Thin-capped atheromata with reduced collagen content in pigs develop in coronary arterial regions exposed to persistently low endothelial shear stress

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 33, Issue 7, 2013, Pages 1494-1504

  Koskinas, Konstantinos C ^a,b   Sukhova, Galina K ^a   Baker, Aaron B ^b,c   Papafaklis, Michail I ^a,b   Chatzizisis, Yiannis S ^a,b   Coskun, Ahmet U ^a   Quillard, Thibaut ^a   Jonas, Michael ^b   Maynard, Charles ^d   Antoniadis, Antonios P ^a   Shi, Guo Ping ^a   Libby, Peter ^a   Edelman, Elazer R ^a,b   Feldman, Charles L ^a   Stone, Peter H ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c The University of Texas at Austin   (United States)

^d UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Atherosclerosis; Collagen; Endothelial shear stress; Metalloproteinases; Natural history

Indexed keywords

COLLAGEN; COLLAGENASE 3; FIBRILLAR COLLAGEN; INTERSTITIAL COLLAGENASE; MATRIX METALLOPROTEINASE 14; NEUTROPHIL COLLAGENASE; PROCOLLAGEN; PROCOLLAGEN 1; TISSUE INHIBITOR OF METALLOPROTEINASE 1; UNCLASSIFIED DRUG;

ANGIOCARDIOGRAPHY; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTERIAL WALL THICKNESS; ARTICLE; COLLAGEN SYNTHESIS; COMPUTATIONAL FLUID DYNAMICS; CONTROLLED STUDY; CORONARY ARTERY ATHEROSCLEROSIS; DIABETES MELLITUS; ENDOTHELIUM CELL; ENZYME ACTIVITY; FOLLOW UP; HISTOPATHOLOGY; HYPERCHOLESTEROLEMIA; IN VIVO STUDY; INTRAVASCULAR ULTRASOUND; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SHEAR STRESS; SMOOTH MUSCLE FIBER;

ATHEROSCLEROSIS; COLLAGEN; ENDOTHELIAL SHEAR STRESS; METALLOPROTEINASES; NATURAL HISTORY;

ANIMALS; COLLAGEN TYPE I; CORONARY ANGIOGRAPHY; CORONARY ARTERY DISEASE; CORONARY CIRCULATION; CORONARY VESSELS; DIABETES MELLITUS, EXPERIMENTAL; DISEASE PROGRESSION; ENDOTHELIUM, VASCULAR; HYPERCHOLESTEROLEMIA; MALE; MATRIX METALLOPROTEINASES; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; NEOINTIMA; PHENOTYPE; PLAQUE, ATHEROSCLEROTIC; PROCOLLAGEN; RUPTURE, SPONTANEOUS; STRESS, MECHANICAL; SWINE; TIME FACTORS; ULTRASONOGRAPHY, INTERVENTIONAL;

EID: 84879069306     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.112.300827     Document Type: Article

References (42)

