Common pathogenic features of atherosclerosis and calcific aortic stenosis: Role of transforming growth factor-β

Cardiovascular Pathology

Volumn 19, Issue 4, 2010, Pages 236-247

  Xu, Songyi ^a,b   Liu, Amber C ^a,b   Gotlieb, Avrum I ^a,b  

^a UNIVERSITY HEALTH NETWORK   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

Atherosclerosis; Calcific aortic stenosis; Statin; Transforming growth factor ; Valve interstitial cell

Indexed keywords

HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL; AORTIC VALVE STENOSIS; ARTERY; ATHEROSCLEROSIS; CALCINOSIS; CELL CULTURE; DISEASE MODEL; DRUG EFFECTS; HUMAN; METABOLISM; PATHOLOGY; RANDOMIZED CONTROLLED TRIAL (TOPIC); VASCULAR ENDOTHELIUM;

ANIMALS; AORTIC VALVE STENOSIS; ARTERIES; ATHEROSCLEROSIS; CALCINOSIS; CELLS, CULTURED; DISEASE MODELS, ANIMAL; ENDOTHELIUM, VASCULAR; HUMANS; HYDROXYMETHYLGLUTARYL-COA REDUCTASE INHIBITORS; RANDOMIZED CONTROLLED TRIALS AS TOPIC; TRANSFORMING GROWTH FACTOR BETA;

EID: 77956310581     PISSN: 10548807     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.carpath.2009.09.007     Document Type: Review

References (97)

