Lowering plasma cholesterol levels halts progression of aortic valve disease in mice

Circulation

Volumn 119, Issue 20, 2009, Pages 2693-2701

  Miller, Jordan D ^a   Weiss, Robert M ^a   Serrano, Kristine M ^a   Brooks, Robert M ^a   Berry, Christopher J ^a   Zimmerman, Kathy ^a,b   Young, Stephen G ^c   Heistad, Donald D ^a,b  

^a UNIVERSITY OF IOWA   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Aortic valve stenosis; Calcification; Free radicals; Hypercholesterolemia; Valves

Indexed keywords

CALCIUM; CHOLESTEROL; CRE RECOMBINASE; MICROSOMAL TRIGLYCERIDE TRANSFER PROTEIN; SUPEROXIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA VALVE STENOSIS; ARTICLE; BONE DEVELOPMENT; CELL ACTIVATION; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE COURSE; ECHOCARDIOGRAPHY; GENE INACTIVATION; HYPERCHOLESTEROLEMIA; LIPID STORAGE; MOUSE; MYOFIBROBLAST; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; AORTIC VALVE STENOSIS; CARRIER PROTEINS; CHOLESTEROL; DISEASE PROGRESSION; GENE SILENCING; HYPERCHOLESTEROLEMIA; LIPIDS; MICE; MICE, MUTANT STRAINS; OSTEOGENESIS; OXIDATIVE STRESS;

EID: 67249120424     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.108.834614     Document Type: Article

References (49)

