Suppression of atherosclerotic plaque progression and instability by tissue inhibitor of metalloproteinase-2: Involvement of macrophage migration and apoptosis

Circulation

Volumn 113, Issue 20, 2006, Pages 2435-2444

  Johnson, Jason L ^a   Baker, Andrew H ^b   Oka, Kazuhiro ^c   Chan, Lawrence ^c   Newby, Andrew C ^a   Jackson, Christopher L ^a   George, Sarah J ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b UNIVERSITY OF GLASGOW   (United Kingdom)

^c BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Adenovirus; Atherosclerosis; Gene therapy; Metalloproteinases; Plaque

Indexed keywords

ADENOVIRUS VECTOR; APOLIPOPROTEIN E; MATRIX METALLOPROTEINASE; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TISSUE INHIBITOR OF METALLOPROTEINASE 2; ENZYME INHIBITOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; ATHEROSCLEROTIC PLAQUE; BRACHIOCEPHALIC TRUNK; CELL MIGRATION; CONTROLLED STUDY; DEGRADATION; DISEASE COURSE; DISEASE MARKER; DRUG MECHANISM; EXTRACELLULAR MATRIX; FOAM CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; KNOCKOUT MOUSE; LIPID DIET; MACROPHAGE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SMOOTH MUSCLE FIBER; TECHNOLOGY; TREATMENT OUTCOME; VIRAL GENE DELIVERY SYSTEM; VIRAL GENE THERAPY; ADENOVIRUS; ANIMAL; ATHEROSCLEROSIS; BLOOD; C57BL MOUSE; DISEASE MODEL; GENE VECTOR; GENETICS; MOUSE MUTANT; PATHOPHYSIOLOGY;

ADENOVIRIDAE; ANIMALS; APOLIPOPROTEINS E; ATHEROSCLEROSIS; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; ENZYME INHIBITORS; GENETIC VECTORS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; TISSUE INHIBITOR OF METALLOPROTEINASE-1; TISSUE INHIBITOR OF METALLOPROTEINASE-2;

EID: 33744485260     PISSN: 00097322     EISSN: None     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.106.613281     Document Type: Article

References (41)