1. Stewart BF, Siscovick D, Link BK, Gardin JM, Gottdiener JS, Smith VE, Kitzman DW, and Otto CM. Clinical factors associated with calcific aortic valve disease. Cardiovascular Health Study J Am Coll Cardiol 29 1997 630 634
2. Otto CM, Burwash IG, Legget ME, Munt BI, Fujioka M, Healy NL, Kraft CD, Miyake-Hull CY, and Schwaegler RG. Prospective study of asymptomatic valvular aortic stenosis. Clinical, echocardiographic, and exercise predictors of outcome Circulation 95 1997 2262 2270
3. Otto CM, Link BK, Kitzman DW, Gersch BJ, and Siscovick DS Association of aortic-valve sclerosis with cardiovascular mortality and morbidity in the elderly N Engl J Med 341 1999 142 147
4. Napoli C, and Cacciatore F Novel pathogenic insights in the primary prevention of cardiovascular disease Prog Cardiovasc Dis 51 2009 503 523
5. Lane HC. The active venous pulse in the wing circulation of bats (Chiroptera). Histology of the vascular wall and its innervation Experientia 34 1978 1403 1410
6. Marron K, Yacoub MH, Polak JM, Sheppard MN, Fagan D, Whitehead BF, de Leval MR, Anderson RH, and Wharton J Innervation of human atrioventricular and arterial valves Circulation 94 1996 368 375
7. Borin C, Vanhercke D, and Weyns A Innervation of the atrioventricular and semi-lunar heart valves: a review Acta Cardiol 61 2006 463 469
8. Cunningham KS, and Gotlieb AI The role of shear stress in the pathogenesis of atherosclerosis Lab Invest 85 2005 9 23
9. Simmons CA, Grant GR, Manduchi E, and Davies PF Spatial heterogeneity of endothelial phenotypes correlates with side-specific vulnerability to calcification in normal porcine aortic valves Circ Res 96 2005 792 799
10. Butcher JT, Tressel S, Johnson T, Turner D, Sorescu G, Jo H, and Nerem RM. Transcriptional profiles of valvular and vascular endothelial cell reveal phenotypic differences: influence of shear stress Arterioscler Thromb Vasc Biol 26 2006 69 77
11. Topouzis S, and Majesky MW. Smooth muscle lineage diversity in the chick embryo. Two types of aortic smooth muscle cell differ in growth and receptor-mediated transcriptional responses to transforming growth factor-β Dev Biol 178 1996 430 445
12. Oh J, Richardson JA, and Olson EN Requirement of myocardin-related transcriptional factor-B for remodeling of branchial arch arteries and smooth muscle differentiation PNAS 102 2005 15122 15127
13. Combs MD, and Yutzey KE Heart valve development: regulatory networks in development and disease Circ Res 105 2009 408 421
14. Clowes AW, Clowes MW, Fingerle J, and Reidy MA Regulation of smooth muscle cell growth in injured artery J Cardiovasc Pharmacol 14 1989 S12 S15
15. Fayet C, Bendeck MP, and Gotlieb AI Cardiac valve interstitial cells secrete fibronectin and form fibrillar adhesions in response to injury Cardiovasc Pathol 16 2007 203 211
16. Liu AC, and Gotlieb AI Transforming growth factor-β regulates in vitro heart valve repair by activated valve interstitial cells Am J Pathol 173 2008 1275 1285
17. Adiquzel E, Ahmad PJ, Franco C, and Bendeck MP Collagen in the progression and complications of atherosclerosis Vasc Med 14 2009 73 89
18. Blevins TL, Peterson SB, Lee EL, Bailey AM, Frederick JD, Huynh TN, Gupta V, and Grande-Allen KJ Mitral valvular interstitial cells demonstrate regional, adhesional, and synthetic heterogeneity Cells Tissues Organs 187 2008 113 122
19. Majesky MW, and Schwartz SM Smooth muscle diversity in arterial wound repair Toxicol Pathol 18 1990 554 559
20. Lester W, Rosenthal A, Granton B, and Gotlieb AI Porcine mitral valve interstitial cells in culture Lab Invest 59 1988 710 719
21. Liu AC, Joag VR, and Gotlieb AI The emerging role of valve interstitial cell phenotypes in regulating heart valve pathobiology Am J Pathol 171 2007 1407 1418
22. Hao H, Gabbiani G, and Bochaton-Piallat M Arterial smooth muscle cell heterogeneity: implications for atherosclerosis and restenosis development Aterioscler Thromb Vasc Biol 23 2003 1510 1520
23. Norris RA, Moreno-Rodriguez RA, Sugi Y, Hoffman S, Amos J, Hart MM, Potts JD, Goodwin RL, and Markwald RR Periostin regulates atrioventricular valve maturation Dev Biol 316 2008 200 213
