Effects of rosuvastatin on cardiovascular morphology and function in an ApoE-knockout mouse model of atherosclerosis

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 295, Issue 5, 2008, Pages

  Gronros J ^a   Wikstrom J ^c   Brandt Eliasson, U ^c   Forsberg, G B ^c   Behrendt, M ^c   Hansson, G I ^c   Gan, L M ^b,c  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b SAHLGRENSKA UNIVERSITY HOSPITAL   (Sweden)

^c ASTRAZENECA R AND D   (Sweden)

Author keywords

Apolipoprotein E knockout mouse; Atherosclerosis; Rosuvastatin; Ultrasound imaging

Indexed keywords

APOLIPOPROTEIN E; COLLAGEN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; ROSUVASTATIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ATHEROSCLEROSIS; CONTROLLED STUDY; DRUG EFFECT; HEART FUNCTION; HEART VOLUME; HISTOPATHOLOGY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; APOLIPOPROTEINS E; ATHEROSCLEROSIS; BIOLOGICAL MARKERS; BLOOD FLOW VELOCITY; BRACHIOCEPHALIC TRUNK; CORONARY CIRCULATION; CORONARY VESSELS; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; FLUOROBENZENES; HYDROXYMETHYLGLUTARYL-COA REDUCTASE INHIBITORS; INFLAMMATION MEDIATORS; LIPIDS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PYRIMIDINES; REGIONAL BLOOD FLOW; SULFONAMIDES; TIME FACTORS;

EID: 57049168787     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00133.2008     Document Type: Article

References (56)

