Probucol attenuates inflammation and increases stability of vulnerable atherosclerotic plaques in rabbits

Tohoku Journal of Experimental Medicine

Volumn 225, Issue 1, 2011, Pages 23-34

  Li, Tingting ^a   Chen, Wenqiang ^a   An, Fengshuang ^a   Tian, Hongbo ^b   Zhang, Jianning ^c   Peng, Jie ^a   Zhang, Yun ^a   Guo, Yuan ^a  

^a BEIJING HOSPITAL   (China)

^b SHANDONG PROVINCIAL HOSPITAL AFFILIATED TO SHANDONG UNIVERSITY   (China)

^c SHANDONG UNIVERSITY   (China)

Author keywords

Atherosclerosis; Inflammation; Probucol; Ultrasonography; Vulnerable plaque

Indexed keywords

ADENOVIRUS VECTOR; C REACTIVE PROTEIN; CD36 ANTIGEN; CYTOKINE; GELATINASE B; HISTAMINE; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 18; INTERLEUKIN 6; MATRIX METALLOPROTEINASE; MONOCYTE CHEMOTACTIC PROTEIN 1; OXIDIZED LOW DENSITY LIPOPROTEIN RECEPTOR 1; PROBUCOL; PROTEIN P53; RECOMBINANT PROTEIN; SCAVENGER RECEPTOR A; SIMVASTATIN; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TRIACYLGLYCEROL; TUMOR NECROSIS FACTOR ALPHA; VIPER VENOM;

ABDOMINAL AORTA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; AORTA INJURY; ARTICLE; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; ATHEROSCLEROTIC PLAQUE STABILITY; CHOLESTEROL DIET; CONTROLLED STUDY; DIET SUPPLEMENTATION; DRUG TARGETING; EXPERIMENTAL RABBIT; LIPOLYSIS; MALE; NONHUMAN; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION;

ANIMALS; AORTA, ABDOMINAL; BIOLOGICAL MARKERS; CHEMOKINE CCL2; ENZYME-LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION REGULATION; IMMUNOHISTOCHEMISTRY; INFLAMMATION; INFLAMMATION MEDIATORS; INTERCELLULAR ADHESION MOLECULE-1; LIPIDS; PLAQUE, ATHEROSCLEROTIC; PROBUCOL; RABBITS; RECEPTORS, SCAVENGER; RNA, MESSENGER; TOLL-LIKE RECEPTOR 2; TOLL-LIKE RECEPTOR 4;

EID: 80052140269     PISSN: 00408727     EISSN: 13493329     Source Type: Journal    
DOI: 10.1620/tjem.225.23     Document Type: Article

References (47)

