Atherosclerosis
Volume 210, Issue 2 , Pages 430-437 , June 2010

AT1 blockade attenuates atherosclerotic plaque destabilization accompanied by the suppression of cathepsin S activity in apoE-deficient mice

  • Takeshi Sasaki

      Affiliations

    • Department of Anatomy and Neuroscience, Hamamatsu University School of Medicine, 1 Handayama, Higashi-ku, Hamamatsu, Shizuoka, Japan
    • Department of Geriatrics, Nagoya University Graduate School of Medicine, 65 Tsuruma-cho, Showa-ku, Nagoya, Japan
    • ,
  • Masafumi Kuzuya

      Affiliations

    • Department of Geriatrics, Nagoya University Graduate School of Medicine, 65 Tsuruma-cho, Showa-ku, Nagoya, Japan
    • Corresponding Author InformationCorresponding author. Tel.: +81 52 744 2364; fax: +81 52 744 2371.
    • ,
  • Kae Nakamura

      Affiliations

    • Department of Geriatrics, Nagoya University Graduate School of Medicine, 65 Tsuruma-cho, Showa-ku, Nagoya, Japan
    • ,
  • Xian Wu Cheng

      Affiliations

    • Department of Cardiology, Nagoya University Graduate School of Medicine, 65 Tsurumai-cho, Showa-ku, Nagoya, Japan
    • ,
  • Taiju Hayashi

      Affiliations

    • Department of Anatomy and Neuroscience, Hamamatsu University School of Medicine, 1 Handayama, Higashi-ku, Hamamatsu, Shizuoka, Japan
    • ,
  • Haizhen Song

      Affiliations

    • Department of Cardiology, Nagoya University Graduate School of Medicine, 65 Tsurumai-cho, Showa-ku, Nagoya, Japan
    • ,
  • Lina Hu

      Affiliations

    • Department of Geriatrics, Nagoya University Graduate School of Medicine, 65 Tsuruma-cho, Showa-ku, Nagoya, Japan
    • ,
  • Kenji Okumura

      Affiliations

    • Department of Cardiology, Nagoya University Graduate School of Medicine, 65 Tsurumai-cho, Showa-ku, Nagoya, Japan
    • ,
  • Toyoaki Murohara

      Affiliations

    • Department of Cardiology, Nagoya University Graduate School of Medicine, 65 Tsurumai-cho, Showa-ku, Nagoya, Japan
    • ,
  • Akihisa Iguchi

      Affiliations

    • Department of Geriatrics, Nagoya University Graduate School of Medicine, 65 Tsuruma-cho, Showa-ku, Nagoya, Japan
    • ,
  • Kohji Sato

      Affiliations

    • Department of Anatomy and Neuroscience, Hamamatsu University School of Medicine, 1 Handayama, Higashi-ku, Hamamatsu, Shizuoka, Japan

Received 25 August 2009 ,Revised 20 December 2009 ,Accepted 21 December 2009.

