Fibroblast activation protein is induced by inflammation and degrades type i collagen in thin-cap fibroatheromata

European Heart Journal

Volumn 32, Issue 21, 2011, Pages 2713-2722

  Brokopp, Chad E ^a,b   Schoenauer, Roman ^b   Richards, Peter ^a   Bauer, Stefan ^c   Lohmann, Christine ^a,b   Emmert, Maximilian Y ^b   Weber, Benedikt ^a,b   Winnik, Stephan ^a,b   Aikawa, Elena ^d   Graves, Kirk ^e   Genoni, Michele ^e   Vogt, Peter ^b   Lscher, Thomas F ^a,b   Renner, Christoph ^b   Hoerstrup, Simon P ^a,b   Matter, Christian M ^a,b  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^c GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^d BRIGHAM AND WOMEN S HOSPITAL   (United States)

^e TRIEMLI HOSPITAL   (Switzerland)

Author keywords

Antibodies; Atherosclerosis; Collagen; Inflammation; Smooth muscle cells

Indexed keywords

ANTIBODY; COLLAGEN TYPE 1; FIBROBLAST ACTIVATION PROTEIN; GELATIN; PROTEIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

AORTA; AORTA ATHEROSCLEROSIS; AORTA DISEASE; AORTIC SMOOTH MUSCLE CELL; ARTICLE; ATHEROSCLEROTIC PLAQUE; CELL CULTURE; COLLAGEN DEGRADATION; CONTROLLED STUDY; DISEASE ASSOCIATION; ENZYME ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; FIBROBLAST; FLOW CYTOMETRY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; INFLAMMATION; MACROPHAGE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SMOOTH MUSCLE FIBER; STAINING; THIN CAP FIBROATHEROMATA; UPREGULATION; ZYMOGRAPHY;

ADULT; AGED; ANALYSIS OF VARIANCE; AORTIC DISEASES; CELLS, CULTURED; COLLAGEN TYPE I; COLLAGENASES; CORONARY ARTERY DISEASE; ENDOTHELIAL CELLS; GELATINASES; HUMANS; MEMBRANE PROTEINS; MIDDLE AGED; MUSCLE, SMOOTH, VASCULAR; PLAQUE, ATHEROSCLEROTIC; SERINE ENDOPEPTIDASES; TUMOR NECROSIS FACTOR-ALPHA;

EID: 80755172656     PISSN: 0195668X     EISSN: 15229645     Source Type: Journal    
DOI: 10.1093/eurheartj/ehq519     Document Type: Article

References (34)

