Circulation. 2002;106:246-253
Published online before print June 17, 2002, doi: 10.1161/01.CIR.0000021122.63813.32
Published online before print June 17, 2002, doi: 10.1161/01.CIR.0000021122.63813.32
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
(Circulation. 2002;106:246.)
© 2002 American Heart Association, Inc.
Basic Science Reports |
Prevention of Accelerated Atherosclerosis by Angiotensin-Converting Enzyme Inhibition in Diabetic Apolipoprotein E–Deficient Mice
From the Department of Medicine, University of Melbourne, Austin and Repatriation Medical Centre, Heidelberg West, Australia (R.C., K.A.J.-D., Z.C., S.P.N., W.C.B., M.E.C., T.J.A.); the Kolling Institute of Medical Research, University of Sydney, Royal North Shore Hospital, St Leonards, Australia (S.M.T.); and the Morphology Laboratory, Baker Medical Research Institute, Melbourne, Australia (R.J.D.).
Correspondence to Dr Terri J. Allen, Division of Diabetes, Lipoproteins and Metabolism, Baker Heart Research Institute, PO Box 6492, Melbourne 8008 Victoria, Australia. E-mail terri.allen{at}baker.edu.au
Background— Atherosclerosis is a major complication of diabetes, but the mechanisms by which diabetes promotes macrovascular disease have not been fully delineated. Although several animal studies have demonstrated that inhibition of ACE results in a decrease in the development of atherosclerotic lesions, information about the potential benefits of these agents on complex and advanced atherosclerotic lesions as observed in long-term diabetes is lacking. The aim of this study was to evaluate whether treatment with the ACE inhibitor perindopril affects diabetes-induced plaque formation in the apolipoprotein E (apoE)-deficient mouse.
Methods and Results— Diabetes was induced by injection of streptozotocin in 6-week-old apoE-deficient mice. Diabetic animals received treatment with perindopril (4 mg · kg-1 · d-1) or no treatment for 20 weeks. Nondiabetic apoE-deficient mice were used as controls. Induction of diabetes was associated with a 4-fold increase in plaque area compared with nondiabetic animals. This accelerated atherosclerosis was associated with a significant increase in aortic ACE expression and activity and connective tissue growth factor and vascular cell adhesion molecule-1 expression. Perindopril treatment inhibited the development of atherosclerotic lesions and diabetes-induced ACE, connective tissue growth factor, and vascular cell adhesion molecule-1 overexpression in the aorta.
Conclusions— The activation of the local renin-angiotensin system in the diabetic aorta and the reduction in atherosclerosis with ACE inhibitor treatment provides further evidence that the renin-angiotensin system plays a pivotal role in the development and acceleration of atherosclerosis in diabetes.
Key Words: atherosclerosis • diabetes mellitus • angiotensin • vessels
This article has been cited by other articles:
 |
|
 |
|
  J.-C. Tardif Angiotensin-converting enzyme inhibitors and atherosclerotic plaque: a key role in the cardiovascular protection of patients with coronary artery disease Eur. Heart J. Suppl., August 1, 2009; 11(suppl_E): E9 - E16. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 D. Brasacchio, J. Okabe, C. Tikellis, A. Balcerczyk, P. George, E. K. Baker, A. C. Calkin, M. Brownlee, M. E. Cooper, and A. El-Osta Hyperglycemia Induces a Dynamic Cooperativity of Histone Methylase and Demethylase Enzymes Associated With Gene-Activating Epigenetic Marks That Coexist on the Lysine Tail Diabetes, May 1, 2009; 58(5): 1229 - 1236. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C.-H. Ku, K. E. White, A. Dei Cas, A. Hayward, Z. Webster, R. Bilous, S. Marshall, G. Viberti, and L. Gnudi Inducible Overexpression of sFlt-1 in Podocytes Ameliorates Glomerulopathy in Diabetic Mice Diabetes, October 1, 2008; 57(10): 2824 - 2833. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Soro-Paavonen, A. M.D. Watson, J. Li, K. Paavonen, A. Koitka, A. C. Calkin, D. Barit, M. T. Coughlan, B. G. Drew, G. I. Lancaster, et al. Receptor for Advanced Glycation End Products (RAGE) Deficiency Attenuates the Development of Atherosclerosis in Diabetes Diabetes, September 1, 2008; 57(9): 2461 - 2469. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 F. Huang, J. C. Thompson, P. G. Wilson, H. H. Aung, J. C. Rutledge, and L. R. Tannock Angiotensin II increases vascular proteoglycan content preceding and contributing to atherosclerosis development J. Lipid Res., March 1, 2008; 49(3): 521 - 530. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. Zadelaar, R. Kleemann, L. Verschuren, J. de Vries-Van der Weij, J. van der Hoorn, H. M. Princen, and T. Kooistra Mouse Models for Atherosclerosis and Pharmaceutical Modifiers Arterioscler Thromb Vasc Biol, August 1, 2007; 27(8): 1706 - 1721. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 E. Suganuma, V. R. Babaev, M. Motojima, Y. Zuo, N. Ayabe, A. B. Fogo, I. Ichikawa, M. F. Linton, S. Fazio, and V. Kon Angiotensin Inhibition Decreases Progression of Advanced Atherosclerosis and Stabilizes Established Atherosclerotic Plaques J. Am. Soc. Nephrol., August 1, 2007; 18(8): 2311 - 2319. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 V. Farah, K. M. Elased, and M. Morris Genetic and dietary interactions: role of angiotensin AT1a receptors in response to a high-fructose diet Am J Physiol Heart Circ Physiol, August 1, 2007; 293(2): H1083 - H1089. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 P. Lewis, N. Stefanovic, J. Pete, A. C. Calkin, S. Giunti, V. Thallas-Bonke, K. A. Jandeleit-Dahm, T. J. Allen, I. Kola, M. E. Cooper, et al. Lack of the Antioxidant Enzyme Glutathione Peroxidase-1 Accelerates Atherosclerosis in Diabetic Apolipoprotein E-Deficient Mice Circulation, April 24, 2007; 115(16): 2178 - 2187. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J.-H. Oak and H. Cai Attenuation of Angiotensin II Signaling Recouples eNOS and Inhibits Nonendothelial NOX Activity in Diabetic Mice Diabetes, January 1, 2007; 56(1): 118 - 126. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. G. Huebschmann, J. G. Regensteiner, H. Vlassara, and J. E.B. Reusch Diabetes and Advanced Glycoxidation End Products. Diabetes Care, June 1, 2006; 29(6): 1420 - 1432. [Full Text] [PDF]
|
|
|
|
 |
|
 T. S. Hermann, W. Li, H. Dominguez, N. Ihlemann, C. Rask-Madsen, A. Major-Pedersen, D. B. Nielsen, K. W. Hansen, M. Hawkins, L. Kober, et al. Quinapril Treatment Increases Insulin-Stimulated Endothelial Function and Adiponectin Gene Expression in Patients with Type 2 Diabetes J. Clin. Endocrinol. Metab., March 1, 2006; 91(3): 1001 - 1008. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. Zulli, L. M. Burrell, R. E. Widdop, M. J. Black, B. F. Buxton, and D. L. Hare Immunolocalization of ACE2 and AT2 Receptors in Rabbit Atherosclerotic Plaques J. Histochem. Cytochem., February 1, 2006; 54(2): 147 - 150. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Zuccollo, C. Shi, R. Mastroianni, K. A. Maitland-Toolan, R. M. Weisbrod, M. Zang, S. Xu, B. Jiang, J. M. Oliver-Krasinski, A. J. Cayatte, et al. The Thromboxane A2 Receptor Antagonist S18886 Prevents Enhanced Atherogenesis Caused by Diabetes Mellitus Circulation, November 8, 2005; 112(19): 3001 - 3008. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 D M Shavelle Are angiotensin converting enzyme inhibitors beneficial in patients with aortic stenosis? Heart, October 1, 2005; 91(10): 1257 - 1259. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. C. Thomas, C. Tikellis, W. M. Burns, K. Bialkowski, Z. Cao, M. T. Coughlan, K. Jandeleit-Dahm, M. E. Cooper, and J. M. Forbes Interactions between Renin Angiotensin System and Advanced Glycation in the Kidney J. Am. Soc. Nephrol., October 1, 2005; 16(10): 2976 - 2984. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. C. Calkin, J. M. Forbes, C. M. Smith, M. Lassila, M. E. Cooper, K. A. Jandeleit-Dahm, and T. J. Allen Rosiglitazone Attenuates Atherosclerosis in a Model of Insulin Insufficiency Independent of Its Metabolic Effects Arterioscler Thromb Vasc Biol, September 1, 2005; 25(9): 1903 - 1909. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 C. A. Daly, K. M. Fox, W. J. Remme, M. E. Bertrand, R. Ferrari, M. L. Simoons, and on behalf of the EUROPA investigators The effect of perindopril on cardiovascular morbidity and mortality in patients with diabetes in the EUROPA study: results from the PERSUADE substudy Eur. Heart J., July 2, 2005; 26(14): 1369 - 1378. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 E. Shinoda, Y. Yui, K. Kodama, A. Hirayama, H. Nonogi, K. Haze, T. Sumiyoshi, S. Hosoda, C. Kawai, and for the Japan Multicenter Investigation for Cardio Quantitative Coronary Angiogram Analysis: Nifedipine Retard Versus Angiotensin-Converting Enzyme Inhibitors (JMIC-B Side Arm Study) Hypertension, June 1, 2005; 45(6): 1153 - 1158. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 D. K. Richardson, S. Kashyap, M. Bajaj, K. Cusi, S. J. Mandarino, J. Finlayson, R. A. DeFronzo, C. P. Jenkinson, and L. J. Mandarino Lipid Infusion Decreases the Expression of Nuclear Encoded Mitochondrial Genes and Increases the Expression of Extracellular Matrix Genes in Human Skeletal Muscle J. Biol. Chem., March 18, 2005; 280(11): 10290 - 10297. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Lassila, K. Jandeleit-Dahm, K. K. Seah, C. M. Smith, A. C. Calkin, T. J. Allen, and M. E. Cooper Imatinib Attenuates Diabetic Nephropathy in Apolipoprotein E-Knockout Mice J. Am. Soc. Nephrol., February 1, 2005; 16(2): 363 - 373. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. V. McLennan, X. Y. Wang, V. Moreno, D. K. Yue, and S. M. Twigg Connective Tissue Growth Factor Mediates High Glucose Effects on Matrix Degradation through Tissue Inhibitor of Matrix Metalloproteinase Type 1: Implications for Diabetic Nephropathy Endocrinology, December 1, 2004; 145(12): 5646 - 5655. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. Lu, M. Raptis, E. Black, M. Stan, S. Amar, and D. T. Graves Influence of Diabetes on the Exacerbation of an Inflammatory Response in Cardiovascular Tissue Endocrinology, November 1, 2004; 145(11): 4934 - 4939. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Nobuhiko, E. Suganuma, V. R. Babaev, A. Fogo, L. L. Swift, M. F. Linton, S. Fazio, I. Ichikawa, and V. Kon Angiotensin II Amplifies Macrophage-Driven Atherosclerosis Arterioscler Thromb Vasc Biol, November 1, 2004; 24(11): 2143 - 2148. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Lassila, K. K. Seah, T. J. Allen, V. Thallas, M. C. Thomas, R. Candido, W. C. Burns, J. M. Forbes, A. C. Calkin, M. E. Cooper, et al. Accelerated Nephropathy in Diabetic Apolipoprotein E-Knockout Mouse: Role of Advanced Glycation End Products J. Am. Soc. Nephrol., August 1, 2004; 15(8): 2125 - 2138. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Y. Naka, L. G. Bucciarelli, T. Wendt, L. K. Lee, L. L. Rong, R. Ramasamy, S. F. Yan, and A. M. Schmidt RAGE Axis: Animal Models and Novel Insights Into the Vascular Complications of Diabetes Arterioscler Thromb Vasc Biol, August 1, 2004; 24(8): 1342 - 1349. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
B. V. Khan, S. Sola, W. B. Lauten, R. Natarajan, W. C. Hooper, R. G. Menon, S. Lerakis, and T. Helmy Quinapril, an ACE Inhibitor, Reduces Markers of Oxidative Stress in the Metabolic Syndrome Diabetes Care, July 1, 2004; 27(7): 1712 - 1715. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. M. Forbes, L. T. L. Yee, V. Thallas, M. Lassila, R. Candido, K. A. Jandeleit-Dahm, M. C. Thomas, W. C. Burns, E. K. Deemer, S. R. Thorpe, et al. Advanced Glycation End Product Interventions Reduce Diabetes-Accelerated Atherosclerosis Diabetes, July 1, 2004; 53(7): 1813 - 1823. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