24. Aikawa E, Whittaker P, Farber M, Mendelson K, Padera RF, Aikawa M, and Schoen FJ. Human semilunar cardiac valve remodelling by activated cells from fetus to adult: Implications of postnatal adaptation, pathology, and tissue engineering Circulation 113 2006 1344 1352
25. Walker GA, Masters KS, Shah DN, Anseth KS, and Leinwand LA Valvular myofibroblast activation by transforming growth factor-β: implications for pathological extracellular matrix remodelling in heart valve disease Circ Res 95 2004 253 260
26. Cushing MC, Liao JT, and Anseth KS Activation of valvular interstitial cells is mediated by transforming growth factor-beta1 interactions with matrix molecules Matrix Biol 24 2005 428 437
27. Desmouliere A, Chaponnier C, and Gabbiani G Tissue repair, contraction, and the myofibroblast Wound Rep Reg 13 2005 7 12
28. Hinz B, Phan SH, Thannickal VJ, Galli A, Bochaton-Piallat M, and Gabbiani G The myofibroblast: one function, multiple origins Am J Pathol 170 2007 1807 1816
29. Visconti RP, Ebihara Y, LaRue AC, Fleming PA, McQuinn TC, Masuya M, Minamiguchi H, Markwald RR, Ogawa M, and Drake CJ An in vivo analysis of hematopoietic stem cell potential: hematopoietic origin of cardiac valve interstitial cells Circ Res 98 2006 690 696
30. Chen J, Yip CYY, Sone ED, and Simmons CA Identification and characterization of aortic valve mesenchymal progenitor cells with robust osteogenic calcification potential Am J Pathol 174 2009 1109 1119
31. Watson KE, Parhami F, Shin V, and Demer LL Fibronectin and collagen I matrixes promote calcification of vascular cells in vitro, whereas collagen IV matrix is inhibitory Arterioscler Thromb Vasc Biol 18 1998 1964 1971
32. Zacks S, Rosenthal A, Granton B, Havenith M, Opas M, and Gotlieb AI Characterization of cobblestone mitral valve interstitial cells Arch Pathol Lab Med 115 1991 774 779
33. O' Brien KD Pathogenesis of calcific aortic valve disease-a disease process comes of age (and a good deal more) Arterioscler Thromb Vasc Biol 26 2006 1721 1728
34. Rajamannan NM, Subramaniam M, Springett M, Sebo TC, Niekrasz M, McConnell JP, Singh RJ, Stone NJ, Bonow RO, and Spelsberg TC Atorvastatin inhibits hypercholesterolemia-induced cellular proliferation and bone matrix production in the rabbit aortic valve Circulation 105 2002 2660 2665
35. Rajamannan NM, Subramaniam M, Stock SR, Stone NJ, Springett M, Ignatiev KI, McConnell JP, Singh RJ, Bonow RO, and Spelsberg TC Atorvastatin inhibits calcification and enhances nitric oxide synthase production in the hypercholesterolemic aortic valve Heart 91 2005 806 810
36. Rajamannan NW, Subramaniam M, Caira F, Stock SR, and Spelsberg TC Atorvastatin inhibits hypercholesterolemia-induced calcification in the aortic valves via the Lrp5 receptor pathway Circulation 112 2005 I 229-I-234
37. Anger T, Carson W, Weyand M, Daniel WG, Hoeher M, and Garlichs CD Atherosclerotic inflammation triggers osteogenic bone transformation in calcified and stenotic human aortic valves: still a matter of debate Exp Mol Pathol 86 2009 10 17
38. Lindroos M, Kupari M, Heikkila J, and Tilvis R Prevalence of aortic valve abnormalities in the elderly: an echocardiographic study of a random population sample J Am Coll Cardiol 21 1993 1220 1225
39. Kaden JJ, Dempfle C, Grobholz R, Fischer CS, Vocke DC, Kilic R, Sarikoc A, Pinol R, Hagl S, Lang S, Brueckmann M, and Borggrefe M Inflammatory regulation of extracellular matrix remodeling in calcific aortic valve stenosis Cardiovasc Pathol 14 2005 80 87
40. Virmani R, Burke AP, Farb A, and Kolodgie FD Pathology of the vulnerable plaque J Am Coll Cardiol 47 2006 C13 C18
41. Ribatti D, Levi-Schaffer F, and Kovanen PT Inflammatory angiogenesis in atherogenesis-a double-edged sword Ann Med 40 2008 606 621
42. Kolodgie FD, Narula J, Yuan C, Burke AP, Finn AV, and Virmani R Elimination of neoangiogenesis for plaque stabilization. Is there a role for local drug therapy? J Am Coll Cardiol 49 2007 2093 2101