1. Ross R. Mechanisms of disease: atherosclerosis - an inflammatory disease. N Engl J Med. 1999;340:115-126.
2. Davies M, Richardson P, Woolf N, Katz D, Mann J. Risk of thrombosis in human atherosclerotic plaques: role of extracellular lipid, macrophage, and smooth muscle cell content. Br Heart J. 1993;69:377-381.
3. Newby AC. Dual role of matrix metalloproteinases (matrixins) in neointima formation and atherosclerotic plaque rupture. Physiol Rev. 2005;85:1-31.
4. Silence J, Lupu F, Collen D, Lijnen HR. Persistence of atherosclerotic plaque but reduced aneurysm formation in mice with stromelysin-1 (MMP-3) gene inactivation. Arterioscler Thromb Vasc Biol. 2001;21:1440-1445.
5. Lemaître V, O'Byrne TK, Borczuk AC, Okada Y, Tall AR, D'Armiento J. ApoE knockout mice expressing human matrix metalloproteinase-1 in macrophages have less advanced atherosclerosis. J Clin Invest. 2001;107:1227-1234.
6. Galis ZS, Sukhova GK, Lark MW, Libby P. Increased expression of matrix metalloproteinases and matrix degrading activity in vulnerable regions of human atherosclerotic plaques. J Clin Invest. 1994;94:2493-2503.
7. Fabunmi RP, Sukhova GK, Sugiyama S, Libby P. Expression of tissue inhibitor of metalloproteinases-3 in human atheroma and regulation in lesion-associated cells. Circ Res. 1998;83:270-278.
8. Galis ZS, Sukhova GK, Libby P. Microscopic localisation of active proteases by in situ zymography: detection of matrix metalloproteinase activity in vascular tissue. FASEB J. 1995;9:974-980.
9. Johnson JL, Jackson CL, Angelini GD, George SJ. Activation of matrix-degrading metalloproteinases by mast cell proteases in atherosclerotic plaques. Arterioscler Thromb Vasc Biol. 1998;18:1707-1715.
10. George SJ, Johnson JL, Angelini GD, Newby AC, Baker AH. Adenovirus-mediated gene transfer of the human TIMP-1 gene inhibits SMC migration and neointima formation in human saphenous vein. Hum Gene Ther. 1998;9:867-877.
11. George SJ, Baker AH, Angelini GD, Newby AC. Gene transfer of tissue inhibitor of metalloproteinase-2 inhibits metalloproteinase activity and neointima formation in human saphenous veins. Gene Ther. 1998;5:1552-1560.
12. Forough R, Hasenstab D, Zempo N, Langley K, De Clerck Y, Clowes A. Induction of tissue inhibitor of metalloproteinase-2 in injured rat artery. In: Greenwald RA, Golub LM, eds. Inhibition of Matrix Metalloproteinases: Therapeutic Potential. New York: N Y Academy of Sciences; 1994:384-388.
13. Dollery CM, Humphries SE, McClelland A, Latchman DS, McEwan JR. Expression of tissue inhibitor of matrix metalloproteinases 1 by use of an adenoviral vector inhibits smooth muscle cell migration and reduces neointimal hyperplasia in the rat model of vascular balloon injury. Circulation. 1999;99:3199-3205.
14. Cheng L, Mantile G, Pauly R, Nater C, Felici A, Monticone R, Bilato C, Gluzband YA, Crow MT, Stetler-Stevenson W, Capogrossi MC. Adenovirus-mediated gene transfer of the human tissue inhibitor of metalloproteinase-2 blocks vascular smooth muscle cell invasiveness in vitro and modulates neointimal development in vivo. Circulation. 1998;98:2195-2201.
15. Furman C, Luo Z, Walsh K, Duverger N, Copin C, Fruchart JC, Rouis M. Systemic tissue inhibitor of metalloproteinase-1 gene delivery reduces neointimal hyperplasia in balloon-injured rat carotid artery. FEBS Lett. 2002;531:122-126.
16. Rouis M, Adamy C, Duverger N, Lesnik P, Horellou P, Moreau M, Emmanuel F, Caillaud JM, Laplaud PM, Dachet C, Chapman MJ. Adenovirus-mediated overexpression of tissue inhibitor of metalloproteinase-1 reduces atherosclerotic lesions in apolipoprotein E-deficient mice. Circulation. 1999;100:533-540.
17. Johnson JL, Jackson CL. Atherosclerotic plaque rupture in the apolipoprotein E knockout mouse. Atherosclerosis. 2001;154:399-406.
18. Williams H, Johnson JL, Carson KGS, Jackson CL. Characteristics of intact and raptured atherosclerotic plaques in brachiocephalic arteries of apolipoprotein E knockout mice. Arterioscler Thromb Vasc Biol. 2002; 22:788-792.
19. Johnson J, Carson K, Williams H, Karanam S, Newby A, Angelini G, George S, Jackson C. Plaque rapture after short periods of fat-feeding in the apolipoprotein E knockout mouse: model characterization and effects of pravastatin treatment. Circulation. 2005;111:1422-1430.
20. Burke AP, Kolodgie FD, Farb A, Weber DK, Malcom GT, Smialek J, Virmani R. Healed plaque raptures and sudden coronary death: evidence that subclinical rapture has a role in plaque progression. Circulation. 2001;103:934-940.