1. Stone GW, Maehara A, Lansky AJ, de Bruyne B, Cristea E, Mintz GS, Mehran R, McPherson J, Farhat N, Marso SP, Parise H, Templin B, White R, Zhang Z, Serruys PW; PROSPECT Investigators. A prospective natural-history study of coronary atherosclerosis. N Engl J Med. 2011;364:226-235.
2. Virmani R, Kolodgie FD, Burke AP, Farb A, Schwartz SM. Lessons from sudden coronary death: a comprehensive morphological classification scheme for atherosclerotic lesions. Arterioscler Thromb Vasc Biol. 2000;20:1262-1275.
3. Libby P. Molecular bases of the acute coronary syndromes. Circulation. 1995;91:2844-2850.
4. Stone PH, Saito S, Takahashi S, et al PREDICTION Investigators. Prediction of progression of coronary artery disease and clinical outcomes using vascular profiling of endothelial shear stress and arterial plaque characteristics: the PREDICTION Study. Circulation. 2012;126:172-181.
5. Stone PH, Coskun AU, Kinlay S, Clark ME, Sonka M, Wahle A, Ilegbusi OJ, Yeghiazarians Y, Popma JJ, Orav J, Kuntz RE, Feldman CL. Effect of endothelial shear stress on the progression of coronary artery disease, vascular remodeling, and in-stent restenosis in humans: in vivo 6-month follow-up study. Circulation. 2003;108:438-444.
6. Chatzizisis YS, Coskun AU, Jonas M, Edelman ER, Feldman CL, Stone PH. Role of endothelial shear stress in the natural history of coronary atherosclerosis and vascular remodeling: molecular, cellular, and vascular behavior. J Am Coll Cardiol. 2007;49:2379-2393.
7. Samady H, Eshtehardi P, McDaniel MC, Suo J, Dhawan SS, Maynard C, Timmins LH, Quyyumi AA, Giddens DP. Coronary artery wall shear stress is associated with progression and transformation of atherosclerotic plaque and arterial remodeling in patients with coronary artery disease. Circulation. 2011;124:779-788.
8. Koskinas KC, Chatzizisis YS, Antoniadis AP, Giannoglou GD. Role of endothelial shear stress in stent restenosis and thrombosis: pathophysiologic mechanisms and implications for clinical translation. J Am Coll Cardiol. 2012;59:1337-1349.
9. Koskinas KC, Feldman CL, Chatzizisis YS, Coskun AU, Jonas M, Maynard C, Baker AB, Papafaklis MI, Edelman ER, Stone PH. Natural history of experimental coronary atherosclerosis and vascular remodeling in relation to endothelial shear stress: a serial, in vivo intravascular ultrasound study. Circulation. 2010;121:2092-2101.
10. Chatzizisis YS, Jonas M, Coskun AU, Beigel R, Stone BV, Maynard C, Gerrity RG, Daley W, Rogers C, Edelman ER, Feldman CL, Stone PH. Prediction of the localization of high-risk coronary atherosclerotic plaques on the basis of low endothelial shear stress: an intravascular ultrasound and histopathology natural history study. Circulation. 2008;117:993-1002.
11. Gimbrone MA Jr., Nagel T, Topper JN. Biomechanical activation: an emerging paradigm in endothelial adhesion biology. J Clin Invest. 1997;100:S61-S65.
12. Zhou YQ, Zhu SN, Foster FS, Cybulsky MI, Henkelman RM. Aortic regurgitation dramatically alters the distribution of atherosclerotic lesions and enhances atherogenesis in mice. Arterioscler Thromb Vasc Biol. 2010;30:1181-1188.
13. Parmar KM, Larman HB, Dai G, Zhang Y, Wang ET, Moorthy SN, Kratz JR, Lin Z, Jain MK, Gimbrone MA Jr., García-Cardeña G. Integration of flow-dependent endothelial phenotypes by Kruppel-like factor 2. J Clin Invest. 2006;116:49-58.
14. Libby P. The molecular mechanisms of the thrombotic complications of atherosclerosis. J Intern Med. 2008;263:517-527.
15. Fukumoto Y, Deguchi JO, Libby P, Rabkin-Aikawa E, Sakata Y, Chin MT, Hill CC, Lawler PR, Varo N, Schoen FJ, Krane SM, Aikawa M. Genetically determined resistance to collagenase action augments interstitial collagen accumulation in atherosclerotic plaques. Circulation. 2004;110:1953-1959.
16. Deguchi JO, Aikawa E, Libby P, Vachon JR, Inada M, Krane SM, Whittaker P, Aikawa M. Matrix metalloproteinase-13/collagenase-3 deletion promotes collagen accumulation and organization in mouse atherosclerotic plaques. Circulation. 2005;112:2708-2715.
17. Schneider F, Sukhova GK, Aikawa M, Canner J, Gerdes N, Tang SM, Shi GP, Apte SS, Libby P. Matrix-metalloproteinase-14 deficiency in bonemarrow-derived cells promotes collagen accumulation in mouse atherosclerotic plaques. Circulation. 2008;117:931-939.
18. Gambillara V, Montorzi G, Haziza-Pigeon C, Stergiopulos N, Silacci P. Arterial wall response to ex vivo exposure to oscillatory shear stress. J Vasc Res. 2005;42:535-544.
19. Cheng C, Tempel D, van Haperen R, van der Baan A, Grosveld F, Daemen MJ, Krams R, de Crom R. Atherosclerotic lesion size and vulnerability are determined by patterns of fluid shear stress. Circulation. 2006;113:2744-2753.
20. Kubo T, Maehara A, Mintz GS, et al. The dynamic nature of coronary artery lesion morphology assessed by serial virtual histology intravascular ultrasound tissue characterization. J Am Coll Cardiol. 2010;55:1590-1597.
21. Chatzizisis YS, Baker AB, Sukhova GK, Koskinas KC, Papafaklis MI, Beigel R, Jonas M, Coskun AU, Stone BV, Maynard C, Shi GP, Libby P, Feldman CL, Edelman ER, Stone PH. Augmented expression and activity of extracellular matrix-degrading enzymes in regions of low endothelial shear stress colocalize with coronary atheromata with thin fibrous caps in pigs. Circulation. 2011;123:621-630.