43. Sliumer JC, Kolodgie FD, Bijnens APJJ, Maxfield K, Pacheco E, Kutys B, Duimel H, Frederik PM, van Hinsbergh VWM, Virmani R, and Daemen MJAP Thin-walled microvessels in human coronary atherosclerotic plaques show incomplete endothelial junctions J Am Col Cardiol 53 2009 1517 1527
44. Hakuno D, Kimura N, Yoshioka M, and Fukuda K Molecular mechanisms underlying the onset of degenerative aortic valve disease J Mol Med 87 2009 17 24
45. Soini Y, Salo T, and Satta J Angiogenesis is involved in the pathogenesis of nonrheumatic aortic valve stenosis Hum Pathol 34 2003 756 763
46. Chalajour F, Treede H, Ebrahimnejad A, Lauke H, Reichenspurner H, and Ergun S Angiogenic activation of valvular endothelial cells in aortic valve stenosis Exp Cell Res 298 2004 455 464
47. Chalajour F, Treede H, Gehling UM, Ebrahimnejad A, Boehm DH, Riemer RK, Ergun S, and Reichenspurner H Identification and characterization of cells with high angiogenic potential and transitional phenotype in calcific aortic valve Exp Cell Res 313 2007 2326 2335
48. Yoshioka M, Yuasa S, Matsumura K, Kimura K, Shiomi T, Kimura N, Shukunami C, Okada Y, Mukai M, Shin H, Yozu R, Sata M, Ogawa S, Hiraki Y, and Fukuda K Chondromodulin-I maintains cardiac valvular function by preventing angiogenesis Nat Med 12 2006 1151 1159
49. Singh NN, and Ramji DP The role of TGF-β in atherosclerosis Cytokine Growth Factor Rev 17 2006 487 499
50. Taipale J, Saharinen J, Hedman K, and Keski-Oja J Latent transforming growth factor-beta 1 and its binding protein are components of extracellular matrix microfibrils J Histochem Cytochem 44 1996 875 889
51. Jian B, Narula N, Li Q, Mohler ER, and Levy RJ. Progression of aortic valve stenosis: TGF-β1 is present in calcified aortic valve cusps and promotes aortic valve interstitial cell calcification via apoptosis Ann Thorac Surg 75 2003 457 466
52. Clark-Greuel JN, Connolly JM, Sorichillo E, Narula NR, Rapoport S, Mohler ER, Gorman JH, Gorman RC, and Levy RJ Transforming growth factor-β1 mechanisms in aortic valve calcification: increased alkaline phosphatase and related events Ann Thorac Surg 83 2007 946 953
53. ten Dijke P, and Hill CS New insights into TGF-β-Smad signalling Trends Biochem Sci 29 2004 265 273
54. Misiakos EP, Kouraklis G, Agapitos E, Perrea D, Karatzas G, Boudoulas H, and Karayannakos PE. Expression of PDGF-A, TGFb and VCAM-1 during the developmental stages of experimental atherosclerosis Eur Surg Res 33 2001 264 269
55. Majesky MW, Lindner V, Twardzik DR, Schwartz SM, and Reidy MA Production of transforming growth factor beta 1 during repair of arterial injury J Clin Invest 88 1991 904 910
56. Little PJ, Tannock L, Olin KL, Chait A, and Wight TN Proteoglycans synthesized by arterial smooth muscle cells in the presence transforming growth factor-β1 exhibit increased binding to LDLs Arterioscler Thromb Vasc Biol 22 2002 55 60
57. Stouffer GA, and Owens GK TGF-β promotes proliferation of cultured SMC via both PDGF-AA-dependent and PDGF-AA-independent mechanisms J Clin Invest 93 1994 2048 2055
58. Nabel EG, Shum L, Pompili VJ, Yang Z, San H, Shu HB, Liptay S, Gold L, Gordon D, Derynck R, and Nabel GJ Direct transfer of transforming growth factor β1 gene into arteries stimulates fibrocellular hyperplasia Proc Natl Acad Sci USA 90 1993 10759 10763
59. Ghosh J, Murphy MO, Turner N, Khwaja N, Halka A, Kielty CM, and Walker MG The role of transforming growth factor β1 in the vascular system Cardiovasc Pathol 14 2005 28 36
60. Grainger DJ, Kemp PR, Metcalfe JC, Liu AC, Lawn RM, Williams NR, Grace AA, Schofield PM, and Chauhan A The serum concentration of active transforming growth factor-β is severely depressed in advanced atherosclerosis Nat Med 1 1995 74 79
61. Mallat Z, Gojova A, Marchiol-Fournigault C, Esposito B, Kamate C, Merval R, Fradelizi D, and Tedgui A Inhibition of transforming growth factor-β signalling accelerates atherosclerosis and induces an unstable plaque phenotype in mice Circ Res 89 2001 930 934
62. Werner F, Jain MK, Feinberg MW, Sibinga NES, Pellacani A, Wiesel P, Chin MT, Topper JN, Perrella MA, and Lee M Transforming growth factor-β1 inhibition of macrophage activation is mediated via smad3 J Biol Chem 275 2000 36653 36658