1. Baigent C, Keech A, Kearney PM, Blackwell L, Back G, Pollicino C, Kirby A, Sourjina T, Peto R, Collins R, Simes R; Cholesterol Treatment Trialists (CTT) Collaborators. Efficacy and safety of cholesterol-lowering treatment: prospective meta-analysis of data from 90 056 participants in 14 randomised trials of statins. Lancet 366: 1267-1278, 2005.
2. Baller D, Notohamiprodjo G, Gleichmann U, Holzinger J, Weise R, Lehmann J. Improvement in coronary flow reserve determined by positron emission tomography after 6 months of cholesterol-lowering therapy in patients with early stages of coronary atherosclerosis. Circulation 99: 2871-2875, 1999.
3. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254, 1976.
4. Chen J, Li D, Schaefer R, Mehta JL. Cross-talk between dyslipidemia and renin-angiotensin system and the role of LOX-1 and MAPK in atherogenesis: studies with the combined use of rosuvastatin and candesartan. Atherosclerosis 184: 295-301, 2006.
5. 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 44: 446-452, 2004.
6. Choudhury RP, Carrelli AL, Stern JD, Chereshnev I, Soccio R, Elmalem VI, Fallon JT, Fisher EA, Reis ED. Effects of simvastatin on plasma lipoproteins and response to arterial injury in wild-type and apolipoprotein-E-deficient mice. J Vasc Res 41: 75-83, 2004.
7. Collins KA, Korcarz CE, Shroff SG, Bednarz JE, Fentzke RC, Lin H, Leiden JM, Lang RM. Accuracy of echocardiographic estimates of left ventricular mass in mice. Am J Physiol Heart Circ Physiol 280: H1954-H1962, 2001.
8. Cortigiani L, Rigo F, Gherardi S, Sicari R, Galderisi M, Bovenzi F, Picano E. Additional prognostic value of coronary flow reserve in diabetic and nondiabetic patients with negative dipyridamole stress echocardiography by wall motion criteria. J Am Coll Cardiol 50: 1354-1361, 2007.
9. Delsing DJ, Jukema JW, van de Wiel MA, Emeis JJ, van der Laarse A, Havekes LM, Princen HM. Differential effects of amlodipine and atorvastatin treatment and their combination on atherosclerosis in ApoE*3-Leiden transgenic mice. J Cardiovasc Pharmacol 42: 63-70, 2003.
10. Delsing DJ, Post SM, Groenendijk M, Solaas K, van der Boom H, van Duyvenvoorde W, de Wit EC, Bloks VW, Kuipers F, Havekes LM, Princen HM. Rosuvastatin reduces plasma lipids by inhibiting VLDL production and enhancing hepatobiliary lipid excretion in ApoE*3-leiden mice. J Cardiovasc Pharmacol 45: 53-60, 2005.
11. Farmer JA, Gotto AM Jr. Currently available hypolipidaemic drugs and future therapeutic developments. Baillieres Clin Endocrinol Metab 9: 825-847, 1995.
12. Fayad ZA, Fallon JT, Shinnar M, Wehrli S, Dansky HM, Poon M, Badimon JJ, Charlton SA, Fisher EA, Breslow JL, Fuster V. Noninvasive in vivo high-resolution magnetic resonance imaging of atherosclerotic lesions in genetically engineered mice. Circulation 98: 1541-1547, 1998.
13. Folch J, Lees M, Sloane Stanley GH. A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226: 497-509, 1957.
14. Foster FS, Zhang MY, Zhou YQ, Liu G, Mehi J, Cherin E, Harasiewicz KA, Starkoski BG, Zan L, Knapik DA, Adamson SL. A new ultrasound instrument for in vivo microimaging of mice. Ultrasound Med Biol 28: 1165-1172, 2002.
15. Fujimoto K, Hozumi T, Watanabe H, Shimada K, Takeuchi M, Sakanoue Y, Shimizu N, Ostuka R, Kawase Y, Sakamoto K, Yoshiyama M, Baba Y, Haze K, Yoshikawa J. Effect of fluvastatin therapy on coronary flow reserve in patients with hypercholesterolemia. Am J Cardiol 93: 1419-1421, 2004.
16. Gan LM, Grönros J, Hägg U, Wikström J, Theodoropoulos C, Friberg P, Fritsche-Danielson R. Non-invasive real-time imaging of atherosclerosis in mice using ultrasound biomicroscopy. Atherosclerosis 190: 313-320, 2007.
17. Guethlin M, Kasel AM, Coppenrath K, Ziegler S, Delius W, Schwaiger M. Delayed response of myocardial flow reserve to lipid-lowering therapy with fluvastatin. Circulation 99: 475-481, 1999.
18. Hinoi T, Matsuo S, Tadehara F, Tsujiyama S, Yamakido M. Acute effect of atorvastatin on coronary circulation measured by transthoracic Doppler echocardiography in patients without coronary artery disease by angiography. Am J Cardiol 96: 89-91, 2005.