22. Doran AC, Meller N, McNamara CA. Role of smooth muscle cells in the initiation and early progression of atherosclerosis. Arterioscler Thromb Vasc Biol. 2008;28:812-819.
23. Hao H, Gabbiani G, Camenzind E, Bacchetta M, Virmani R, Bochaton-Piallat ML. Phenotypic modulation of intima and media smooth muscle cells in fatal cases of coronary artery lesion. Arterioscler Thromb Vasc Biol. 2006;26:326-332.
24. Hastings NE, Simmers MB, McDonald OG, Wamhoff BR, Blackman BR. Atherosclerosis-prone hemodynamics differentially regulates endothelial and smooth muscle cell phenotypes and promotes pro-inflammatory priming. Am J Physiol Cell Physiol. 2007;293:C1824-C1833.
25. Qi YX, Qu MJ, Long DK, Liu B, Yao QP, Chien S, Jiang ZL. Rho-GDP dissociation inhibitor alpha downregulated by low shear stress promotes vascular smooth muscle cell migration and apoptosis: a proteomic analysis. Cardiovasc Res. 2008;80:114-122.
26. Gerrity RG, Natarajan R, Nadler JL, Kimsey T. Diabetes-induced accelerated atherosclerosis in swine. Diabetes. 2001;50:1654-1665.
27. Cheng GC, Loree HM, Kamm RD, Fishbein MC, Lee RT. Distribution of circumferential stress in ruptured and stable atherosclerotic lesions. A structural analysis with histopathological correlation. Circulation. 1993;87:1179-1187.
28. von Birgelen C, Klinkhart W, Mintz GS, Papatheodorou A, Herrmann J, Baumgart D, Haude M, Wieneke H, Ge J, Erbel R. Plaque distribution and vascular remodeling of ruptured and nonruptured coronary plaques in the same vessel: an intravascular ultrasound study in vivo. J Am Coll Cardiol. 2001;37:1864-1870.
29. Christen T, Verin V, Bochaton-Piallat M, Popowski Y, Ramaekers F, Debruyne P, Camenzind E, van Eys G, Gabbiani G. Mechanisms of neointima formation and remodeling in the porcine coronary artery. Circulation. 2001;103:882-888.
30. Owens GK, Kumar MS, Wamhoff BR. Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol Rev. 2004;84:767-801.
31. Verhamme P, Quarck R, Hao H, Knaapen M, Dymarkowski S, Bernar H, Van Cleemput J, Janssens S, Vermylen J, Gabbiani G, Kockx M, Holvoet P. Dietary cholesterol withdrawal reduces vascular inflammation and induces coronary plaque stabilization in miniature pigs. Cardiovasc Res. 2002;56:135-144.
32. Gijsen FJ, Mastik F, Schaar JA, Schuurbiers JC, van der Giessen WJ, de Feyter PJ, Serruys PW, van der Steen AF, Wentzel JJ. High shear stress induces a strain increase in human coronary plaques over a 6-month period. EuroIntervention. 2011;7:121-127.
33. Papafaklis MI, Takahashi S, Antoniadis A, Coskun AU, Tsuda M, Orita Y, et al. Endothelial shear stress magnitude and circumferential heterogeneity predict the localization of eccentric coronary atherosclerotic plaques in humans (abstr). Circulation. 2012;126:A17559.
34. Koskinas KC, Chatzizisis YS, Papafaklis MI, et al. Incremental effect of hypercholesterolemia on coronary plaque progression and high-risk composition despite similarly low local endothelial shear stress (abstr). Eur Heart J 2012;33:273.
35. Aikawa M, Sivam PN, Kuro-o M, Kimura K, Nakahara K, Takewaki S, Ueda M, Yamaguchi H, Yazaki Y, Periasamy M. Human smooth muscle myosin heavy chain isoforms as molecular markers for vascular development and atherosclerosis. Circ Res. 1993;73:1000-1012.
36. Aikawa M, Rabkin E, Voglic SJ, Shing H, Nagai R, Schoen FJ, Libby P. Lipid lowering promotes accumulation of mature smooth muscle cells expressing smooth muscle myosin heavy chain isoforms in rabbit atheroma. Circ Res. 1998;83:1015-1026.
37. Geng YJ, Libby P. Evidence for apoptosis in advanced human atheroma. Colocalization with interleukin-1 beta-converting enzyme. Am J Pathol. 1995;147:251-266.
38. Clarke MC, Figg N, Maguire JJ, Davenport AP, Goddard M, Littlewood TD, Bennett MR. Apoptosis of vascular smooth muscle cells induces features of plaque vulnerability in atherosclerosis. Nat Med. 2006;12:1075-1080.
39. Thomas JA, Deaton RA, Hastings NE, Shang Y, Moehle CW, Eriksson U, Topouzis S, Wamhoff BR, Blackman BR, Owens GK. PDGF-DD, a novel mediator of smooth muscle cell phenotypic modulation, is upregulated in endothelial cells exposed to atherosclerosis-prone flow patterns. Am J Physiol Heart Circ Physiol. 2009;296:H442-H452.
40. Amento EP, Ehsani N, Palmer H, Libby P. Cytokines and growth factors positively and negatively regulate interstitial collagen gene expression in human vascular smooth muscle cells. Arterioscler Thromb. 1991;11:1223-1230.
41. Herman MP, Sukhova GK, Libby P, Gerdes N, Tang N, Horton DB, Kilbride M, Breitbart RE, Chun M, Schönbeck U. Expression of neutrophil collagenase (matrix metalloproteinase-8) in human atheroma: a novel collagenolytic pathway suggested by transcriptional profiling. Circulation. 2001;104:1899-1904.
42. Aikawa M, Rabkin E, Okada Y, Voglic SJ, Clinton SK, Brinckerhoff CE, Sukhova GK, Libby P. Lipid lowering by diet reduces matrix metalloproteinase activity and increases collagen content of rabbit atheroma: a potential mechanism of lesion stabilization. Circulation. 1998;97:2433-2444.