A new murine model of stress-induced complex atherosclerotic lesions

DMM Disease Models and Mechanisms

Volumn 6, Issue 2, 2013, Pages 323-331

  Najafi, Amir H ^a   Aghili, Nima ^a   Tilan, Justin U ^a   Andrews, James A ^a   Peng, Xinzhi ^a   Lassance Soares, Roberta M ^a   Sood, Subeena ^a   Alderman, Lee O ^a   Abe, Ken ^b   Li, Lijun ^b   Kolodgie, Frank D ^c   Virmani, Renu ^c   Zukowska, Zofia ^b,d   Epstein, Stephen E ^a   Burnett, Mary Susan ^a  

^a MEDSTAR RESEARCH INSTITUTE   (United States)

^b GEORGETOWN UNIVERSITY   (United States)

^c Cardiovascular Pathology Institute   (United States)

^d UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPROTEIN E; CHOLESTEROL; NEUROPEPTIDE Y;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERY OCCLUSION; ARTICLE; ATHEROSCLEROTIC PLAQUE; BLEEDING; BLOOD PRESSURE; CHRONIC STRESS; CONTROLLED STUDY; DISEASE COURSE; HISTOPATHOLOGY; INFLAMMATION; MALE; MOUSE; NEOVASCULARIZATION (PATHOLOGY); NONHUMAN; PRIORITY JOURNAL; TISSUE NECROSIS;

ANIMALS; ATHEROSCLEROSIS; BLOOD PRESSURE; CHOLESTEROL; CORONARY STENOSIS; CORTICOSTERONE; DISEASE MODELS, ANIMAL; HEMORRHAGE; HUMANS; INFLAMMATION; MICE; MICE, INBRED C57BL; NECROSIS; NEOVASCULARIZATION, PATHOLOGIC; NEUROPEPTIDE Y; PLAQUE, ATHEROSCLEROTIC; STRESS, PSYCHOLOGICAL;

EID: 84875191364     PISSN: 17548403     EISSN: 17548411     Source Type: Journal    
DOI: 10.1242/dmm.009977     Document Type: Article

References (43)

