Atherosclerosis
Volume 182, Issue 1 , Pages 57-69 , September 2005

Combined effects of HMG-CoA-reductase inhibition and renin–angiotensin system blockade on experimental atherosclerosis

  • Christina Grothusen

      Affiliations

    • Department of Cardiology and Angiology, Medizinische Hochschule Hannover, Carl Neuberg Strasse 1, 30625 Hannover, Germany
    • These authors contributed equally.
    • ,
  • Sylvia Bley

      Affiliations

    • Department of Cardiology and Angiology, Medizinische Hochschule Hannover, Carl Neuberg Strasse 1, 30625 Hannover, Germany
    • These authors contributed equally.
    • ,
  • Tina Selle

      Affiliations

    • Department of Cardiology and Angiology, Medizinische Hochschule Hannover, Carl Neuberg Strasse 1, 30625 Hannover, Germany
    • ,
  • Maren Luchtefeld

      Affiliations

    • Department of Cardiology and Angiology, Medizinische Hochschule Hannover, Carl Neuberg Strasse 1, 30625 Hannover, Germany
    • ,
  • Karsten Grote

      Affiliations

    • Department of Cardiology and Angiology, Medizinische Hochschule Hannover, Carl Neuberg Strasse 1, 30625 Hannover, Germany
    • ,
  • Uwe J.F. Tietge

      Affiliations

    • Department of Medicine and NWFZ, Charite Campus Mitte, Humboldt University Berlin, Germany
    • ,
  • Helmut Drexler

      Affiliations

    • Department of Cardiology and Angiology, Medizinische Hochschule Hannover, Carl Neuberg Strasse 1, 30625 Hannover, Germany
    • ,
  • Bernhard Schieffer

      Affiliations

    • Department of Cardiology and Angiology, Medizinische Hochschule Hannover, Carl Neuberg Strasse 1, 30625 Hannover, Germany
    • Corresponding Author InformationCorresponding author. Tel.: +49 511 532 2129; fax: +49 511 532 5412.

Received 9 July 2004 ,Revised 30 December 2004 ,Accepted 17 January 2005.