1. Farb A, Burke AP, Tang AL, Liang Y, Mannan P, Smialek J, Virmani R. Coronary plaque erosion without rupture into a lipid core: a frequent cause of coronary thrombosis in sudden coronary death. Circulation 1996;93:1354-1363. (Pubitemid 26099346)
2. Virmani R, Burke AP, Farb A, Kolodgie FD. Pathology of the vulnerable plaque. J Am Coll Cardiol 2006;47:C13-C18.
3. Van Der Wal A, Becker A, Van Der Loos C, Das P. Site of intimal rupture or erosion of thrombosed coronary atherosclerotic plaques is characterized by an inflammatory process irrespective of the dominant plaque morphology. Circulation 1994;89:36-44. (Pubitemid 24026469)
4. Shah P, Falk E, Badimon J, Fernandez-Ortiz A, Mailhac A, Villareal-Levy G, Fallon J, Regnstrom J, Fuster V. Human monocyte-derived macrophages induce collagen breakdown in fibrous caps of atherosclerotic plaques. Potential role of matrixdegrading metalloproteinases and implications for plaque rupture. Circulation 1995;92:1565-1569.
5. Rajavashisth TB, Xu X-P, Jovinge S, Meisel S, Xu X-O, Chai N-N, Fishbein MC, Kaul S, Cercek B, Sharifi B, Shah PK. Membrane type 1 matrix metalloproteinase expression in human atherosclerotic plaques. Circulation 1999;99:3103-3109.
6. Crisby M, Nordin-Fredriksson G, Shah PK, Yano J, Zhu J, Nilsson J. Pravastatin treatment increases collagen content and decreases lipid content, inflammation, metalloproteinases, and cell death in human carotid plaques: implications for plaque stabilization. Circulation 2001;103:926-933. (Pubitemid 32183796)
7. Herman MP, Sukhova GK, Libby P, Gerdes N, Tang N, Horton DB, Kilbride M, Breitbart RE, Chun M, Schonbeck U. Expression of neutrophil collagenase (matrix metalloproteinase-8) in human atheroma: a novel collagenolytic pathway suggested by transcriptional profiling. Circulation 2001;104:1899-1904. (Pubitemid 32983231)
8. Aikawa E, Nahrendorf M, Figueiredo J-L, Swirski FK, Shtatland T, Kohler RH, Jaffer FA, Aikawa M, Weissleder R. Osteogenesis associates with inflammation in early-stage atherosclerosis evaluated by molecular imaging in vivo. Circulation 2007;116:2841-2850. (Pubitemid 350301146)
9. Jaffer FA, Kim D-E, Quinti L, Tung C-H, Aikawa E, Pande AN, Kohler RH, Shi G-P, Libby P,Weissleder R. Optical visualization of cathepsin k activity in atherosclerosis with a novel, protease-activatable fluorescence sensor. Circulation 2007;115: 2292-2298. (Pubitemid 46685897)
10. Schafers M, Riemann B, Kopka K, Breyholz H-J, Wagner S, Schafers KP, Law MP, Schober O, Levkau B. Scintigraphic imaging of matrix metalloproteinase activity in the arterial wall in vivo. Circulation 2004;109:2554-2559. (Pubitemid 38720556)
11. Deguchi J-O, Aikawa M, Tung C-H, Aikawa E, Kim D-E, Ntziachristos V, Weissleder R, Libby P. Inflammation in atherosclerosis: visualizing matrix metalloproteinase action in macrophages in vivo. Circulation 2006;114:55-62. (Pubitemid 44305275)
12. Herman MP, Sukhova GK, Kisiel W, Foster D, Kehry MR, Libby P, Schönbeck U. Tissue factor pathway inhibitor-2 is a novel inhibitor of matrix metalloproteinases with implications for atherosclerosis. J Clin Invest 2001;107:1117-1126. (Pubitemid 32422908)
13. Sukhova GK, Shi GP, Simon DI, Chapman HA, Libby P. Expression of the elastolytic cathepsins s and k in human atheroma and regulation of their production in smooth muscle cells. J Clin Invest 1998;102:576-583. (Pubitemid 28376160)
14. Kong Y-Z, Yu X, Tang J-J, Ouyang X, Huang X-R, Fingerle-Rowson G, Bacher M, Scher LA, Bucala R, Lan HY. Macrophage migration inhibitory factor induces mmp-9 expression: implications for destabilization of human atherosclerotic plaques. Atherosclerosis 2005;178:207-215. (Pubitemid 39600835)
15. Bauer S, Jendro M, Wadle A, Kleber S, Stenner F, Dinser R, Reich A, Faccin E, Godde S, Dinges H, Muller-Ladner U, Renner C. Fibroblast activation protein is expressed by rheumatoid myofibroblast-like synoviocytes. Arthritis Res Ther 2006;8:R171.
16. Edosada CY, Quan C, Wiesmann C, Tran T, Sutherlin D, Reynolds M, Elliott JM, Raab H, Fairbrother W, Wolf BB. Selective inhibition of fibroblast activation protein protease based on dipeptide substrate specificity. J Biol Chem 2006;281: 7437-7444. (Pubitemid 43847515)
17. Park JE, Lenter MC, Zimmermann RN, Garin-Chesa P, Old LJ, Rettig WJ. Fibroblast activation protein, a dual specificity serine protease expressed in reactive human tumor stromal fibroblasts. J Biol Chem 1999;274:36505-36512.
