Progression and Characterization of the Accelerated Atherosclerosis in Iliac Artery of New Zealand White Rabbits: Effect of Simvastatin

Journal of Cardiovascular Pharmacology

Volumn 69, Issue 5, 2017, Pages 314-325

  Kanshana, Jitendra S ^a   Khanna, Vivek ^a   Singh, Vishal ^a   Jain, Manish ^a   Misra, Ankita ^a   Kumar, Sachin ^a   Farooqui, Mariya ^a   Barthwal, Manoj K ^a   Dikshit, Madhu ^a  

^a CENTRAL DRUG RESEARCH INSTITUTE   (India)

Author keywords

atherosclerosis progression; balloon injury; iliac artery; New Zealand White rabbit

Indexed keywords

ACETYLCHOLINE; ALPHA ACTIN; ALPHA SMOOTH MUSCLE ACTIN; ARACHIS OIL; CD68 ANTIGEN; CHOLESTEROL; COLLAGEN TYPE 1; COLLAGEN TYPE 3; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GAMMA INTERFERON; GELATINASE B; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; INTERLEUKIN 10; LOW DENSITY LIPOPROTEIN CHOLESTEROL; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; PHENYLEPHRINE; PROTEOGLYCAN; SIMVASTATIN; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TRANSFORMING GROWTH FACTOR BETA1; TRIACYLGLYCEROL; TUMOR NECROSIS FACTOR; VASCULAR CELL ADHESION MOLECULE 1; AUTACOID; BIOLOGICAL MARKER; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; LIPID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERIAL WALL THICKNESS; ARTICLE; ATHEROGENIC DIET; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; CELL INFILTRATION; CHOLESTEROL BLOOD LEVEL; CHOLESTEROL DIET; CONTROLLED STUDY; DISEASE COURSE; ENDOTHELIAL DYSFUNCTION; EXPERIMENTAL BALLOON CATHETER INJURY; EXPERIMENTAL RABBIT; EXTRACELLULAR MATRIX; FOAM CELL; HISTOPATHOLOGY; HYPERTRIGLYCERIDEMIA; ILIAC ARTERY ATHEROSCLEROSIS; INFLAMMATION; MACROPHAGE; MALE; NEW ZEALAND WHITE (RABBIT); NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION; TREATMENT DURATION; TRIACYLGLYCEROL BLOOD LEVEL; UPREGULATION; VASOCONSTRICTION; VASODILATATION; ANIMAL; BLOOD; DISEASE EXACERBATION; DISEASE MODEL; DRUG EFFECTS; ILIAC ARTERY; LEPORIDAE; LIPID DIET; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PERCUTANEOUS TRANSLUMINAL ANGIOPLASTY; TIME FACTOR; VASCULAR ENDOTHELIUM; VASCULAR REMODELING;

ANGIOPLASTY, BALLOON; ANIMALS; ATHEROSCLEROSIS; BIOMARKERS; DIET, HIGH-FAT; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; ENDOTHELIUM, VASCULAR; EXTRACELLULAR MATRIX; HYDROXYMETHYLGLUTARYL-COA REDUCTASE INHIBITORS; ILIAC ARTERY; INFLAMMATION MEDIATORS; LIPIDS; MACROPHAGES; MALE; PLAQUE, ATHEROSCLEROTIC; RABBITS; SIMVASTATIN; TIME FACTORS; VASCULAR REMODELING; VASOCONSTRICTION; VASODILATION;

EID: 85013054825     PISSN: 01602446     EISSN: 15334023     Source Type: Journal    
DOI: 10.1097/FJC.0000000000000477     Document Type: Article

References (65)