B. Jiang, S. Xu, X. Hou, D. R. Pimentel, and R. A. Cohen Angiotensin II Differentially Regulates Interleukin-1-{beta}-inducible NO Synthase (iNOS) and Vascular Cell Adhesion Molecule-1 (VCAM-1) Expression: ROLE OF p38 MAPK J. Biol. Chem., May 7, 2004; 279(19): 20363 - 20368. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T. Kadowaki and N. Kubota Protective Role of Imatinib in Atherosclerosis Arterioscler Thromb Vasc Biol, May 1, 2004; 24(5): 801 - 803. [Full Text]
|
|
|
|
|
|
M. Lassila, T. J. Allen, Z. Cao, V. Thallas, K. A. Jandeleit-Dahm, R. Candido, and M. E. Cooper Imatinib Attenuates Diabetes-Associated Atherosclerosis Arterioscler Thromb Vasc Biol, May 1, 2004; 24(5): 935 - 942. [Abstract] [Full Text]
|
|
|
|
|
|
R. Candido, T. J. Allen, M. Lassila, Z. Cao, V. Thallas, M. E. Cooper, and K. A. Jandeleit-Dahm Irbesartan but Not Amlodipine Suppresses Diabetes-Associated Atherosclerosis Circulation, March 30, 2004; 109(12): 1536 - 1542. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Ling, A. Dai, R. J. Dilley, M. Jones, E. Simpson, P. A. Komesaroff, and K. Sudhir Endogenous Estrogen Deficiency Reduces Proliferation and Enhances Apoptosis-Related Death in Vascular Smooth Muscle Cells: Insights From the Aromatase-Knockout Mouse Circulation, February 3, 2004; 109(4): 537 - 543. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. Tikellis, M. E. Cooper, Stephen. M. Twigg, W. C. Burns, and M. Tolcos Connective Tissue Growth Factor Is Up-Regulated in the Diabetic Retina: Amelioration by Angiotensin-Converting Enzyme Inhibition Endocrinology, February 1, 2004; 145(2): 860 - 866. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. Saraff, F. Babamusta, L. A. Cassis, and A. Daugherty Aortic Dissection Precedes Formation of Aneurysms and Atherosclerosis in Angiotensin II-Infused, Apolipoprotein E-Deficient Mice Arterioscler Thromb Vasc Biol, September 1, 2003; 23(9): 1621 - 1626. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 P. Finckenberg, K. Inkinen, J. Ahonen, S. Merasto, M. Louhelainen, H. Vapaatalo, D. Muller, D. Ganten, F. Luft, and E. Mervaala Angiotensin II Induces Connective Tissue Growth Factor Gene Expression via Calcineurin-Dependent Pathways Am. J. Pathol., July 1, 2003; 163(1): 355 - 366. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. Fox Poststroke patients: implications for the cardiologist Eur. Heart J. Suppl., July 1, 2003; 5(suppl_E): E4 - E10. [Abstract] [PDF]
|
|
|
|
|
|
R. Ferrari, G. Guardigli, D. Mele, M. Valgimigli, and C. Ceconi Myocardial ischaemia: new evidence for angiotensin-converting enzyme inhibition Eur. Heart J. Suppl., July 1, 2003; 5(suppl_E): E11 - E17. [Abstract] [PDF]
|
|
|
|
 |
|
 D. S. Jacoby and D. J. Rader Renin-Angiotensin System and Atherothrombotic Disease: From Genes to Treatment Arch Intern Med, May 26, 2003; 163(10): 1155 - 1164. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 R. Candido, J. M. Forbes, M. C. Thomas, V. Thallas, R. G. Dean, W. C. Burns, C. Tikellis, R. H. Ritchie, S. M. Twigg, M. E. Cooper, et al. A Breaker of Advanced Glycation End Products Attenuates Diabetes-Induced Myocardial Structural Changes Circ. Res., April 18, 2003; 92(7): 785 - 792. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. Tikellis, C. I. Johnston, J. M. Forbes, W. C. Burns, L. M. Burrell, J. Risvanis, and M. E. Cooper Characterization of Renal Angiotensin-Converting Enzyme 2 in Diabetic Nephropathy Hypertension, March 1, 2003; 41(3): 392 - 397. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Buzello, J. Tornig, J. Faulhaber, H. Ehmke, E. Ritz, and K. Amann The Apolipoprotein E Knockout Mouse: A Model Documenting Accelerated Atherogenesis In Uremia J. Am. Soc. Nephrol., February 1, 2003; 14(2): 311 - 316. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. De Caterina and C. Manes Inflammation in early atherogenesis: impact of ACE inhibition Eur. Heart J. Suppl., January 1, 2003; 5(suppl_A): A15 - A24. [Abstract] [PDF]
|
|
|
|
|
|
F. Ribichini, V. Ferrero, W. Wijns, G. Matullo, A. Piazza, E. Uslenghi, J. L. Zhuo, F. A.O. Mendelsohn, and M. Ohishi Can ACE Inhibitors Promote Detrimental Vascular Effects After Percutaneous Injury? * Response Hypertension, October 1, 2002; e6(4): . [Full Text] [PDF]
|
|