References 

  1. Katagiri H, Yamada T, Oka Y. Adiposity and cardiovascular disorders: disturbance of the regulatory system consisting of humoral and neuronal signals. Circ Res. 2007;101:27–39
  2. Kuzuya M, Iguchi A. Role of matrix metalloproteinases in vascular remodeling. J Atheroscler Thromb. 2003;10:275–282
  3. Liu J, Sukhova GK, Sun JS, et al. Lysosomal cysteine proteases in atherosclerosis. Arterioscler Thromb Vasc Biol. 2004;24:1359–1366
  4. Garcia-Touchard A, Henry TD, Sangiorgi G, et al. Extracellular proteases in atherosclerosis and restenosis. Arterioscler Thromb Vasc Biol. 2005;25:1119–1127
  5. Lutgens SP, Cleutjens KB, Daemen MJ, Heeneman S. Cathepsin cysteine proteases in cardiovascular disease. FASEB J. 2007;21:3029–3041
  6. Shi GP, Munger JS, Meara JP, Rich DH, Chapman HA. Molecular cloning and expression of human alveolar macrophage cathepsin S, an elastinolytic cysteine protease. J Biol Chem. 1992;267:7258–7262
  7. Maciewicz RA, Etherington DJ. A comparison of four cathepsins (B, L, N and S) with collagenolytic activity from rabbit spleen. Biochem J. 1998;256:433–440
  8. Cheng XW, Obata K, Kuzuya M, et al. Elastolytic cathepsin induction/activation system exists in myocardium and is upregulated in hypertensive heart failure. Hypertension. 2006;48:979–987
  9. Cheng XW, Kuzuya M, Nakamura K, et al. Localization of cysteine protease, cathepsin S, to the surface of vascular smooth muscle cells by association with integrin alphanubeta3. Am J Pathol. 2006;168:685–694
  10. Sukhova GK, Shi G-P, Simon DI, Chapman HA, Libby P. Expression of the elastolytic cathepsins S and K in human atheroma and regulation of their production in smooth muscle cells. J Clin Invest. 1998;102:576–583
  11. Cheng XW, Kuzuya M, Sasaki T, et al. Increased expression of elastolytic cysteine proteases, cathepsins S and K, in the neointima of balloon-injured rat carotid arteries. Am J Pathol. 2004;164:243–251
  12. Sukhova GK, Zhang Y, Pan JH, et al. Deficiency of cathepsin S reduces atherosclerosis in LDL receptor-deficient mice. J Clin Invest. 2003;111:897–906
  13. Rodgers KJ, Watkins DJ, Miller AL, et al. Destabilizing role of cathepsin S in murine atherosclerotic plaques. Arterioscler Thromb Vasc Biol. 2006;26:851–856
  14. Lutgens E, Lutgens SP, Faber BC, et al. Disruption of the cathepsin K gene reduces atherosclerosis progression and induces plaque fibrosis but accelerates macrophage foam cell formation. Circulation. 2006;113:98–107
  15. Vaughan DE. AT1 receptor blockade and atherosclerosis: hopeful insights into vascular protection. Circulation. 2000;101:1496–1497
  16. The Heart Outcomes Prevention Evaluation Study Investigators . Effects of an angiotensin-converting enzyme inhibitor, ramipril, on death from cardiovascular causes, myocardial infarction, and stroke in high-risk patients. N Engl J Med. 2000;342:145–153
  17. The European Trial on Reduction of Cardiac Events with Perindopril in Stable Coronary Artery Disease Investigators . Efficacy of perindopril in reduction of cardiovascular events among patients with stable coronary artery disease: randomised, double-blind, placebo-controlled, multicentre trial (EUROPA). Lancet. 2003;362:782–788
  18. Fliser D, Buchholz K, Haller H. European Trial on Olmesartan and Pravastatin in Inflammation and Atherosclerosis (EUTOPIA) Investigators. 1. Antiinflammatory effects of angiotensin II subtype 1 receptor blockade in hypertensive patients with microinflammation. Circulation. 2004;110:1103–1107
  19. Weiss D, Kools JJ, Taylor WR. Angiotensin II-induced hypertension accelerates the development of atherosclerosis in apoE-deficient mice. Circulation. 2001;103:448–454
  20. Wassmann S, Czech T, van Eickels M, et al. Inhibition of diet-induced atherosclerosis and endothelial dysfunction in apolipoprotein E/angiotensin II type 1A receptor double-knockout mice. Circulation. 2004;110:3062–3067
  21. Browatzki M, Larsen D, Pfeiffer CA, et al. Angiotensin II stimulates matrix metalloproteinase secretion in human vascular smooth muscle cells via nuclear factor-kappaB and activator protein 1 in a redox-sensitive manner. J Vasc Res. 2005;42:415–423