1. Aikawa, M., Rabkin, E., Okada, Y., Voglic, S. J., Clinton, S. K., Brinckerhoff, C. E., Sukhova, G. K. and Libby, P. (1998). Lipid lowering by diet reduces matrix metalloproteinase activity and increases collagen content of rabbit atheroma: a potential mechanism of lesion stabilization. Circulation 97, 2433-2444. (Pubitemid 28278188)
2. Arbustini, E., Dal Bello, B., Morbini, P., Burke, A. P., Bocciarelli, M., Specchia, G. and Virmani, R. (1999). Plaque erosion is a major substrate for coronary thrombosis in acute myocardial infarction. Heart 82, 269-272. (Pubitemid 29429595)
3. Binder, E. B., Salyakina, D., Lichtner, P., Wochnik, G. M., Ising, M., Pütz, B., Papiol, S., Seaman, S., Lucae, S., Kohli, M. A. et al. (2004). Polymorphisms in FKBP5 are associated with increased recurrence of depressive episodes and rapid response to antidepressant treatment. Nat. Genet. 36, 1319-1325. (Pubitemid 39577942)
4. Cheng, C., Tempel, D., Van Haperen, R., Van der Baan, A., Grosveld, F., Daemen, M. J., Krams, R. and De Crom, R. (2006). Atherosclerotic lesion size and vulnerability are determined by patterns of fluid shear stress. Circulation 113, 2744-2753. (Pubitemid 43947992)
5. Davies, M. J. (2000). The pathophysiology of acute coronary syndromes. Heart 83, 361-366. (Pubitemid 30313346)
6. Falk, E. (1983). Plaque rupture with severe pre-existing stenosis precipitating coronary thrombosis. Characteristics of coronary atherosclerotic plaques underlying fatal occlusive thrombi. Br. Heart J. 50, 127-134. (Pubitemid 13027014)
7. Falk, E., Schwartz, S. M., Galis, Z. S. and Rosenfeld, M. E. (2007). Putative murine models of plaque rupture. Arterioscler. Thromb. Vasc. Biol. 27, 969-972. (Pubitemid 46606733)
8. Finn, A. V., Nakano, M., Narula, J., Kolodgie, F. D. and Virmani, R. (2010). Concept of vulnerable/unstable plaque. Arterioscler. Thromb. Vasc. Biol. 30, 1282-1292.
9. Gössl, M., Versari, D., Mannheim, D., Ritman, E. L., Lerman, L. O. and Lerman, A. (2007). Increased spatial vasa vasorum density in the proximal LAD in hypercholesterolemia - implications for vulnerable plaque-development. Atherosclerosis 192, 246-252. (Pubitemid 46726324)
10. Gu, H., Tang, C., Peng, K., Sun, H. and Yang, Y. (2009). Effects of chronic mild stress on the development of atherosclerosis and expression of toll-like receptor 4 signaling pathway in adolescent apolipoprotein E knockout mice. J. Biomed. Biotechnol. 2009, 613879.
11. Jackson, C. L. (2007). Defining and defending murine models of plaque rupture. Arterioscler. Thromb. Vasc. Biol. 27, 973-977. (Pubitemid 46606734)
12. Jackson, C. L., Bennett, M. R., Biessen, E. A., Johnson, J. L. and Krams, R. (2007). Assessment of unstable atherosclerosis in mice. Arterioscler. Thromb. Vasc. Biol. 27, 714-720. (Pubitemid 46606696)
13. Johnson, J. L. and Jackson, C. L. (2001). Atherosclerotic plaque rupture in the apolipoprotein E knockout mouse. Atherosclerosis 154, 399-406. (Pubitemid 32146612)
14. Johnson, J., Carson, K., Williams, H., Karanam, S., Newby, A., Angelini, G., George, S. and Jackson, C. (2005). Plaque rupture after short periods of fat feeding in the apolipoprotein E-knockout mouse: model characterization and effects of pravastatin treatment. Circulation 111, 1422-1430. (Pubitemid 40396809)
15. Kaijser, L., Pernow, J., Berglund, B., Grubbström, J. and Lundberg, J. M. (1994). Neuropeptide Y release from human heart is enhanced during prolonged exercise in hypoxia. J. Appl. Physiol. 76, 1346-1349. (Pubitemid 24099981)