References 

  1. Libby P. Molecular bases of the acute coronary syndromes. Circulation. 1995;91(11):2844–2850
  2. Davies MJ, Thomas AC. Plaque fissuring—the cause of acute myocardial infarction, sudden ischaemic death, and crescendo angina. Br Heart J. 1985;53(4):363–373
  3. Wood D. Established and emerging cardiovascular risk factors. Am Heart J. 2001;141(2 Suppl.):S49–S57
  4. Sever PS, Dahlof B, Poulter NR, et al. Prevention of coronary and stroke events with atorvastatin in hypertensive patients who have average or lower-than-average cholesterol concentrations, in the Anglo-Scandinavian cardiac outcomes trial—lipid lowering arm (ASCOT-LLA), a multicentre randomised controlled trial. Lancet. 2003;361(9364):1149–1158
  5. Yusuf S, Sleight P, Pogue J, et al. Effects of an angiotensin-converting-enzyme inhibitor, ramipril, on cardiovascular events in high-risk patients. The heart outcomes prevention evaluation study investigators. N Engl J Med. 2000;342(3):145–153
  6. Fox KM. Efficacy of perindopril in reduction of cardiovascular events among patients with stable coronary artery disease: randomised, double-blind, placebo-controlled, multicentre trial (the EUROPA study). Lancet. 2003;362(9386):782–788
  7. Farmer JA, Gotto AM. The heart protection study: expanding the boundaries for high-risk coronary disease prevention. Am J Cardiol. 2003;92(1A):3i–9i
  8. Yoshida M. Potential role of statins in inflammation and atherosclerosis. J Atheroscler Thromb. 2003;10(3):140–144
  9. O’Keefe JH, Lurk JT, Kahatapitiya RC, Haskin JA. The renin–angiotensin–aldosterone system as a target in coronary disease. Curr Atheroscler Rep. 2003;5(2):124–130
  10. Martin MJ, Hulley SB, Browner WS, Kuller LH, Wentworth D. Serum cholesterol, blood pressure, and mortality: implications from a cohort of 361,662 men. Lancet. 1986;2(8513):933–936
  11. Nazzaro P, Manzari M, Merlo M, et al. Distinct and combined vascular effects of ACE blockade and HMG-CoA-reductase inhibition in hypertensive subjects. Hypertension. 1999;33(2):719–725
  12. Kowala MC, Valentine M, Recce R, et al. Enhanced reduction of atherosclerosis in hamsters treated with pravastatin and captopril: ACE in atheromas provides cellular targets for captopril. J Cardiovasc Pharmacol. 1998;32(1):29–38
  13. Teo KK, Burton JR, Buller CE, et al. Long-term effects of cholesterol lowering and angiotensin-converting enzyme inhibition on coronary atherosclerosis: the simvastatin/enalapril coronary atherosclerosis trial (SCAT). Circulation. 2000;102(15):1748–1754
  14. Zhang SH, Reddick RL, Piedrahita JA, Maeda N. Spontaneous hypercholesterolemia and arterial lesions in mice lacking apolipoprotein E. Science. 1992;258(5081):468–471
  15. Bea F, Blessing E, Bennett B, et al. Simvastatin promotes atherosclerotic plaque stability in apoE-deficient mice independently of lipid lowering. Arterioscler Thromb Vasc Biol. 2002;22(11):1832–1837
  16. Sparrow CP, Burton CA, Hernandez M, et al. Simvastatin has anti-inflammatory and antiatherosclerotic activities independent of plasma cholesterol lowering. Arterioscler Thromb Vasc Biol. 2001;21(1):115–121
  17. Laufs U, Gertz K, Huang P, et al. Atorvastatin upregulates type III nitric oxide synthase in thrombocytes, decreases platelet activation, and protects from cerebral ischemia in normocholesterolemic mice. Stroke. 2000;31(10):2442–2449
  18. Bohm M, Lee M, Kreutz R, et al. Angiotensin II receptor blockade in TGR(mREN2)27: effects of renin–angiotensin-system gene expression and cardiovascular functions. J Hypertens. 1995;13(8):891–899
  19. Keidar S, Attias J, Coleman R, et al. Attenuation of atherosclerosis in apolipoprotein E-deficient mice by ramipril is dissociated from its antihypertensive effect and from potentiation of bradykinin. J Cardiovasc Pharmacol. 2000;35(1):64–72
  20. Lutgens E, Daemen M, Kockx M, et al. Atherosclerosis in APOE*3-Leiden transgenic mice: from proliferative to atheromatous stage. Circulation. 1999;99(2):276–283