1. Bonow RO, Carabello B, de Leon AC, Edmunds LH Jr, Fedderly BJ, Freed MD, Gaasch WH, McKay CR, Nishimura RA, O'Gara PT, O'Rourke RA, Rahimtoola SH, Ritchie JL, Cheitlin MD, Eagle KA, Gardner TJ, Garson A Jr, Gibbons RJ, Russell RO, Ryan TJ, Smith SC Jr. ACC/AHA guidelines for the management of patients with valvular heart disease: executive summary: a report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines (Committee on Management of Patients With Valvular Heart Disease). J Heart Valve Dis. 1998;7:672-707.
2. Messika-Zeitoun D, Bielak LF, Peyser PA, Sheedy PF, Turner ST, Nkomo VT, Breen JF, Maalouf J, Scott C, Tajik AJ, Enriquez-Sarano M. Aortic valve calcification: determinants and progression in the population. Arterioscler Thromb Vasc Biol. 2007;27:642-648.
3. Otto CM, Kuusisto J, Reichenbach DD, Gown AM, O'Brien KD. Characterization of the early lesion of "degenerative" valvular aortic stenosis: histological and immunohistochemical studies. Circulation. 1994;90: 844-853.
4. Jian B, Jones PL, Li Q, Mohler ER 3rd, Schoen FJ, Levy RJ. Matrix metalloproteinase-2 is associated with tenascin-C in calcific aortic stenosis. Am J Pathol. 2001;159:321-327.
5. Kaden JJ, Vocke DC, Fischer CS, Grobholz R, Brueckmann M, Vahl CF, Hagl S, Haase KK, Dempfle CE, Borggrefe M. Expression and activity of matrix metalloproteinase-2 in calcific aortic stenosis. Z Kardiol. 2004; 93:124-130.
6. Satta J, Oiva J, Salo T, Eriksen H, Ohtonen P, Biancari F, Juvonen TS, Soini Y. Evidence for an altered balance between matrix metalloproteinase-9 and its inhibitors in calcific aortic stenosis. Ann Thorac Surg. 2003;76:681-688.
7. Rajamannan NM, Subramaniam M, Stock SR, Stone NJ, Springett M, Ignatiev KI, McConnell JP, Singh RJ, Bonow RO, Spelsberg TC. Ator-vastatin inhibits calcification and enhances nitric oxide synthase production in the hypercholesterolaemic aortic valve. Heart. 2005;91:806-810.
8. Liberman M, Bassi E, Martinatti MK, Lario FC, Wosniak J Jr, Pomer-antzeff PM, Laurindo FR. Oxidant generation predominates around calcifying foci and enhances progression of aortic valve calcification. Arterioscler Thromb Vasc Biol. 2008;28:463-470.
9. Miller JD, Chu Y, Brooks RM, Richenbacher WE, Pena-Silva RA, Heistad DD. Dysregulation of anti-oxidant mechanisms contributes to increased oxidative stress in calcific aortic valvular stenosis in humans. J Am Coll Cardiol. 2008;52:843-850.
10. Weiss RM, Ohashi M, Miller JD, Young SG, Heistad DD. Calcific aortic valve stenosis in old hypercholesterolemic mice. Circulation. 2006;114: 2065-2069.
11. Rajamannan NM, Subramaniam M, Rickard D, Stock SR, Donovan J, Springett M, Orszulak T, Fullerton DA, Tajik AJ, Bonow RO, Spelsberg T. Human aortic valve calcification is associated with an osteoblast phenotype. Circulation. 2003;107:2181-2184.
12. Rajamannan NM, Subramaniam M, Springett M, Sebo TC, Niekrasz M, McConnell JP, Singh RJ, Stone NJ, Bonow RO, Spelsberg TC. Atorva-statin inhibits hypercholesterolemia-induced cellular proliferation and bone matrix production in the rabbit aortic valve. Circulation. 2002;105: 2660-2665.
13. Tintut Y, Alfonso Z, Saini T, Radcliff K, Watson K, Bostrom K, Demer LL. Multilineage potential of cells from the artery wall. Circulation. 2003;108:2505-2510.
14. Tintut Y, Patel J, Territo M, Saini T, Parhami F, Demer LL. Monocyte/macrophage regulation of vascular calcification in vitro. Circulation. 2002;105:650-655.
15. Benzuly KH, Padgett RC, Kaul S, Piegors DJ, Armstrong ML, Heistad DD. Functional improvement precedes structural regression of atherosclerosis. Circulation. 1994;89:1810-1818.
16. Sipahi I, Nicholls SJ, Tuzcu EM, Nissen SE. Coronary atherosclerosis can regress with very intensive statin therapy. Cleve Clin J Med. 2006;73: 937-944.
17. Hathaway CA, Heistad DD, Piegors DJ, Miller FJ Jr. Regression of atherosclerosis in monkeys reduces vascular superoxide levels. Circ Res. 2002;90:277-283.
18. Harrison DG, Armstrong ML, Freiman PC, Heistad DD. Restoration of endothelium-dependent relaxation by dietary treatment of atherosclerosis. J Clin Invest. 1987;80:1808-1811.
19. Corti R, Osende JI, Fallon JT, Fuster V, Mizsei G, Jneid H, Wright SD, Chaplin WF, Badimon JJ. The selective peroxisomal proliferator-acti-vated receptor-gamma agonist has an additive effect on plaque regression in combination with simvastatin in experimental atherosclerosis: in vivo study by high-resolution magnetic resonance imaging. J Am Coll Cardiol. 2004;43:464-473.
20. Novaro GM, Tiong IY, Pearce GL, Lauer MS, Sprecher DL, Griffin BP. Effect of hydroxymethylglutaryl coenzyme a reductase inhibitors on the progression of calcific aortic stenosis. Circulation. 2001;104:2205-2209.
21. Shavelle DM, Takasu J, Budoff MJ, Mao S, Zhao XQ, O'Brien KD. HMG CoA reductase inhibitor (statin) and aortic valve calcium. Lancet. 2002;359:1125-1126.
22. Cowell SJ, Newby DE, Prescott RJ, Bloomfield P, Reid J, Northridge DB, Boon NA. A randomized trial of intensive lipid-lowering therapy in calcific aortic stenosis. N Engl J Med. 2005;352:2389-2397.
23. Moura LM, Ramos SF, Zamorano JL, Barros IM, Azevedo LF, Rocha-Goncalves F, Rajamannan NM. Rosuvastatin affecting aortic valve en-dothelium to slow the progression of aortic stenosis. J Am Coll Cardiol. 2007;49:554-561.