1. Singh V, Tiwari RL, Dikshit M, et al. Models to study atherosclerosis: A mechanistic insight. Curr Vasc Pharmacol. 2009;7:75-109.
2. Dornas WC, Oliveira TT, Augusto LE, et al. Experimental atherosclerosis in rabbits. Arq Bras Cardiol. 2010;95:272-278.
3. Phinikaridou A, Hallock KJ, Qiao Y, et al. A robust rabbit model of human atherosclerosis and atherothrombosis. J Lipid Res. 2009;50:787-797.
4. Waksman R, McEwan PE, Moore TI, et al. PhotoPoint photodynamic therapy promotes stabilization of atherosclerotic plaques and inhibits plaque progression. J Am Coll Cardiol. 2008;52:1024-1032.
5. Nakazawa G, Finn AV, Ladich E, et al. Drug-eluting stent safety: findings from preclinical studies. Expert Rev Cardiovasc Ther. 2008;6:1379-1391.
6. Pasterkamp G, Schoneveld AH, Hillen B, et al. Is plaque formation in the common carotid artery representative for plaque formation and luminal stenosis in other atherosclerotic peripheral arteries A post mortem study. Atherosclerosis. 1998;137:205-210.
7. Aikawa M, Rabkin E, Okada Y, et al. Lipid lowering by diet reduces matrix metalloproteinase activity and increases collagen content of rabbit atheroma: A potential mechanism of lesion stabilization. Circulation. 1998;97:2433-2444.
8. Krejcy K, Schwarzacher S, Ferber W, et al. Expression of VCAM-1 in rabbit iliac arteries is associated with vasodilator dysfunction of regenerated endothelium following balloon injury. Atherosclerosis. 1996;122: 59-67.
9. Okabe T, Hoshiga M, Negoro N, et al. Rabbit plaque models closely resembling lesions in human coronary artery disease. Int J Cardiol. 2011; 147:271-277.
10. Riedmuller K, Metz S, Bonaterra GA, et al. Cholesterol diet and effect of long-term withdrawal on plaque development and composition in the thoracic aorta of New Zealand White rabbits. Atherosclerosis. 2010; 210:407-413.
11. Khanna V, Jain M, Singh V, et al. Cholesterol diet withdrawal leads to an initial plaque instability and subsequent regression of accelerated iliac artery atherosclerosis in rabbits. PLoS One. 2013;8:e77037.
12. Burke AP, Kolodgie FD, Farb A, et al. Morphological predictors of arterial remodeling in coronary atherosclerosis. Circulation. 2002;105: 297-303.
13. Tian J, Hu S, Sun Y, et al. A novel model of atherosclerosis in rabbits using injury to arterial walls induced by ferric chloride as evaluated by optical coherence tomography as well as intravascular ultrasound and histology. J Biomed Biotechnol. 2012;2012:121867.
14. Paino A, Tuominen H, Jaaskelainen M, et al. Trimeric form of intracellular ATP synthase subunit beta of Aggregatibacter actinomycetemcomitans binds human interleukin-1beta. PLoS One. 2011;6: e18929.
15. Candipan RC, Hsiun PT, Pratt R, et al. Vascular injury augments adrenergic neurotransmission. Circulation. 1994;89:777-784.
16. Hansson J, Vasan RS, Arnlov J, et al. Biomarkers of extracellular matrix metabolism (MMP-9 and TIMP-1) and risk of stroke, myocardial infarction, and cause-specific mortality: cohort study. PLoS One. 2011;6: e16185.
17. Dapson RW, Fagan C, Kiernan JA, et al. Certification procedures for sirius red F3B (CI 35780, Direct red 80). Biotech Histochem. 2011;86: 133-139.
18. Rekhter MD, Hicks GW, Brammer DW, et al. Animal model that mimics atherosclerotic plaque rupture. Circ Res. 1998;83:705-713.
19. Lepedda AJ, Cigliano A, Cherchi GM, et al. A proteomic approach to differentiate histologically classified stable and unstable plaques from human carotid arteries. Atherosclerosis. 2009;203:112-118.
20. Herrero-Beaumont G, Marcos ME, Sanchez-Pernaute O, et al. Effect of chondroitin sulphate in a rabbit model of atherosclerosis aggravated by chronic arthritis. Br J Pharmacol. 2008;154:843-851.
21. Dong B, Zhang C, Feng JB, et al. Overexpression of ACE2 enhances plaque stability in a rabbit model of atherosclerosis. Arterioscler Thromb Vasc Biol. 2008;28:1270-1276.