  21. Stary HC, Chandler AB, Dinsmore RE, et al. A definition of advanced types of atherosclerotic lesions and a histological classification of atherosclerosis. A report from the Committee on Vascular Lesions of the Council on Arteriosclerosis, American Heart Association. Circulation. 1995;92(5):1355–1374
  22. Tietge UJ, Maugeais C, Cain W, et al. Overexpression of secretory phospholipase A(2) causes rapid catabolism and altered tissue uptake of high density lipoprotein cholesteryl ester and apolipoprotein A-I. J Biol Chem. 2000;275(14):10077–10084
  23. Grote K, Flach I, Luchtefeld M, et al. Mechanical stretch enhances mRNA expression and proenzyme release of matrix metalloproteinase-2 (MMP-2) via NAD(P)H oxidase-derived reactive oxygen species. Circ Res. 2003;92(11):e80–e86
  24. Sukhova GK, Zhang Y, Pan JH, et al. Deficiency of cathepsin S reduces atherosclerosis in LDL receptor-deficient mice. J Clin Invest. 2003;111(6):897–906
  25. Ferrario CM, Richmond RS, Smith R, et al. Renin–angiotensin system as a therapeutic target in managing atherosclerosis. Am J Ther. 2004;11(1):44–53
  26. Rekhter MD, Hicks GW, Brammer DW, et al. Hypercholesterolemia causes mechanical weakening of rabbit atheroma: local collagen loss as a prerequisite of plaque rupture. Circ Res. 2000;86(1):101–108
  27. Delsing DJ, Jukema JW, van de Wiel MA, et al. Differential effects of amlodipine and atorvastatin treatment and their combination on atherosclerosis in ApoE*3-Leiden transgenic mice. J Cardiovasc Pharmacol. 2003;42(1):63–70
  28. Quarfordt SH, Oswald B, Landis B, et al. In vivo cholesterol kinetics in apolipoprotein E-deficient and control mice. J Lipid Res. 1995;36(6):1227–1235
  29. Hayek T, Kaplan M, Raz A, et al. Ramipril administration to atherosclerotic mice reduces oxidized low-density lipoprotein uptake by their macrophages and blocks the progression of atherosclerosis. Atherosclerosis. 2002;161(1):65–74
  30. Schupp M, Janke J, Clasen R, Unger T, Kintscher U. Angiotensin type 1 receptor blockers induce peroxisome proliferator-activated receptor-gamma activity. Circulation. 2004;109(17):2054–2057[Epub April 26, 2004]
  31. Chen Z, Ishibashi S, Perrey S, et al. Troglitazone inhibits atherosclerosis in apolipoprotein E-knockout mice: pleiotropic effects on CD36 expression and HDL. Arterioscler Thromb Vasc Biol. 2001;21(3):372–377
  32. Dol F, Martin G, Staels B, et al. Angiotensin AT1 receptor antagonist irbesartan decreases lesion size, chemokine expression, and macrophage accumulation in apolipoprotein E-deficient mice. J Cardiovasc Pharmacol. 2001;38(3):395–405
  33. Michel MC, Bohner H, Koster J, Schafers R, Heemann U. Safety of telmisartan in patients with arterial hypertension: an open-label observational study. Drug Saf. 2004;27(5):335–344
  34. Derosa G, Cicero AF, Bertone G, et al. Comparison of the effects of telmisartan and nifedipine gastrointestinal therapeutic system on blood pressure control, glucose metabolism, and the lipid profile in patients with type 2 diabetes mellitus and mild hypertension: a 12-month, randomized, double-blind study. Clin Ther. 2004;26(8):1228–1236
  35. Benson SC, Pershadsingh HA, Ho CI, et al. Identification of telmisartan as a unique angiotensin II receptor antagonist with selective PPARgamma-modulating activity. Hypertension. 2004;43(5):993–1002
  36. Li Z, Iwai M, Wu L, et al. Fluvastatin enhances the inhibitory effects of a selective AT1 receptor blocker, valsartan, on atherosclerosis. Hypertension. 2004;44(5):758–763
  37. Bea F, Blessing E, Shelley MI, Shultz JM, Rosenfeld ME. Simvastatin inhibits expression of tissue factor in advanced atherosclerotic lesions of apolipoprotein E deficient mice independently of lipid lowering: potential role of simvastatin-mediated inhibition of Egr-1 expression and activation. Atherosclerosis. 2003;167(2):187–194
  38. 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(6):1532–1541
  39. Han J, Zhou X, Yokoyama T, et al. Pitavastatin downregulates expression of the macrophage type B scavenger receptor, CD36. Circulation. 2004;109(6):790–796
  40. Galis ZS, Khatri JJ. Matrix metalloproteinases in vascular remodeling and atherogenesis: the good, the bad, and the ugly. Circ Res. 2002;90(3):251–262