24. Rossebo AB, Pedersen TR, Boman K, Brudi P, Chambers JB, Egstrup K, Gerdts E, Gohlke-Barwolf C, Holme I, Kesaniemi YA, Malbecq W, Nienaber CA, Ray S, Skjaerpe T, Wachtell K, Willenheimer R. Intensive lipid lowering with simvastatin and ezetimibe in aortic stenosis. N Engl J Med. 2008;359:1343-1356.
25. Yildirir A, Muderrisoglu H. Non-lipid effects of statins: emerging new indications. Curr Vasc Pharmacol. 2004;2:309-318.
26. Drolet MC, Roussel E, Deshaies Y, Couet J, Arsenault M. A high fat/high carbohydrate diet induces aortic valve disease in C57BL/6J mice. J Am Coll Cardiol. 2006;47:850-855.
27. Tanaka K, Sata M, Fukuda D, Suematsu Y, Motomura N, Takamoto S, Hirata Y, Nagai R. Age-associated aortic stenosis in apolipoprotein E-deficient mice. J Am Coll Cardiol. 2005;46:134-141.
28. Lieu HD, Withycombe SK, Walker Q, Rong JX, Walzem RL, Wong JS, Hamilton RL, Fisher EA, Young SG. Eliminating atherogenesis in mice by switching off hepatic lipoprotein secretion. Circulation. 2003;107: 1315-1321.
29. Hussain MM, Shi J, Dreizen P. Microsomal triglyceride transfer protein and its role in apoB-lipoprotein assembly. J Lipid Res. 2003;44:22-32.
30. Barry-Lane PA, Patterson C, van der Merwe M, Hu Z, Holland SM, Yeh ET, Runge MS. p47phox is required for atherosclerotic lesion progression in ApoE(-/-) mice. J Clin Invest. 2001;108:1513-1522.
31. Csiszar A, Labinskyy N, Jo H, Ballabh P, Ungvari ZI. Differential pro-inflammatory and pro-oxidant effects of bone morphogenetic protein-4 in coronary and pulmonary arterial endothelial cells. Am J Physiol Heart Circ Physiol. 2008;295:H569-H577.
32. Shao JS, Aly ZA, Lai CF, Cheng SL, Cai J, Huang E, Behrmann A, Towler DA. Vascular Bmp Msx2 Wnt signaling and oxidative stress in arterial calcification. Ann N Y Acad Sci. 2007;1117:40-50.
33. Bai XC, Lu D, Liu AL, Zhang ZM, Li XM, Zou ZP, Zeng WS, Cheng BL, Luo SQ. Reactive oxygen species stimulates receptor activator of NF-kappaB ligand expression in osteoblast. J Biol Chem. 2005;280: 17497-17506.
34. Pang M, Martinez AF, Fernandez I, Balkan W, Troen BR. AP-1 stimulates the cathepsin K promoter in RAW 264.7 cells. Gene. 2007;403: 151-158.
35. Byon CH, Javed A, Dai Q, Kappes JC, Clemens TL, Darley-Usmar VM, McDonald JM, Chen Y. Oxidative stress induces vascular calcification through modulation of the osteogenic transcription factor Runx2 by AKT signaling. J Biol Chem. 2008;283:15319-15327.
36. Mody N, Parhami F, Sarafian TA, Demer LL. Oxidative stress modulates osteoblastic differentiation of vascular and bone cells. Free Radic Biol Med. 2001;31:509-519.
37. Libby P. The molecular mechanisms of the thrombotic complications of atherosclerosis. J Intern Med. 2008;263:517-527.
38. Williams KJ, Feig JE, Fisher EA. Rapid regression of atherosclerosis: insights from the clinical and experimental literature. Nat Clin Pract Cardiovasc Med. 2008;5:91-102.
39. Osman L, Chester AH, Sarathchandra P, Latif N, Meng W, Taylor PM, Yacoub MH. A novel role of the sympatho-adrenergic system in regulating valve calcification. Circulation. 2007;116(suppl):I-282-I-287.
40. Johnson KA, Polewski M, Terkeltaub RA. Transglutaminase 2 is central to induction of the arterial calcification program by smooth muscle cells. Circ Res. 2008;102:529-537.
41. Tanaka T, Sato H, Doi H, Yoshida CA, Shimizu T, Matsui H, Yamazaki M, Akiyama H, Kawai-Kowase K, Iso T, Komori T, Arai M, Kurabayashi M. Runx2 represses myocardin-mediated differentiation and facilitates osteogenic conversion of vascular smooth muscle cells. Mol Cell Biol. 2008;28:1147-1160.
42. Miller JD, Chu Y, Brooks RM, Richenbacher WE, Pena-Silva R, Heistad DD. Dysregulation of antioxidant mechanisms contributes to increased oxidative stress in calcific aortic valvular stenosis in humans. J Am Coll Cardiol. 2008;52:843-850.
43. Marie PJ. Transcription factors controlling osteoblastogenesis. Arch Biochem Biophys. 2008;473:98-105.
44. Stary HC. The development of calcium deposits in atherosclerotic lesions and their persistence after lipid regression. Am J Cardiol. 2001;88: 16E-19E.
45. Euler-Taimor G, Heger J. The complex pattern of SMAD signaling in the cardiovascular system. Cardiovasc Res. 2006;69:15-25.
46. Jian B, Narula N, Li QY, Mohler ER 3rd, Levy RJ. Progression of aortic valve stenosis: TGF-betal is present in calcified aortic valve cusps and promotes aortic valve interstitial cell calcification via apoptosis. Ann Thorac Surg. 2003;75:457-465.
47. Helske S, Syvaranta S, Kupari M, Lappalainen J, Laine M, Lommi J, Turto H, Mayranpaa M, Werkkala K, Kovanen PT, Lindstedt KA. Possible role for mast cell-derived cathepsin G in the adverse remodelling of stenotic aortic valves. Eur Heart J. 2006;27:1495-1504.
48. Rosenhek R, Rader F, Loho N, Gabriel H, Heger M, Klaar U, Schemper M, Binder T, Maurer G, Baumgartner H. Statins but not angiotensin-converting enzyme inhibitors delay progression of aortic stenosis. Circulation. 2004;110:1291-1295.
49. Chen Z, Fukutomi T, Zago AC, Ehlers R, Detmers PA, Wright SD, Rogers C, Simon DI. Simvastatin reduces neointimal thickening in low-density lipoprotein receptor-deficient mice after experimental angioplasty without changing plasma lipids. Circulation. 2002;106: 20-23.