22. Jain M, Barthwal MK, Haq W, et al. Synthesis and pharmacological evaluation of novel arginine analogs as potential inhibitors of acetylcholine-induced relaxation in rat thoracic aortic rings. Chem Biol Drug Des. 2012;79:459-469.
23. Khanna V, Jain M, Barthwal MK, et al. Vasomodulatory effect of novel peroxovanadate compounds on rat aorta: role of rho kinase and nitric oxide/cGMP pathway. Pharmacol Res. 2011;64:274-282.
24. Chomczynski P. A reagent for the single-step simultaneous isolation of RNA, DNA and proteins from cell and tissue samples. Biotechniques. 1993;15:532-534. 536-537.
25. Li CJ, Sun HW, Zhu FL, et al. Local adiponectin treatment reduces atherosclerotic plaque size in rabbits. J Endocrinol. 2007;193:137-145.
26. Gough PJ, Gomez IG, Wille PT, et al. Macrophage expression of active MMP-9 induces acute plaque disruption in apoE-deficient mice. J Clin Invest. 2006;116:59-69.
27. Liu P, Sun M, Sader S. Matrix metalloproteinases in cardiovascular disease. Can J Cardiol. 2006;22(suppl B):25B-30B.
28. Watanabe N, Ikeda U. Matrix metalloproteinases and atherosclerosis. Curr Atheroscler Rep. 2004;6:112-120.
29. Loftus IM, Naylor AR, Goodall S, et al. Increased matrix metalloproteinase-9 activity in unstable carotid plaques. A potential role in acute plaque disruption. Stroke. 2000;31:40-47.
30. Nadkarni SK, Bouma BE, de Boer J, et al. Evaluation of collagen in atherosclerotic plaques: The use of two coherent laser-based imaging methods. Lasers Med Sci. 2009;24:439-445.
31. Newby AC, Zaltsman AB. Fibrous cap formation or destruction-the critical importance of vascular smooth muscle cell proliferation, migration and matrix formation. Cardiovasc Res. 1999;41:345-360.
32. Glass CK, Witztum JL. Atherosclerosis. The road ahead. Cell. 2001;23: 503-516.
33. Bobryshev YV. Monocyte recruitment and foam cell formation in atherosclerosis. Micron. 2006;37:208-222.
34. Stary HC, Chandler AB, Glagov S, et al. A definition of initial, fatty streak, and intermediate lesions of atherosclerosis. A report from the committee on vascular lesions of the council on arteriosclerosis, American heart association. Circulation. 1994;89:2462-2478.
35. Steinberg D. Hypercholesterolemia and inflammation in atherogenesis: Two sides of the same coin. Mol Nutr Food Res. 2005;49:995-998.
36. Weidinger FF, McLenachan JM, Cybulsky MI, et al. Hypercholesterolemia enhances macrophage recruitment and dysfunction of regenerated endothelium after balloon injury of the rabbit iliac artery. Circulation. 1991;84:755-767.
37. Hernandez-Presa M, Bustos C, Ortego M, et al. Angiotensin-converting enzyme inhibition prevents arterial nuclear factor-kappa B activation, monocyte chemoattractant protein-1 expression, and macrophage infiltration in a rabbit model of early accelerated atherosclerosis. Circulation. 1997;95:1532-1541.
38. Denger S, Jahn L, Wende P, et al. Expression of monocyte chemoattractant protein-1 cDNA in vascular smooth muscle cells: induction of the synthetic phenotype: A possible clue to SMC differentiation in the process of atherogenesis. Atherosclerosis. 1999;144:15-23.
39. Deaton RA, Su C, Valencia TG, et al. Transforming growth factor-beta1-induced expression of smooth muscle marker genes involves activation of PKN and p38 MAPK. J Biol Chem. 2005;280:31172-31181.
40. Tanaka H, Sukhova G, Schwartz D, et al. Proliferating arterial smooth muscle cells after balloon injury express TNF-alpha but not interleukin-1 or basic fibroblast growth factor. Arterioscler Thromb Vasc Biol. 1996;16:12-18.
41. Feinberg MW, Shimizu K, Lebedeva M, et al. Essential role for Smad3 in regulating MCP-1 expression and vascular inflammation. Circ Res. 2004; 94:601-608.
42. Lin CC, Pan CS, Wang CY, et al. Tumor necrosis factor-alpha induces VCAM-1-mediated inflammation via c-Src-dependent transactivation of EGF receptors in human cardiac fibroblasts. J Biomed Sci. 2015;22:53.