  41. Nickenig G, Baumer AT, Temur Y, et al. Statin-sensitive dysregulated AT1 receptor function and density in hypercholesterolemic men. Circulation. 1999;100(21):2131–2134
  42. Wassmann S, Laufs U, Baumer AT, et al. Inhibition of geranylgeranylation reduces angiotensin II-mediated free radical production in vascular smooth muscle cells: involvement of angiotensin AT1 receptor expression and Rac1 GTPase. Mol Pharmacol. 2001;59(3):646–654
  43. Oubina MP, de las Heras N, Cediel E, et al. Synergistic effect of angiotensin-converting enzyme (ACE) and 3-hydroxy-3-methylglutaryl-CoA (HMG-CoA) reductase inhibition on inflammatory markers in atherosclerotic rabbits. Clin Sci (Lond). 2003;105(6):655–662
  44. Ferroni P, Basili S, Martini F, et al. Serum metalloproteinase nine levels in patients with coronary artery disease: a novel marker of inflammation. J Investig Med. 2003;51(5):295–300
  45. Yamashita H, Shimada K, Seki E, Mokuno H, Daida H. Concentrations of interleukins, interferon, and C-reactive protein in stable and unstable angina pectoris. Am J Cardiol. 2003;91(2):133–136
  46. Schieffer B, Schieffer E, Hilfiker-Kleiner D, et al. Expression of angiotensin II and interleukin 6 in human coronary atherosclerotic plaques: potential implications for inflammation and plaque instability. Circulation. 2000;101(12):1372–1378
  47. Waehre T, Halvorsen B, Damas JK, et al. Inflammatory imbalance between IL-10 and TNFalpha in unstable angina potential plaque stabilizing effects of IL-10. Eur J Clin Invest. 2002;32(11):803–810
  48. Anguera I, Miranda-Guardiola F, Bosch X, et al. Elevation of serum levels of the anti-inflammatory cytokine interleukin-10 and decreased risk of coronary events in patients with unstable angina. Am Heart J. 2002;144(5):811–817
  49. Mallat Z, Besnard S, Duriez M, et al. Protective role of interleukin-10 in atherosclerosis. Circ Res. 1999;85(8):e17–e24
  50. Schieffer B, Bunte C, Witte J, et al. Comparative effects of AT1-antagonism and angiotensin-converting enzyme inhibition on markers of inflammation and platelet aggregation in patients with coronary artery disease. J Am Coll Cardiol. 2004;44(2):362–368
  51. Rezaie-Majd A, Maca T, Bucek RA, et al. Simvastatin reduces expression of cytokines interleukin-6, interleukin-8, and monocyte chemoattractant protein-1 in circulating monocytes from hypercholesterolemic patients. Arterioscler Thromb Vasc Biol. 2002;22(7):1194–1199
  52. Nawawi H, Osman NS, Annuar R, Khalid BA, Yusoff K. Soluble intercellular adhesion molecule-1 and interleukin-6 levels reflect endothelial dysfunction in patients with primary hypercholesterolaemia treated with atorvastatin. Atherosclerosis. 2003;169(2):283–291
  53. Steinberg D. Atherogenesis in perspective: hypercholesterolemia and inflammation as partners in crime. Nat Med. 2002;8(11):1211–1217
  54. Liao JK. Beyond lipid lowering: the role of statins in vascular protection. Int J Cardiol. 2002;86(1):5–18
  55. Youssef S, Stuve O, Patarroyo JC, et al. The HMG-CoA-reductase inhibitor, atorvastatin, promotes a Th2 bias and reverses paralysis in central nervous system autoimmune disease. Nature. 2002;420(6911):78–84
  56. Diomede L, Albani D, Sottocorno M, et al. In vivo anti-inflammatory effect of statins is mediated by nonsterol mevalonate products. Arterioscler Thromb Vasc Biol. 2001;21(8):1327–1332
  57. Seasholtz TM, Majumdar M, Brown JH. Rho as a mediator of G protein-coupled receptor signaling. Mol Pharmacol. 1999;55(6):949–956
  58. Wassmann S, Laufs U, Muller K, et al. Cellular antioxidant effects of atorvastatin in vitro and in vivo. Arterioscler Thromb Vasc Biol. 2002;22(2):300–305
  59. Hayek T, Attias J, Coleman R, et al. The angiotensin-converting enzyme inhibitor, fosinopril, and the angiotensin II receptor antagonist, losartan, inhibit LDL oxidation and attenuate atherosclerosis independent of lowering blood pressure in apolipoprotein E deficient mice. Cardiovasc Res. 1999;44(3):579–587

PII: S0021-9150(05)00122-X

doi: 10.1016/j.atherosclerosis.2005.01.045

Atherosclerosis
Volume 182, Issue 1 , Pages 57-69 , September 2005

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