63. Harris H, Kirschenlohr H, Szabados N, and Metcalfe J Transforming growth factor-beta1 inhibits thrombin activation of endothelial cells Cytokine 25 2004 85 93
64. Febbo CD, Baccante G, Reale M, Castellani ML, Angelini A, Cuccurullo F, and Porreca E Transforming growth factor β1 induces IL-1 receptor antagonist production and gene expression in rat vascular smooth muscle cells Atherosclerosis 136 1998 377 382
65. Feinberg MW, Shimizu K, Lebedeva M, Haspel R, Takayama K, Chen Z, Frederick JP, Wang X, Simon DI, Libby P, Mitchell RN, and Jain MK Essential role for Smad3 in regulating MCP-1 expression and vascular inflammation Circ Res 94 2004 601 608
66. Smith WB, Noack L, Khew-Goodall Y, Isenmann S, Vadas MA, and Gamble JR Transforming growth factor-β1 inhibits the production of IL-8 and the transmigration of neutrophils through activated endothelium J Immunol 157 1996 360 368
67. Lawrence R, Hartmann DJ, and Sonenshein GE Transforming growth factor β1 stimulates type V collagen expression in bovine vascular smooth muscle cells J Biol Chem 269 1994 9603 9609
68. Cipollone F, Fazia M, Mincione G, Iezzi A, Pini B, Cuccurullo C, Ucchino S, Spigonardo F, Nisio MD, Cuccurullo F, Mezzetti A, and Porreca E Increased expression of transforming growth factor-{beta}1 as a stabilizing factor in human atherosclerotic plaques Stroke 35 2004 2253 2257
69. Grainger DJ, Mosedale DE, Metcalfe JC, and Bottinger E Dietary fat and reduced levels of TGFβ1 act synergistically to promote activation of the vascular endothelium and formation of lipid lesions J Cell Sci 113 2000 2355 2361
70. Grainger DJ, Witchell CM, and Metcalfe JC Tamoxifen elevates transforming growth factor-β and suppresses diet-induced formation of lipid lesions in mouse aorta Nat Med 1 1995 1067 1073
71. Argmann CA, Van Den Diepstraten CH, Sawyez CG, Edwards JY, Hegele RA, Wolfe BM, and Huff MW Transforming growth factor-β1 inhibits macrophage cholesteryl ester accumulation induced by native and oxidized VLDL remnants Arterioscler Thromb Vasc Biol 21 2001 2011 2018
72. Feinberg MW, Watanabe M, Lebedeva MA, Depina AS, Hanai J, Mammoto T, Frederick JP, Wang X, Sukhatme VP, and Jain MK Transforming growth factor-β1 inhibition of vascular smooth muscle cell activation is mediated via Smad3 J Biol Chem 279 2004 16388 16393
73. Kobayashi K, Yokote K, Fujimoto M, Yamashita K, Sakamoto A, Kitahara M, Kawamura H, Maezawa Y, Asaumi S, Tokuhisa T, Mori S, and Saito Y Targeted disruption of TGF-β-smad3 signaling leads to enhanced neointimal hyperplasia with diminished matrix deposition in response to vascular injury Circ Res 96 2005 904 912
74. McCaffrey TA, Consigli S, Du B, Falcone DJ, Sanborn TA, Spokojny AM, and Bush HL Decreased type II/type I TGF-β receptor ratio in cells derived from human atherosclerotic lesions J Clin Invest 96 1995 2667 2675
75. Goumans M, Valdimarsdottir G, Itoh S, Rosendahl A, Sideras P, and Dijke PT Balancing the activation state of the endothelium via two distinct TGF-β type I receptors EMBO J 21 2002 1743 1753
76. Kojima S, Harpel PC, and Rifkin DB Lipoprotein (a) inhibits the generation of transforming growth factor β: an endogenous inhibitor of smooth muscle cell migration J Cell Biol 113 1991 1439 1445
77. Ng CM, Cheng A, Myers LA, Martinez-Murillo F, Jie C, Bedja D, Gabrielson KL, Hausladen JM, Mecham RP, Judge DP, and Dietz HC TGF-β-dependent pathogenesis of mitral valve prolapsed in a mouse model of Marfan syndrome J Clin Invest 114 2004 1543 1592
78. Loeys BL, Schwarze U, Holm T, Callewaert BL, Thomas GH, Pannu H, De Backer JF, Oswald GL, Symoens S, Manouvrier S, Roberts AE, Faravelli F, Greco MA, Pyeritz RE, Milewicz DM, Coucke PJ, Cameron DE, Braverman AC, Byers PH, De Paepe AM, and Dietz HC Aneurysm syndromes caused by mutations in the TGF-beta receptor N Eng J Med 355 2006 788 798
79. Frutkin AD, Otsuka G, Stempien-Otero A, Sesti C, Du L, Jaffe M, Dichek HL, Pennington CJ, Edwards DR, Nieves-Cintron M, Minter D, Preusch M, Hu JH, Marie JC, and Dichek DA TGF-β1 limits plaque growth, stabilizes plaque structure, and prevents aortic dilation in apolipoprotein E-null mice Arterioscler Thromb Vasc Biol 29 2009 1251 1257