43. Hadi HA, Carr CS, Al Suwaidi J. Endothelial dysfunction: cardiovascular risk factors, therapy, and outcome. Vasc Health Risk Manag. 2005;1:183-198.
44. Ferns GA, Avades TY. The mechanisms of coronary restenosis: insights from experimental models. Int J Exp Pathol. 2000;81:63-88.
45. Park KC, Park EJ, Kim ER, et al. Therapeutic effects of PG201, an ethanol extract from herbs, through cartilage protection on collagenaseinduced arthritis in rabbits. Biochem Biophys Res Commun. 2005;331: 1469-1477.
46. Schwartz SM, deBlois D, O'Brien ER. The intima. Soil for atherosclerosis and restenosis. Circ Res. 1995;77:445-465.
47. Gong Y, Hart E, Shchurin A, et al. Inflammatory macrophage migration requires MMP-9 activation by plasminogen in mice. J Clin Invest. 2008; 118:3012-3024.
48. Zaltsman AB, George SJ, Newby AC. Increased secretion of tissue inhibitors of metalloproteinases 1 and 2 from the aortas of cholesterol fed rabbits partially counterbalances increased metalloproteinase activity. Arterioscler Thromb Vasc Biol. 1999;19:1700-1707.
49. Ross R. Atherosclerosis is an inflammatory disease. Am Heart J. 1999; 138:S419-S420.
50. Bot PT, Grundmann S, Goumans MJ, et al. Forkhead box protein P1 as a downstream target of transforming growth factor-beta induces collagen synthesis and correlates with a more stable plaque phenotype. Atherosclerosis. 2011;218:33-43.
51. Ridker PM, Cannon CP, Morrow D, et al. C-reactive protein levels and outcomes after statin therapy. N Engl J Med. 2005;352:20-28.
52. Daoud AS, Fritz KE, Jarmolych J, et al. Role of macrophages in regression of atherosclerosis. Ann N Y Acad Sci. 1985;454:101-114.
53. Suwanabol PA, Seedial SM, Shi X, et al. Transforming growth factorbeta increases vascular smooth muscle cell proliferation through the Smad3 and extracellular signal-regulated kinase mitogen-activated protein kinases pathways. J Vasc Surg. 2012;56:446-454.
54. Lusis AJ. Atherosclerosis. Nature. 2000;407:233-241.
55. ShiomiM, Ito T, Hirouchi Y, et al. Fibromuscular cap composition is important for the stability of established atherosclerotic plaques in mature WHHL rabbits treated with statins. Atherosclerosis. 2001; 157:75-84.
56. Gomez-Garre D, Munoz-Pacheco P, Gonzalez-Rubio ML, et al. Ezetimibe reduces plaque inflammation in a rabbit model of atherosclerosis and inhibits monocyte migration in addition to its lipid-lowering effect. Br J Pharmacol. 2009;156:1218-1227.
57. Maron DJ, Fazio S, Linton MF. Current perspectives on statins. Circulation. 2000;101:207-213.
58. Libby P, Aikawa M. Stabilization of atherosclerotic plaques: new mechanisms and clinical targets. Nat Med. 2002;8:1257-1262.
59. Koh KK. Effects of statins on vascular wall: vasomotor function, inflammation, and plaque stability. Cardiovasc Res. 2000;47:648-657.
60. Maekawa T, Komori K, Morisaki K, et al. Ezetimibe reduces intimal hyperplasia in rabbit jugular vein graft. J Vasc Surg. 2012;56:1689-1697.
61. Vaughan CJ, Gotto AM Jr, Basson CT. The evolving role of statins in the management of atherosclerosis. J Am Coll Cardiol. 2000;35:1-10.
62. Jimenez AM, Millas I, Farre J, et al. Effect of HMG-CoA reductase inhibition on endothelial dysfunction-inducing protein in hypercholesterolemic rabbits. Rev Esp Cardiol. 2002;55:1151-1158.
63. Davignon J. Beneficial cardiovascular pleiotropic effects of statins. Circulation. 2004;109:III39-III43.
64. Fenning RS, Burgert ME, Hamamdzic D, et al. Atherosclerotic plaque inflammation varies between vascular sites and correlates with response to inhibition of lipoprotein-associated phospholipase A2. J Am Heart Assoc. 2015;4:e001477.
65. Van Craeyveld E, Gordts SC, Jacobs F, et al. Correlation of atherosclerosis between different topographic sites is highly dependent on the type of hyperlipidemia. Heart Vessels. 2012;27:231-234.