19. Homan R, Anderson MK. Rapid separation and quantitation of combined neutral and polar lipid classes by high-performance liquid chromatography and evaporative light-scattering mass detection. J Chromatogr B Biomed Sci Appl 708: 21-26, 1998.
20. Illingworth DR, Bacon S. Hypolipidemic effects of HMG-CoA reductase inhibitors in patients with hypercholesterolemia. Am J Cardiol 60: 33G-42G, 1987.
21. Johnson J, Carson K, Williams H, Karanam S, Newby A, Angelini G, George S, Jackson C. Plaque rupture after short periods of fat feeding in the apolipoprotein E-knockout mouse: model characterization and effects of pravastatin treatment. Circulation 111: 1422-1430, 2005.
22. Kablak-Ziembicka A, Tracz W, Przewlocki T, Pieniazek P, Sokolowski A, Konieczynska M. Association of increased carotid intima-media thickness with the extent of coronary artery disease. Heart 90: 1286-1290, 2004.
23. Kleemann R, Princen HM, Emeis JJ, Jukema JW, Fontijn RD, Horrevoets AJ, Kooistra T, Havekes LM. Rosuvastatin reduces atherosclerosis development beyond and independent of its plasma cholesterol-lowering effect in APOE*3-leiden transgenic mice: evidence for antiinflammatory effects of rosuvastatin. Circulation 108: 1368-1374, 2003.
24. Klein RM, Schwartzkopff B, Gabbert HE, Strauer BE. Diminished coronary reserve in patients with biopsy-proven inflammatory infiltrates. Cardiology 100: 120-128, 2003.
25. Laufs U, La Fata V, Plutzky J, Liao JK. Upregulation of endothelial nitric oxide synthase by HMG CoA reductase inhibitors. Circulation 97: 1129-1135, 1998.
26. Liao JK, Laufs U. Pleiotropic effects of statins. Annu Rev Pharmacol Toxicol 45: 89-118, 2005.
27. Longo MR, Guzman AW, Triebwasser JH. Normal values and commonly used echocardiographic formulae for adults. Aviat Space Environ Med 46: 1062-1064, 1975.
28. López M, Lage R, Saha AK, Pérez-Tilve D, Vázquez MJ, Varela L, Sangiao-Alvarellos S, Tovar S, Raghay K, Rodríguez-Cuenca S, Deoliveira RM, Castañeda T, Datta R, Dong JZ, Culler M, Sleeman MW, Álvarez CV, Gallego R, Lelliott CJ, Carling D, Tschöp MH, Diéguez C, Vidal-Puig A. Hypothalamic fatty acid metabolism mediates the orexigenic action of ghrelin cell. Metabolism 7: 389-399, 2008.
29. Malik S, McGlone F, Bedrossian D, Dagher A. Ghrelin modulates brain activity in areas that control appetitive behavior. Cell Metab 7: 400-409, 2008.
30. Mancini GB, Abbott D, Kamimura C, Yeoh E. Validation of a new ultrasound method for the measurement of carotid artery intima medial thickness and plaque dimensions. Can J Cardiol 20: 1355-1359, 2004.
31. McAteer MA, Schneider JE, Clarke K, Neubauer S, Channon KM, Choudhury RP. Quantification and 3D reconstruction of atherosclerotic plaque components in apolipoprotein E knockout mice using ex vivo high-resolution MRI. Arterioscler Thromb Vasc Biol 24: 2384-2390, 2004.
32. Meredith IT, Plunkett JC, Worthley SG, Hope SA, Cameron JD. Systemic inflammatory markers in acute coronary syndrome: association with cardiovascular risk factors and effect of early lipid lowering. Coron Artery Dis 16: 415-422, 2005.
33. Monetti M, Canavesi M, Camera M, Parente R, Paoletti R, Tremoli E, Corsini A, Bellosta S. Rosuvastatin displays anti-atherothrombotic and anti-inflammatory properties in apoE-deficient mice. Pharm Res 55: 441-449, 2007.
34. Ni M, Zhang M, Ding SF, Chen WQ, Zhang Y. Micro-ultrasound imaging assessment of carotid plaque characteristics in apolipoprotein-E knockout mice. Atherosclerosis 197: 64-71, 2008.
35. Nissen SE, Nicholls SJ, Sipahi I, Libby P, Raichlen JS, Ballantyne CM, Davignon J, Erbel R, Fruchart JC, Tardif JC, Schoenhagen P, Crowe T, Cain V, Wolski K, Goormastic M, Tuzcu EM; ASTEROID Investigators. Effect of very high-intensity statin therapy on regression of coronary atherosclerosis: the ASTEROID trial. JAMA 295: 1556-1565, 2006.
36. Nissen SE, Tuzcu EM, Schoenhagen P, Crowe T, Sasiela WJ, Tsai J, Orazem J, Magorien RD, O'Shaughnessy C, Ganz P. Statin therapy, LDL cholesterol, C-reactive protein, and coronary artery disease. N Engl J Med 352: 29-38, 2005.
37. O'Driscoll G, Green D, Taylor RR. Simvastatin, an HMG-coenzyme A reductase inhibitor, improves endothelial function within 1 month. Circulation 95: 1126-1131, 1997.
