC, Rosebury WS, Robertson AW, Kindt EK, Homan R, Karathanasis SK, Rekhter MD. Inhibition of sphingomyelin synthesis reduces atherogenesis in apolipoprotein E-knockout mice. Circulation. 2004;110:3465-3471.
38. Bunderson M, Brooks DM, Walker DL, Rosenfeld ME, Coffin JD, Beall HD. Arsenic exposure exacerbates atherosclerotic plaque formation and increases nitrotyrosine and leukotriene biosynthesis. Toxicol Appl Pharmacol. 2004;201:32-39.
39. McAteer MA, Schneider JE, Clarke K, Neubauer S, Channon KM, Choudhury RP. Quantification and 3D reconstruction of atherosclerotic plaque components in apolipoprotein E knockout mice using ex vivo high-resolution MRI. Arterioscler Thromb Vasc Biol. 2004;24:2384-2390.
40. Blessing E, Bea F, Kuo CC, Campbell LA, Chesebro B, Rosenfeld ME. Lesion progression and plaque composition are not altered in older apoE-/- mice lacking tumor necrosis factor-α receptor p55. Atherosclerosis. 2004;176:227-232.
41. Bea F, Blessing E, Bennett BJ, Kuo CC, Campbell LA, Kreuzer J, Rosenfeld ME. Chronic inhibition of cyclooxygenase-2 does not alter plaque composition in a mouse model of advanced unstable atherosclerosis. Cardiovasc Res. 2003;60:198-204.
42. McAteer MA, Schneider JE, Clarke K, Neubauer S, Channon KM, Choudhury RP. Quantification and 3D reconstruction of atherosclerotic plaque components in apolipoprotein E knockout mice using ex vivo high-resolution MRI. Arterioscler Thromb Vasc Biol. 2004;24:2384-2390.
43. Haust MD, More RH. Development of modern theories on the pathogenesis of atherosclerosis. In The Pathogenesis of Atherosclerosis, ed. Geer JC and Wissler RW, Williams and Wilkins, Baltimore, USA (1972).
44. von der Thüsen JH, van Berkel TJ, Biessen EA. Induction of rapid atherogenesis by perivascular carotid collar placement in apolipoprotein E-deficient and low-density lipoprotein receptor-deficient mice. Circulation. 2001;103:1164-1170.
45. Cheng C, Tempel D, van Haperen R, van der Baan A, Grosveld F, Daemen MJ, Krams R, de Crom R. Atherosclerotic lesion size and vulnerability are determined by patterns of fluid shear stress. Circulation. 2006;113:2744-2753.
46. Dekker RJ, van Thienen JV, Rohlena J, de Jager SC, Elderkamp YW, Seppen J, de Vries CJ, Biessen EA, van Berkel TJ, Pannekoek H, Horrevoets AJ. Endothelial KLF2 links local arterial shear stress levels to the expression of vascular tone-regulating genes. Am J Pathol. 2005;167:609-618.
47. -/- mice after adenovirus-mediated transfer of p53. Circulation. 2002;105:2064-2070.
48. Clarke MC, Figg N, Maguire JJ, Davenport AP, Goddard M, Littlewood TD, Bennett MR. Apoptosis of vascular smooth muscle cells induces features of plaque vulnerability in atherosclerosis. Nat Med. 2006;12:1075-1080.
49. Mann J, Davies MJ. Mechanisms of progression in native coronary artery disease: role of healed plaque disruption. Heart. 1999;82:265-268.
50. Sasaki T, Kuzuya M, Nakamura K, Cheng XW, Shibata T, Sato K, Iguchi A. A simple method of plaque rupture induction in apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol. 2006;26:1304-1309.
51. -/- mice and predisposes to an inflammatory plaque phenotype prone to hemorrhage. Am J Pathol. 2006;168:649-658.
52. de Nooijer R, Verkleij CJ, von der Thusen JH, Jukema JW, van der Wall EE, van Berkel TJ, Baker AH, Biessen EA. Lesional overexpression of matrix metalloproteinase-9 promotes intraplaque hemorrhage in advanced lesions but not at earlier stages of atherogenesis. Arterioscler Thromb Vasc Biol. 2006;26:340-346.
53. de Nooijer R, von der Thusen JH, Verkleij CJ, Kuiper J, Jukema JW, van der Wall EE, van Berkel JC, Biessen EA. Overexpression of IL-18 decreases intimal collagen content and promotes a vulnerable plaque phenotype in apolipoprotein-E-deficient mice. Arterioscler Thromb Vasc Biol. 2004;24:2313-2319.
54. Khatri JJ, Johnson C, Magid R, Lessner SM, Laude KM, Dikalov SI, Harrison DG, Sung HJ, Rong Y, Galis ZS. Vascular oxidant stress enhances progression and angiogenesis of experimental atheroma. Circulation. 2004;109:520-525.
55. (-/-) double knockout mice. Arterioscler Thromb Vasc Biol. 2006;26:347-352.
56. Kolodgie FD, Gold HK, Burke AP, Fowler DR, Kruth HS, Weber DK, Farb A, Guerrero LJ, Hayase M, Kutys R, Narula J, Finn AV, Virmani R. Intraplaque hemorrhage and progression of coronary atheroma. N Engl J Med. 2003;349:2316-2325.
57. Pasterkamp G, Virmani R. The erythrocyte: a new player in atheromatous core formation. Heart. 2002;88:115-116.