18. Levy MT, McCaughan GW, Abbott CA, Park JE, Cunningham AM, Müller E, Rettig WJ, Gorrell MD. Fibroblast activation protein: a cell surface dipeptidyl peptidase and gelatinase expressed by stellate cells at the tissue remodelling interface in human cirrhosis. Hepatology 1999;29:1768-1778. (Pubitemid 29247051)
19. Aertgeerts K, Levin I, Shi L, Snell GP, Jennings A, Prasad GS, Zhang Y, Kraus ML, Salakian S, Sridhar V, Wijnands R, Tennant MG. Structural and kinetic analysis of the substrate specificity of human fibroblast activation protein a. J Biol Chem 2005; 280:19441-19444. (Pubitemid 41379462)
20. Stary HC, Chandler AB, Dinsmore RE, Fuster V, Glagov S, Insull W Jr, Rosenfeld ME, Schwartz CJ, Wagner WD, Wissler RW. A definition of advanced types of atherosclerotic lesions and a histological classification of atherosclerosis: a report from the Committee on Vascular Lesions of the Council on Arteriosclerosis, American Heart Association. Circulation 1995;92:1355-1374.
21. Stary HC, Chandler AB, Dinsmore RE, Fuster V, Glagov S, Insull W Jr, Rosenfeld ME, Schwartz CJ, Wagner WD, Wissler RW. A definition of advanced types of atherosclerotic lesions and a histological classification of atherosclerosis: a report from the Committee on Vascular Lesions of the Council on Arteriosclerosis, American Heart Association. Arterioscler Thromb Vasc Biol 1995;15: 1512-1531.
22. Hansson GK. Inflammation, atherosclerosis, and coronary artery disease. N Engl J Med 2005;352:1685-1695.
23. Galis ZS, Khatri JJ. Matrix metalloproteinases in vascular remodeling and atherogenesis: the good, the bad, and the ugly. Circ Res 2002;90:251-262. (Pubitemid 34633925)
24. Newby AC. Dual role of matrix metalloproteinases (matrixins) in intimal thickening and atherosclerotic plaque rupture. Physiol Rev 2005;85:1-31. (Pubitemid 40171256)
25. Sluijter JPG, Pulskens WPC, Schoneveld AH, Velema E, Strijder CF, Moll F, de Vries J-P, Verheijen J, Hanemaaijer R, de Kleijn DPV, Pasterkamp G. Matrix metalloproteinase 2 is associated with stable and matrix metalloproteinases 8 and 9 with vulnerable carotid atherosclerotic lesions: a study in human endarterectomy specimen pointing to a role for different extracellular matrix metalloproteinase inducer glycosylation forms. Stroke 2006;37:235-239. (Pubitemid 43732079)
26. Sukhova GK, Schonbeck U, Rabkin E, Schoen FJ, Poole AR, Billinghurst RC, Libby P. Evidence for increased collagenolysis by interstitial collagenases-1 and-3 in vulnerable human atheromatous plaques. Circulation 1999;99:2503-2509. (Pubitemid 29228279)
27. Lutgens SPM, Cleutjens KBJM, Daemen MJAP, Heeneman S. Cathepsin cysteine proteases in cardiovascular disease. FASEB J 2007;21:3029-3041. (Pubitemid 47565524)
28. Burke AP, Farb A, Malcom GT, Liang Y-H, Smialek J, Virmani R. Coronary risk factors and plaque morphology in men with coronary disease who died suddenly. N Engl J Med 1997;336:1276-1282. (Pubitemid 27187780)
29. Brown DL, Hibbs MS, Kearney M, Loushin C, Isner JM. Identification of 92-kd gelatinase in human coronary atherosclerotic lesions: association of active enzyme synthesis with unstable angina. Circulation 1995;91:2125-2131.
30. Aikawa M, Rabkin E, Sugiyama S, Voglic SJ, Fukumoto Y, Furukawa Y, Shiomi M, Schoen FJ, Libby P. An HMG-CoA reductase inhibitor, cerivastatin, suppresses growth of macrophages expressing matrix metalloproteinases and tissue factor in vivo and in vitro. Circulation 2001;103:276-283. (Pubitemid 32095415)
31. Spagnoli LG, Bonanno E, Mauriello A, Palmieri G, Partenzi A, Sangiorgi G, Crea F. Multicentric inflammation in epicardial coronary arteries of patients dying of acute myocardial infarction. J Am Coll Cardiol 2002;40:1579-1588. (Pubitemid 35253635)
32. Szmitko PE, Wang C-H, Weisel RD, de Almeida JR, Anderson TJ, Verma S. New markers of inflammation and endothelial cell activation: Part i. Circulation 2003; 108:1917-1923. (Pubitemid 37296533)
33. Skinner MP, Raines EW, Ross R. Dynamic expression of alpha 1 beta 1 and alpha 2 beta 1 integrin receptors by human vascular smooth muscle cells. Alpha 2 beta 1 integrin is required for chemotaxis across type i collagen-coated membranes. Am J Pathol 1994;1:1070-1081.
34. Matter CM, Stuber M, Nahrendorf M. Imaging of the unstable plaque: how far have we got? Eur Heart J 2009;30:2566-2574.