80. Aronow WS, Ahn C, Kronzon I, and Goldman ME Association of coronary risk factors and use of statins with progression of mild valvular aortic stenosis in older persons Am J Cardiol 88 2001 693 695 (Pubitemid 32831111)
81. Novaro GM, Tiong IY, Pearce GL, Lauer MS, Sprecher DL, and Griffin BP Effect of hydroxymethylglutaryl coenzyme A reductase inhibitors on the progression of calcific aortic stenosis Circulation 104 2001 2205 2209
82. Shavelle DM, Takasu J, Budoff MJ, Mao SS, Zhao X, and O'Brien KD HMG CoA reductase inhibitor (statin) and aortic valve calcium Lancet 359 2002 1125 1126
83. Moura LM, Ramos SF, Zamorano JL, Barros IM, Azevedo LF, Rocha-Gonçalves F, and Rajamannan NM Rosuvastatin affecting aortic valve endothelium to slow the progression of aortic stenosis J Am Coll Cardiol 49 2007 554 561
84. Rossebø AB, Pedersen TR, Boman K, Brudi P, Chambers JB, Egstrup K, Gerdts E, Gohlke-Bärwolf C, Holme I, Kesäniemi YA, Malbecq W, Nienaber CA, Ray S, Skjærpe T, Wachtell K, and Willenheimer R Intensive lipid lowering with simvastatin and ezetimibe in aortic stenosis N Engl J Med 359 2008 1343 1356
85. Cowell SJ, Newby DE, Prescott RJ, Bloomfield P, Reid J, Northridge DB, and Boon NA A randomized trial of intensive lipid-lowering therapy in calcific aortic stenosis N Engl J Med 352 2005 2389 2397
86. Chan K, Teo K, Tam J, and Dumesnil JG Astronomer investigators. Rationale, design, and baseline characteristics of a randomized trial to assess the effect of cholesterol lowering on the progression of aortic stenosis: the aortic stenosis progression observation: measuring effects of rosuvastatin (ASTRONOMER) trial Am Heart J 153 2007 925 931
87. Wu B, Elmariah S, Kaplan FS, Cheng G, and Mohler ER Paradoxical effects of statins on aortic valve myofibroblasts and osteoblasts Arterioscler Thromb Vasc Biol 25 2005 592 597
88. Bea F, Blessing E, Shelley MI, Shultz JM, and 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 167 2003 187 194
89. Bellamy MF, Pellikka PA, Klarich KW, Tajik AJ, and Enriquez-Sarano M Association of cholesterol levels, hydroxymethylglutaryl coenzyme-A reductase inhibitor treatment, and progression of aortic stenosis in the community J Am Coll Cardiol 40 2002 1723 1730
90. Rosenhek R, Rader F, Loho N, Gabriel H, Heger M, Klaar U, Schemper M, Binder T, Maurer G, and Baumgartner H Statins but not angiotensin-converting enzyme inhibitors delay progression of aortic stenosis Circulation 110 2004 1291 1295
91. Monzack EL, Gu X, and Masters KS Efficacy of simvastatin treatment of valvular interstitial cells varies with the extracellular environment Arterioscler Thromb Vasc Biol 29 2009 246 253
92. Osman L, Chester AH, Amrani M, Yacoub MH, and Smolenski RT A novel role of extracellular nucleotides in valve calcification Circulation 114 2006 I 556-I-572
93. Osman L, Yacoub MH, Latif N, Amrani M, and Chester AH Role of human valve interstitial cells in valve calcification and their response to atorvastatin Circulation 114 2006 I 547-I-552
94. Rodriguez-Vita J, Sanchez-Galan E, Santamaria B, Sanchez-Lopez E, Rodriguez-Diez R, Blanco-Colio LM, Egido J, Ortiz A, and Ruiz-Ortega M Essential role of TGF-β/Smad pathway on statin dependent vascular smooth muscle cell regulation PLoS ONE 3 2008 e3959
95. O'Brien KD, Shavelle DM, Caulfield MT, McDonald TO, Olin-Lewis K, Otto CM, and Probstfield JL Association of angiotensin-converting enzyme with low-density lipoprotein in aortic valvular lesions and in human plasma Circulation 106 2002 2224 2230
96. Arishiro K, Hoshiga M, Negoro N, Jin D, Takai S, Miyazaki M, Ishihara T, and Hanafusa T Angiotensin receptor-1 blocker inhibits atherosclerotic changes and endothelial disruption of the aortic valve in hypercholesterolemic rabbits J Am Coll Cardiol 49 2007 1482 1489
97. O'Brien KD, Probstfield JL, Caulfield MT, Nasir K, Takasu J, Shavelle DM, Wu AH, Zhao XO, and Budoff MJ Angiotensin-converting enzyme inhibitors and change in aortic valve calcium Arch Intern Med 165 2005 858 862