1. Alsheikh-Ali, A.A., Maddukuri, P.V., Han, H. & Karas, R.H. (2007) Effect of the magnitude of lipid lowering on risk of elevated liver enzymes, rhabdomyolysis, and cancer: insights from large randomized statin trials. J. Am. Coll. Cardiol., 50, 409-418.
2. Aoki, M., Nata, T., Morishita, R., Matsushita, H., Nakagami, H., Yamamoto, K., Yamazaki, K., Nakabayashi, M., Ogihara, T. & Kaneda, Y. (2001) Endothelial apoptosis Induced by oxidative stress through activation of NF-kB antiapoptotic effect of antioxidant agents on endothelial cells. Hypertension, 38, 48-55.
3. Ball, R.Y., Stowers, E.C., Burton, J.H., Cary, N.R., Skepper, J.N. & Mitchinson, M.J. (1995) Evidence that the death of macrophage foam cells contributes to the lipid core of atheroma. Atherosclerosis, 114, 45-54.
4. Barnhart, J.W., Sefranka, J.A. & McIntosh, D.D. (1970) Hypocholesterolemic effect of 4, 4′-(isopropylidenedithio)-bis (2,6-di-tbutylphenol) (probucol). Am. J. Clin. Nutr., 23, 1229-1233.
5. Bräsen, J.H., Koenig, K., Bach, H., Kontush, A., Heinle, H., Witting, P.K., Ylä-Herttuala, S., Stocker, R. & Beisiegel, U. (2002) Comparison of the effects of alpha-tocopherol, ubiquinone- 10 and probucol at therapeutic doses on atherosclerosis in WHHL rabbits. Atherosclerosis, 163, 249-259.
6. Braun, A., Zhang, S., Miettinen, H.E., Ebrahim, S., Holm, T.M., Vasile, E., Post, M.J., Yoerger, D.M., Picard, M.H., Krieger, J.L., Andrews, N.C., Simons, M. & Krieger, M. (2003) Probucol prevents early coronary heart disease and death in the high-density lipoprotein receptor SR-BI/apolipoprotein E double knockout mouse. Proc. Natl. Acad. Sci. USA., 100, 7283-7288.
7. Carew, T.E., Schwenke, D.C. & Steinberg, D. (1987) Antiatherogenic effect of probucol unrelated to its hypocholesterolemic effect: evidence that antioxidants in vivo can selectively inhibit low density lipoprotein degradation in macrophagerich fatty streaks and slow the progression of atherosclerosis in the Watanabe heritable hyperlipidemic rabbit. Proc. Natl. Acad. Sci. USA., 84, 7725-7729.
8. Chan, P.S., Nallamothu, B.K., Gurm, H.S., Hayward, R.A. & Vijan, S. (2007) Incremental benefit and cost-effectiveness of high-dose statin therapy in highrisk patients with coronary artery disease. Circulation, 115, 2398-2409.
9. Chang, M.Y., Sasahara, M., Chait, A., Raines, E.W. & Ross, R. (1995) Inhibition of hypercholesterolemia-induced atherosclerosis in the nonhuman primate by probucol: II. Cellular composition and proliferation. Arterioscler. Thromb. Vasc. Biol., 15, 1631-1640.
10. Chen, W.Q., Zhang, L., Liu, Y.F., Chen, L., Ji, X.P., Zhang, M., Zhao, Y.X., Yao, G.H., Zhang, C., Wang, X.L. & Zhang, Y. (2007) Prediction of atherosclerotic plaque ruptures with high frequency ultrasound imaging and serum infl{ligature}ammatory markers. Am. J. Physiol. Heart. Circ. Physiol., 293, H2836-H2844.
11. Chen, W.Q., Zhang, Y., Zhang, M., Ji, X.P., Yin, Y. & Zhu, Y.F. (2004) Establishing an animal model of unstable atherosclerotic plaques. Chin. Med. J. (Engl), 117, 1293-1298.
12. Faure, E., Equils, O., Sieling, P.A., Thomas, L., Zhang, F.X., Kirschning, C.J., Polentarutti, N., Muzio, M. & Arditi, M. (2000) Bacterial lipopolysaccharide activates NF κB through toll like receptor 4 in cultured human dermal endothelial cells: differential expression of TLR-4 and TLR-2 in endothelial cells. J. Biol. Chem., 275, 11058-11063.
13. Grundy, S.M., Cleeman, J.I., Merz, C.N., Brewer, H.B. Jr., Clark, L.T., Hunninghake, D.B., Pasternak, R.C., Smith, S.C. Jr. & Stone, N.J. (2004) Implications of recent clinical trials for the National Cholesterol Education Program Adult Treatment Panel III guidelines. Circulation, 110, 227-239.
14. Hansson, G.K., Libby, P., Schonbeck, U. & Yan, Z.Q. (2002) Innate and adaptive immunity in the pathogenesis of atherosclerosis. Circ. Res., 91, 281-291.
15. Hernández-Presa, M.A., Ortego, M., Tuñón, J., Martín-Ventura, J.L., Mas, S., Blanco-Colio, L.M., Aparicio, C., Ortega, L., Gómez-Gerique, J., Vivanco, F. & Egido, J. (2003) Simvastatin reduces NF-kappaB activity in peripheral mononuclear and in plaque cells of rabbit atheroma more markedly than lipid lowering diet. Cardiovascular. Research., 57, 168-177.