  22. Wang M, Zhang J, Spinetti G, et al. Angiotensin II activates matrix metalloproteinase type II and mimics age-associated carotid arterial remodeling in young rats. Am J Pathol. 2005;167:1429–1442
  23. Guo RW, Yang LX, Wang H, Liu B, Wang L. Angiotensin II induces matrix metalloproteinase-9 expression via a nuclear factor-kappaB-dependent pathway in vascular smooth muscle cells. Regul Pept. 2008;147:37–44
  24. Cipollone F, Fazia M, Iezzi A, et al. Blockade of the angiotensin II type 1 receptor stabilizes atherosclerotic plaques in humans by inhibiting prostaglandin E2-dependent matrix metalloproteinase activity. Circulation. 2004;109:1482–1488
  25. Liang C, Wu ZG, Ding J, et al. Losartan inhibited expression of matrix metalloproteinases in rat atherosclerotic lesions and angiotensin II-stimulated macrophages. Acta Pharmacol Sin. 2004;25:1426–1432
  26. Suganuma E, Babaev VR, Motojima M, et al. Angiotensin inhibition decreases progression of advanced atherosclerosis and stabilizes established atherosclerotic plaques. J Am Soc Nephrol. 2007;18:2311–2319
  27. Fukuda D, Sata M, Ishizaka N, Nagai R. Critical role of bone marrow angiotensin II type 1 receptor in the pathogenesis of atherosclerosis in apolipoprotein E deficient mice. Arterioscler Thromb Vasc Biol. 2008;28:90–96
  28. Tsuda M, Iwai M, Li JM, et al. Inhibitory effects of AT1 receptor blocker, olmesartan, and estrogen on atherosclerosis via anti-oxidative stress. Hypertension. 2005;45:545–551
  29. Liu J, Sukhova GK, Yang JT, et al. Cathepsin L expression and regulation in human abdominal aortic aneurysm, atherosclerosis, and vascular cells. Atherosclerosis. 2006;184:302–311
  30. Galis ZS, Khatri JJ. Matrix metalloproteinases in vascular remodeling and atherogenesis: the good, the bad, and the ugly. Circ Res. 2002;90:251–262
  31. Chen J, Li D, Schaefer RF, Mehta JL. Inhibitory effect of candesartan and rosuvastatin on cd40 and mmps expression in apo-e knockout mice: novel insights into the role of ras and dyslipidemia in atherogenesis. J Cardiovasc Pharmacol. 2004;44:446–452
  32. Luchtefeld M, Grote K, Grothusen C, et al. Angiotensin II induces mmp-2 in a p47phox-dependent manner. Biochem Biophys Res Commun. 2005;328:183–188
  33. Cheng XW, Murohara T, Kuzuya M, et al. Superoxide-dependent cathepsin activation is associated with hypertensive myocardial remodeling and represents a target for angiotensin II type 1 receptor blocker treatment. Am J Pathol. 2008;173:358–369
  34. Rueckschloss U, Quinn MT, Holtz J, Morawietz H. Dose-dependent regulation of NAD(P)H oxidase expression by angiotensin II in human endothelial cells: protective effect of angiotensin II type 1 receptor blockade in patients with coronary artery disease. Arterioscler Thromb Vasc Biol. 2002;22:1845–1851
  35. Kato Y, Mori Y, Makino Y, et al. Formation of N&supɛ;-(hexanonyl)lysine in protein exposed to lipid hydroperoxide. A plausible marker for lipid hydroperoxide-derived protein modification. J Biol Chem. 1999;274:20406–20414
  36. Fukuchi Y, Miura Y, Nabeno Y, et al. Immunohistochemical detection of oxidative stress biomarkers, dityrosine and N(epsilon)-(hexanoyl)lysine, and C-reactive protein in rabbit atherosclerotic lesions. J Atheroscler Thromb. 2008;15:185–192
  37. Samokhin AO, Wong A, Saftig P, Brömme D. Role of cathepsin K in structural changes in brachiocephalic artery during progression of atherosclerosis in apoE-deficient mice. Atherosclerosis. 2008;200:58–68
  38. 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;38:395–405
  39. Tummala PE, Chen XL, Sundell CL, et al. Angiotensin II induces vascular cell adhesion molecule-1 expression in rat vasculature: a potential link between the renin–angiotensin system and atherosclerosis. Circulation. 1999;100:1223–1229
  40. Pueyo ME, Gonzalez W, Nicoletti A, et al. Angiotensin II stimulates endothelial vascular cell adhesion molecule-1 via nuclear factor-kappaB activation induced by intracellular oxidative stress. Arterioscler Thromb Vasc Biol. 2000;20:645–651

PII: S0021-9150(09)01082-X

doi: 10.1016/j.atherosclerosis.2009.12.031

Atherosclerosis
Volume 210, Issue 2 , Pages 430-437 , June 2010

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