38. Parini P, Gustafsson U, Davis MA, Larsson L, Einarsson C, Wilson M, Rudling M, Tomoda H, Omura S, Sahlin S, Angelin B, Rudel LL, Eriksson M. Cholesterol synthesis inhibition elicits an integrated molecular response in human livers including decreased ACAT2. Arterioscler Thromb Vasc Biol 28: 1200-1206, 2008.
39. -/- mice in vivo. Circulation 107: 2480-2486, 2003.
40. Reardon CA, Blachowicz L, Lukens J, Nissenbaum M, Getz GS. Genetic background selectively influences innominate artery atherosclerosis: immune system deficiency as a probe. Arterioscler Thromb Vasc Biol 23: 1449-1454, 2003.
41. Ridker PM, Rifai N, Pfeffer MA, Sacks FM, Moye LA, Goldman S, Flaker GC, Braunwald E. Inflammation, pravastatin, and the risk of coronary events after myocardial infarction in patients with average cholesterol levels. Cholesterol and Recurrent Events (CARE) Investigators. Circulation 98: 839-844, 1998.
42. Sahn DJ, DeMaria A, Kisslo J, Weyman A. Recommendations regarding quantitation in M-mode echocardiography: results of a survey of echocardiographic measurements. Circulation 58: 1072-1083, 1978.
43. Schachter M. Chemical, pharmacokinetic and pharmacodynamic properties of statins: an update. Fundam Clin Pharmacol 19: 117-125, 2005.
44. Stalker TJ, Lefer AM, Scalia R. A new HMG-CoA reductase inhibitor, rosuvastatin, exerts anti-inflammatory effects on the microvascular endothelium: the role of mevalonic acid. Br J Pharmacol 133: 406-412, 2001.
45. Stroes ES, Koomans HA, de Bruin TW, Rabelink TJ. Vascular function in the forearm of hypercholesterolaemic patients off and on lipid-lowering medication. Lancet 346: 467-471, 1995.
46. Tok D, Caliskan M, Gullu H, Erdogan D, Demirtas S, Muderrisoglu H. The association between hematological parameters and coronary flow reserve and coronary haemorheology in healthy subjects. Clin Hemorheol Microcirc 36: 345-352, 2007.
47. VanderLaan PA, Reardon CA, Getz GS. Site specificity of atherosclerosis: site-selective responses to atherosclerotic modulators. Arterioscler Thromb Vasc Biol 24: 12-22, 2004.
48. Verschuren L, Kleemann R, Offerman EH, Szalai AJ, Emeis SJ, Princen HM, Kooistra T. Effect of low dose atorvastatin versus diet-induced cholesterol lowering on atherosclerotic lesion progression and inflammation in apolipoprotein E*3-Leiden transgenic mice. Arterioscler Thromb Vasc Biol 25: 161-167, 2005.
49. Wang PY, Caspi L, Lam CK, Chari M, Li X, Light PE, Gutierrez-Juarez R, Ang M, Schwartz GJ, Lam TK. Upper intestinal lipids trigger a gut-brain-liver axis to regulate glucose production. Nature 452: 1012-1016, 2008.
50. Wang YX. Cardiovascular functional phenotypes and pharmacological responses in apolipoprotein E deficient mice. Neurobiol Aging 26: 309-316, 2005.
51. Wang YX, Martin-McNulty B, Huw LY, da Cunha V, Post J, Hinchman J, Vergona R, Sullivan ME, Dole W, Kauser K. Anti-atherosclerotic effect of simvastatin depends on the presence of apolipoprotein E. Atherosclerosis 162: 23-31, 2002.
52. Wikstrom J, Grönros J, Bergström G, Gan LM. Functional and morphologic imaging of coronary atherosclerosis in living mice using high-resolution color Doppler echocardiography and ultrasound biomicroscopy. J Am Coll Cardiol 46: 720-727, 2005.
53. Wikström J, Grönros J, Gan LM. Adenosine induces dilation of epicardial coronary arteries in mice - relationship between coronary flow velocity reserve and coronary flow reserve in vivo using transthoracic echocardiography. Ultrasound Med Biol 34: 1053-1062, 2008.
54. Williams H, Johnson JL, Carson KG, Jackson CL. Characteristics of intact and ruptured atherosclerotic plaques in brachiocephalic arteries of apolipoprotein E knockout mice. Arterioscler Thromb Vasc Biol 22: 788-792, 2002.
55. Zadelaar S, Kleemann R, Verschuren L, de Vries-Van der Weij J, van der Hoorn J, Princen HM, Kooistra T. Mouse models for atherosclerosis and pharmaceutical modifiers. Arterioscler Thromb Vasc Biol 27: 1706-1721, 2007.
56. Zhou YQ, Foster FS, Qu DW, Zhang M, Harasiewicz KA, Adamson SL. Applications for multifrequency ultrasound biomicroscopy in mice from implantation to adulthood. Physiol Genomics 10: 113-126, 2002.