21. Baker AH, Wilkinson GWG, Hembry RM, Murphy G, Newby AC. Development of recombinant adenoviruses that drive high level expression of the human metalloproteinase-9 and tissue inhibitor of metalloproteinase-1 and -2 genes: characterization of their infection into rabbit smooth muscle cells and human MCF-7 adenocarcinoma cells. Matrix Biol. 1996;15:383-395.
22. Baker AH, Zaltsman AB, George SJ, Newby AC. Divergent effects of tissue inhibitor of metalloproteinase-1, -2, or -3 overexpression on rat vascular smooth muscle cell invasion, proliferation, and death in vitro. J Clin Invest. 1998;101:1478-1487.
23. Tao NJ, Gao GP, Parr M, Johnston J, Baradet T, Wilson JM, Barsoum J, Fawell SE. Sequestration of adenoviral vector by Kupffer cells leads to a nonlinear dose response of transduction in liver. Mol Ther. 2001;3:28-35.
24. Oh LY, Larsen PH, Krekoski CA, Edwards DR, Donovan F, Werb Z, Yong VW. Matrix metalloproteinase-9/gelatinase B is required for process outgrowth by oligodendrocytes. J Neurosci. 1999;19:8464-8475.
25. Magnoni S, Baker A, George SJ, Duncan WC, Kerr LE, McCulloch J, Horsburgh K. Differential alterations in the expression and activity of matrix metalloproteinases 2 and 9 after transient cerebral ischemia in mice. Neurobiol Dis. 2004;17:188-197.
26. Oka K, Pastore L, Kin IH, Merched A, Nomura S, Lee HJ, Merched-Sauvage M, Arden-Riley C, Lee B, Finegold M, Beaudet A, Chan L. Long-term stable correction of low-density lipoprotein receptor-deficient mice with a helper-dependent adenoviral vector expressing the very low-density lipoprotein receptor. Circulation. 2001;103:1274-1281.
27. Apparailly F, Noel D, Millet V, Baker AH, Lisignoli G, Jacquet C, Kaiser M-J, Sany J, Jorgensen C. Paradoxical effects of tissue inhibitor of metalloproteinases 1 gene transfer in collagen-induced arthritis. Arth Rheum. 2001;44:1444-1454.
28. Belalcazar LM, Merched A, Carr B, Oka K, Chen K-H, Pastore L, Beaudet A, Chan L. Long-term stable expression of human apolipoprotein A-I mediated by helper-dependent adenoviras gene transfer inhibits atherosclerosis progression and remodels atherosclerotic plaques in a mouse model of familial hypercholesterolemia. Circulation. 2003;107:2726-2732.
29. Wesley RB II, Meng X, Godin D, Galis ZS. Extracellular matrix modulates macrophage functions characteristic to atheroma: collagen type 1 enhances acquisition of resident macrophage traits by human peripheral blood monocytes in vitro. Arterioscler Thromb Vasc Biol. 1998;18:432-440.
30. Shipley JM, Wesselschmidt RL, Kobayashi DK, Ley TJ, Shapiro SD. Metalloelastase is required for macrophage-mediated proteolysis and matrix invasion in mice. Proc Natl Acad Sci U S A. 1996;93:3942-3946.
31. Matias-Roman S, Galvez BG, Genis L, Yanez-Mo M, de la Rosa G, Sanchez-Mateos P, Sanchez-Madrid F, Arroyo AG. Membrane type 1-matrix metalloproteinase is involved in migration of human monocytes and is regulated through their interaction with fibronectin or endothelium. Blood. 2005;105:3956-3964.
32. Schrijvers DM, De Meyer GRY, Kockx MM, Herman AG, Martinet W. Phagocytosis of apoptotic cells by macrophages is impaired in atherosclerosis. Arterioscler Thromb Vasc Biol. 2005;25:1256-1261.
33. Kockx MM, Herman AG. Apoptosis in atherosclerosis: beneficial or detrimental? Cardiovasc Res. 2000;45:736-746.
34. -/- mice after adenovirus-mediated transfer of p53. Circulation. 2002;105:2064-2070.
35. Zadelaar ASM, von der Thüsen JH, Boesten LSM, Hoeben RC, Kockx MM, Versnel MA, van Berkel TJC, Havekes LM, Biessen EAL, van Vlijmen BJM. Increased vulnerability of pre-existing atherosclerosis in ApoE-deficient mice following adenovirus-mediated Fas ligand gene transfer. Atherosclerosis. 2005;183:244-250.
36. Bowen-Pope DF, Schaub FJ. Apoptosis of smooth muscle cells is not silent: Fas/FADD initiates a program of inflammatory gene expression. Trends Cardiovasc Med. 2001;11:42-45.
37. Seo D-W, Li H, Guedez L, Wingfield PT, Diaz T, Salloum R, Wei B-Y, Stetler-Stevenson G. TIMP-2 mediated inhibition of angiogenesis: an MMP-independent mechanism. Cell. 2003;q114:171-180.
38. Rosenfeld ME, Polinsky P, Virmani R, Kauser K, Rubanyi G, Schwartz SM. Advanced atherosclerotic lesions in the innominate artery of the ApoE knockout mouse. Arterioscler Thromb Vasc Biol. 2000;20:2587-2592.
39. VanderLaan PA, Reardon CA, Getz GS. Site specificity of atherosclerosis. Arterioscler Thromb Vasc Biol. 2004;24:12-22.
40. Baker AH, Edwards DR, Murphy G. Metalloproteinase inhibitors: biological actions and therapeutic opportunities. J Cell Sci. 2002;115:3719-3727.
41. Howard EW, Bullen EC, Banda MJ. Preferential inhibition of 72- and 92-kDa gelatinases by tissue inhibitor of metalloproteinases-2. J Biol Chem. 1991;266:13070-13075.