16. Johnstone, M.T., Botnar, R.M., Perez, A.S., Stewart, R., Quist, W.C., Hamilton, J.A. & Manning, W.J. (2001) In vivo magnetic resonance imaging of experimental thrombosis in a rabbit model. Arterioscler. Thromb. Vasc. Biol., 21, 1556-1560.
17. Kita, T., Nagano, Y., Yokode, M., Ishii, K., Kume, N., Ooshima, A., Yoshida, H. & Kawai, C. (1987) Probucol prevents the progression of atherosclerosis in Watanabe heritable hyperlipidemic rabbit, an animal model for familial hypercholesterolemia. Proc. Natl. Acad. Sci. USA., 84, 5928-5931.
18. Ku, G., Doherty, N.S., Schmidt, L.F., Jackson, R.L. & Dinerstein, R.J. (1990) Ex vivo lipopolysaccharide-induced interleukin-1 secretion from murine peritoneal macrophages inhibited by probucol, a hypocholesterolemic agent with antioxidant properties. FASEB J., 4, 1645-1653.
19. Lau, A.K., Leichtweis, S.B., Hume, P., Mashima, R., Hou, J.Y., Chaufour, X., Wilkinson, B., Hunt, N.H., Celermajer, D.S. & Stocker, R. (2003) Probucol promotes functional reendothelialization in balloon injured rabbit aortas. Circulation, 107, 2031-2036.
20. Libby, P. (2002) Inflammation in atherosclerosis. Nature, 420, 868-874.
21. Liu, X., Ukai, T., Yumoto, H., Davey, M., Goswami, S., Gibson, F.C. & Genco, C.A. (2008) Toll-like receptor 2 plays a critical role in the progression of atherosclerosis that is independent of dietary lipids. Atherosclerosis, 196, 146-154.
22. Methe, H., Kim, J.O., Kofler, S., Nabauer, M. & Weis, M. (2005) Statins decrease Toll-like receptor 4 expression and downstream signaling in human CD14+ monocytes. Arterioscler. Thromb. Vasc. Biol., 25, 1439-1445.
23. Michelsen, K.S., Wong, M.H., Shah, P.K., Zhang, W., Yano, J., Doherty, T.M., Akira, S., Rajavashisth, T.B. & Arditi, M. (2004) Lack of toll-like receptor 4 or myeloid differentiation factor 88 reduces atherosclerosis and alters plaque phenotype in mice deficient in apolipoprotein E. Proc. Natl. Acad. Sci. USA, 101, 10679-10684.
24. Miida, T., Seino, U., Miyazaki, O., Hanyu, O., Hirayama, S., Saito, T., Ishikawa, Y., Akamatsu, S., Nakano, T., Nakajima, K., Okazaki, M. & Okada, M. (2008) Probucol markedly reduces HDL phospholipids and elevated prebeta1-HDL without delayed conversion into alpha-migrating HDL: putative role of angiopoietin-like protein 3 in probucol-induced HDL remodeling. Atherosclerosis, 200, 329-335.
25. Mintz, G.S., Nissen, S.E., Anderson, W.D., Bailey, S.R., Erbel, R., Fitzgerald, P.J., Pinto, F.J., Rosenfield, K., Siegel, R.J., Tuzcu, E.M. & Yock, P.G. (2001) American College of Cardiology clinical expert consensus document on standards for acquisition, measurement and reporting of intravascular ultrasound studies (IVUS): a report of the American College of Cardiology task force on clinical expert consensus documents. J. Am. Coll. Cardiol., 37, 1478-1492.
26. Muzio, M., Natoli, G., Saccani, S., Levrero, M. & Mantovani, A. (1998) The human toll signaling pathway: divergence of nuclear factor kB and JNK/SAPK activation upstream of tumor necrosis factor receptor-associated factor 6 (TRAF6). J. Exp. Med., 187, 2097-2101.
27. Nishio, Y., Kashiwagi, A., Taki, H., Shinozaki, K., Maeno, Y., Kojima, H., Maegawa, H., Haneda, M., Hidaka, H., Yasuda, H., Horiike, K. & Kikkawa, R. (1998) Altered activities of transcription factors and their related gene expression in cardiac tissues of diabetic rats. Diabetes, 47, 1318-1325.
28. Parthasarathy, S., Young, S.G., Witztum, J.L., Pittman, R.C. & Steinberg, D. (1986) Probucol inhibits oxidative modifi{ligature}cation of low density lipoprotein. J. Clin. Invest., 77, 641-644.
29. Ridker, P.M., Cannon, C.P., Morrow, D., Rifai, N., Rose, L.M., McCabe, C.H., Pfeffer, M.A. & Braunwald, E. Pravastatin or Atorvastatin Evaluation and Infection Therapy-Thrombolysis in Myocardial Infarction 22 (PROVE IT-TIMI 22) Investigators. (2005) C-reactive protein levels and outcomes after statin therapy. N. Engl. J. Med., 352, 20-28.
30. Sasahara, M., Raines, E.W., Chait, A., Carew, T.E., Steinberg, D., Wahl, P.W. & Ross, R. (1994) Inhibition of hypercholesterolemia induced atherosclerosis in Macaca Nemestrina by probucol: I. Intimal lesion area correlates inversely with resistance of lipoproteins to oxidation. J. Clin. Invest., 94, 155-164.