16. Kolodgie, F. D., Gold, H. K., Burke, A. P., Fowler, D. R., Kruth, H. S., Weber, D. K., Farb, A., Guerrero, L. J., Hayase, M., Kutys, R. et al. (2003). Intraplaque hemorrhage and progression of coronary atheroma. N. Engl. J. Med. 349, 2316-2325. (Pubitemid 37509739)
17. Kuo, L. E., Kitlinska, J. B., Tilan, J. U., Li, L., Baker, S. B., Johnson, M. D., Lee, E. W., Burnett, M. S., Fricke, S. T., Kvetnansky, R. et al. (2007). Neuropeptide Y acts directly in the periphery on fat tissue and mediates stress-induced obesity and metabolic syndrome. Nat. Med. 13, 803-811. (Pubitemid 47038195)
18. Lee, E. W., Michalkiewicz, M., Kitlinska, J., Kalezic, I., Switalska, H., Yoo, P., Sangkharat, A., Ji, H., Li, L., Michalkiewicz, T. et al. (2003). Neuropeptide Y induces ischemic angiogenesis and restores function of ischemic skeletal muscles. J. Clin. Invest. 111, 1853-1862. (Pubitemid 38057730)
19. Li, L., Lee, E. W., Ji, H. and Zukowska, Z. (2003). Neuropeptide Y-induced acceleration of postangioplasty occlusion of rat carotid artery. Arterioscler. Thromb. Vasc. Biol. 23, 1204-1210. (Pubitemid 36871274)
20. Li, L., Jönsson-Rylander, A. C., Abe, K. and Zukowska, Z. (2005). Chronic stress induces rapid occlusion of angioplasty-injured rat carotid artery by activating neuropeptide Y and its Y1 receptors. Arterioscler. Thromb. Vasc. Biol. 25, 2075-2080. (Pubitemid 41416303)
21. Li, L., Cai, X. J., Feng, M., Rong, Y. Y., Zhang, Y. and Zhang, M. (2010). Effect of adiponectin overexpression on stability of preexisting plaques by inducing prolyl-4-hydroxylase expression. Circ. J. 74, 552-559.
22. Malzburg, B. (1937). Mortality among patients with involution melancholia. Am. J. Psychiatry 93, 1231-1238.
23. Mazzolai, L., Duchosal, M. A., Korber, M., Bouzourene, K., Aubert, J. F., Hao, H., Vallet, V., Brunner, H. R., Nussberger, J., Gabbiani, G. et al. (2004). Endogenous angiotensin II induces atherosclerotic plaque vulnerability and elicits a Th1 response in ApoE-/-mice. Hypertension 44, 277-282. (Pubitemid 39167222)
24. McCutcheon, J. E., Fisher, A. S., Guzdar, E., Wood, S. A., Lightman, S. L. and Hunt, S. P. (2008). Genetic background influences the behavioural and molecular consequences of neurokinin-1 receptor knockout. Eur. J. Neurosci. 27, 683-690. (Pubitemid 351239299)
25. Mohler, E. R., 3rd, Sarov-Blat, L., Shi, Y., Hamamdzic, D., Zalewski, A., Macphee, C., Llano, R., Pelchovitz, D., Mainigi, S. K., Osman, H. et al. (2008). Site-specific atherogenic gene expression correlates with subsequent variable lesion development in coronary and peripheral vasculature. Arterioscler. Thromb. Vasc. Biol. 28, 850-855. (Pubitemid 351544098)
26. Moulton, K. S., Heller, E., Konerding, M. A., Flynn, E., Palinski, W. and Folkman, J. (1999). Angiogenesis inhibitors endostatin or TNP-470 reduce intimal neovascularization and plaque growth in apolipoprotein E-deficient mice. Circulation 99, 1726-1732. (Pubitemid 29162486)
27. Moulton, K. S., Vakili, K., Zurakowski, D., Soliman, M., Butterfield, C., Sylvin, E., Lo, K. M., Gillies, S., Javaherian, K. and Folkman, J. (2003). Inhibition of plaque neovascularization reduces macrophage accumulation and progression of advanced atherosclerosis. Proc. Natl. Acad. Sci. USA 100, 4736-4741. (Pubitemid 36457799)
28. Pakala, R., Leborgne, L., Cheneau, E., Chan, R. C., Yazdi, H., Fournadjiev, J., Weber, D., Hellinga, D., Kolodgie, F., Virmani, R. et al. (2003). Radiation-induced atherosclerotic plaque progression in a hypercholesterolemic rabbit: a prospective vulnerable plaque model? Cardiovasc. Radiat. Med. 4, 146-151. (Pubitemid 38230307)
29. Pons, J., Kitlinska, J., Ji, H., Lee, E. W. and Zukowska, Z. (2003). Mitogenic actions of neuropeptide Y in vascular smooth muscle cells: synergetic interactions with the beta-adrenergic system. Can. J. Physiol. Pharmacol. 81, 177-185. (Pubitemid 36398892)
30. Roncal, C., Buysschaert, I., Gerdes, N., Georgiadou, M., Ovchinnikova, O., Fischer, C., Stassen, J. M., Moons, L., Collen, D., De Bock, K. et al. (2010). Short-term delivery of anti-PlGF antibody delays progression of atherosclerotic plaques to vulnerable lesions. Cardiovasc. Res. 86, 29-36.
31. Rosenfeld, M. E., Polinsky, P., Virmani, R., Kauser, K., Rubanyi, G. and Schwartz, S. M. (2000). Advanced atherosclerotic lesions in the innominate artery of the ApoE knockout mouse. Arterioscler. Thromb. Vasc. Biol. 20, 2587-2592.
32. Sasaki, T., Kuzuya, M., Nakamura, K., Cheng, X. W., Shibata, T., Sato, K. and Iguchi, A. (2006). A simple method of plaque rupture induction in apolipoprotein E-deficient mice. Arterioscler. Thromb. Vasc. Biol. 26, 1304-1309. (Pubitemid 44305374)
33. Schwartz, S. M., Galis, Z. S., Rosenfeld, M. E. and Falk, E. (2007). Plaque rupture in humans and mice. Arterioscler. Thromb. Vasc. Biol. 27, 705-713. (Pubitemid 46606695)
34. Van Rossum, E. F., Binder, E. B., Majer, M., Koper, J. W., Ising, M., Modell, S., Salyakina, D., Lamberts, S. W. and Holsboer, F. (2006). Polymorphisms of the glucocorticoid receptor gene and major depression. Biol. Psychiatry 59, 681-688.
35. Virmani, R., Kolodgie, F. D., Burke, A. P., Farb, A. and Schwartz, S. M. (2000). Lessons from sudden coronary death: a comprehensive morphological classification scheme for atherosclerotic lesions. Arterioscler. Thromb. Vasc. Biol. 20, 1262-1275. (Pubitemid 30262927)
36. Virmani, R., Kolodgie, F. D., Burke, A. P., Finn, A. V., Gold, H. K., Tulenko, T. N., Wrenn, S. P. and Narula, J. (2005). Atherosclerotic plaque progression and vulnerability to rupture: angiogenesis as a source of intraplaque hemorrhage. Arterioscler. Thromb. Vasc. Biol. 25, 2054-2061. (Pubitemid 41416300)
37. Williams, H., Johnson, J. L., Carson, K. G. and Jackson, C. L. (2002). Characteristics of intact and ruptured atherosclerotic plaques in brachiocephalic arteries of apolipoprotein E knockout mice. Arterioscler. Thromb. Vasc. Biol. 22, 788-792. (Pubitemid 34517790)
38. Yan, L. L., Liu, K., Matthews, K. A., Daviglus, M. L., Ferguson, T. F. and Kiefe, C. I. (2003). Psychosocial factors and risk of hypertension: the Coronary Artery Risk Development in Young Adults (CARDIA) study. JAMA 290, 2138-2148. (Pubitemid 37432974)
39. Yusuf, S., Reddy, S., Ounpuu, S. and Anand, S. (2001). Global burden of cardiovascular diseases: Part II: variations in cardiovascular disease by specific ethnic groups and geographic regions and prevention strategies. Circulation 104, 2855-2864. (Pubitemid 33126663)
40. Zukowska-Grojec, Z. and Wahlestedt, C. (1993). Origins and actions of Neuropeptide Y in the cardiovascular circulation. Totawa, NJ: Human Press.
41. Zukowska-Grojec, Z., Dayao, E. K., Karwatowska-Prokopczuk, E., Hauser, G. J. and Doods, H. N. (1996). Stress-induced mesenteric vasoconstriction in rats is mediated by neuropeptide Y Y1 receptors. Am. J. Physiol. 270, H796-H800.
42. Zukowska-Grojec, Z., Karwatowska-Prokopczuk, E., Fisher, T. A. and Ji, H. (1998a). Mechanisms of vascular growth-promoting effects of neuropeptide Y: role of its inducible receptors. Regul. Pept. 75-76, 231-238. (Pubitemid 28477532)
43. Zukowska-Grojec, Z., Karwatowska-Prokopczuk, E., Rose, W., Rone, J., Movafagh, S., Ji, H., Yeh, Y., Chen, W. T., Kleinman, H. K., Grouzmann, E. et al. (1998b). Neuropeptide Y: a novel angiogenic factor from the sympathetic nerves and endothelium. Circ. Res. 83, 187-195. (Pubitemid 28354463)