31. Schneider, J.E., Berk, B.C., Gravanis, M.B., Santoian, E.C., Cipolla, G.D., Tarazona, N., Lassegue, B. & King, S.B. 3rd. (1993) Probucol decreases neointimal formation in a swine model of coronary artery balloon injury: a possible role for antioxidants in restenosis. Circulation, 88, 628-637.
32. Sekiya, M., Funada, J., Watanabe, K., Miyagawa, M. & Akutsu, H. (1998) Effects of probucol and cilostazol alone and in combination on frequency of poststenting restenosis. Am. J. Cardiol., 82, 144-147.
33. Shinohara, M., Hirata, K., Yamashita, T., Takaya, T., Sasaki, N., Shiraki, R., Ueyama, T., Emoto, N., Inoue, N., Yokoyama, M. & Kawashima, S. (2007) Local overexpression of toll-like receptors at the vessel wall induces atherosclerotic lesion formation: synergism of TLR2 and TLR4. Arterioscler. Thromb. Vasc. Biol., 27, 2384-2391.
34. Shiomi, M., Ito, T., Hirouchi, Y. & Enomoto, M. (2001) Stability of atheromatous plaque affected by lesional composition: study of WHHL rabbits treated with statins. Ann. N. Y. Acad. Sci., 947, 419-423.
35. Tardif, J.C., Cöté, G., Lespérance, J., Bourassa, M., Lambert, J., Doucet, S., Bilodeau, L., Nattel, S. & de Guise, P. (1997) Probucol and multivitamins in the prevention of restenosis after coronary angioplasty. N. Engl. J. Med., 337, 365-372.
36. Tardif, J.C., Grégoire, J., Schwartz, L., Title, L., Laramée, L., Reeves, F., Lespérance, J., Bourassa, M.G., L'Allier, P.L., Glass, M., Lambert, J. & Guertin, M.C. (2003) Canadian Antioxidant Restenosis Trial (CART-1) Investigators. Effects of AGI-1067 and probucol after percutaneous coronary interventions. Circulation, 107, 552-558.
37. Virmani, R., Kolodgie, F.D., Burke, A.P., Farb, A. & Schwartz, S.M. (2000) Lessons from sudden coronary death: a comprehensive morphological classification scheme for atherosclerotic lesions. Arterioscler. Thromb. Vasc. Biol., 20, 1262- 1275.
38. Wiviott, S.D., de Lemos, J.A., Cannon, C.P., Blazing, M., Murphy, S.A., McCabe, C.H., Califf, R. & Braunwald, E. (2006) A tale of two trials: a comparison of the post-acute coronary syndromelipid-lowering trials A to Z and PROVE IT-TIMI 22. Circulation, 113, 1406-1414.
39. Wu, B.J., Di Girolamo, N., Beck, K., Hanratty, C.G., Choy, K., Hou, J.Y., Ward, M.R. & Stocker, R. (2007) Probucol [4,4'-[(1-methylethylidene)bis(thio)]bis-[2,6-bis(1,1- dimethylethyl) phenol]] inhibits compensatory remodeling and promotes lumen loss associated with atherosclerosis in apolipoprotein E-deficient mice. J. Pharmacol. Exp. Ther., 321, 477-484.
40. Wu, B.J., Kathir, K., Witting, P.K., Beck, K., Choy, K., Li, C., Croft, K.D., Mori, T.A., Tanous, D., Adams, M.R., Lau, A.K. & Stocker, R. (2006) Antioxidants protect from atherosclerosis by a heme oxygenase-1 pathway that is independent of free radical scavenging. J. Exp. Med., 203, 1117-1127.
41. Yamamoto, A., Hara, H., Takaichi, S., Wakasugi, J. & Tomikawa, M. (1988) Effect of probucol on macrophages, leading to regression of xanthomas and atheromatous vascular lesions. Am. J. Cardiol., 62, 31B-36B.
42. Yamamoto, A., Matsuzawa, Y., Kishino, B.I., Hayashi, R., Hirobe, K. & Kikkawa, T. (1983) Effects of probucol on homozygous cases of familial hypercholesterolemia. Atherosclerosis, 48, 157-166.
43. Yamamoto, A., Takaichi, S., Hara, H., Nishikawa, O., Yokoyama, S., Yamamura, T. & Yamaguchi, T. (1986) Probucol prevents lipid storage in macrophages. Atherosclerosis, 62, 209-217.
44. Yamashita, S., Hbujo, H., Arai, H., Harada-Shiba, M., Matsui, S., Fukushima, M., Saito, Y., Kita, T. & Matsuzawa, Y. (2008) Long-term probucol treatment prevents secondary cardiovascular events: a cohort study of patients with heterozygous familial hypercholesterolemia in Japan. J. Atheroscler. Thromb., 15, 292-303.
45. Yamashita, S. & Matsuzawa, Y. (2009) Where are we with probucol: a new life for an old drug? Atherosclerosis, 207, 16-23.
46. Zhang, L., Liu, Y., Lu, X.T., Xu, X.S., Zhao, Y.X., Ji, X.P., Zhang, P.F., Liu, C.X., Tang, M.X., Chen, W.Q. & Zhang, Y. (2008) Intraplaque injection of Ad5-CMV.p53 aggravates local inflammation and leads to plaque instability in rabbits. J. Cell. Mol. Med., 12, 1-11.
47. Zhong, L., Chen, W.Q., Ji, X.P., Zhang, M., Zhao, Y.X., Yao, G.H., Zhang, P.F., Zhang, C. & Zhang, Y. (2008) Dominant-negative mutation of monocyte chemoattractant protein-1 prevents vulnerable plaques from rupture in rabbits independent of serum lipid levels. J. Cell. Mol. Med., 6A, 2362-2371.