Metalloproteinases promote plaque rupture and myocardial infarction: A persuasive concept waiting for clinical translation

Matrix Biology

Volumn 44-46, Issue , 2015, Pages 157-166

  Newby, Andrew C ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

Atherosclerosis; Cardiovascular disease; Inflammation; Macrophages; Stroke; Vascular smooth muscle

Indexed keywords

COLLAGENASE 3; GELATINASE A; GELATINASE B; INTERSTITIAL COLLAGENASE; MACROPHAGE ELASTASE; MATRILYSIN; MATRIX METALLOPROTEINASE; MATRIX METALLOPROTEINASE 14; MATRIX METALLOPROTEINASE 19; MATRIX METALLOPROTEINASE 25; NEUTROPHIL COLLAGENASE; STROMELYSIN; STROMELYSIN 2; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TISSUE INHIBITOR OF METALLOPROTEINASE 2; TISSUE INHIBITOR OF METALLOPROTEINASE 3; UNCLASSIFIED DRUG; TISSUE INHIBITOR OF METALLOPROTEINASE;

ATHEROSCLEROTIC PLAQUE; ATHEROSCLEROTIC PLAQUE RUPTURE; CLINICAL FEATURE; DISEASE COURSE; ENZYME ACTIVITY; GENE CONTROL; GENETIC MANIPULATION; HEART INFARCTION; HUMAN; MACROPHAGE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; RUPTURE; ANIMAL; DISEASE MODEL; DRUG EFFECTS; ENZYMOLOGY; METABOLISM; MOLECULARLY TARGETED THERAPY; MYOCARDIAL INFARCTION; PATHOLOGY; PLAQUE, ATHEROSCLEROTIC; TRANSLATIONAL RESEARCH;

ANIMALS; DISEASE MODELS, ANIMAL; HUMANS; MACROPHAGES; MATRIX METALLOPROTEINASES; MOLECULAR TARGETED THERAPY; MYOCARDIAL INFARCTION; PLAQUE, ATHEROSCLEROTIC; TISSUE INHIBITOR OF METALLOPROTEINASES; TRANSLATIONAL MEDICAL RESEARCH;

EID: 84930764170     PISSN: 0945053X     EISSN: 15691802     Source Type: Journal    
DOI: 10.1016/j.matbio.2015.01.015     Document Type: Review

References (83)

1. Galis Z.S., Khatri J.J. Matrix metalloproteinases in vascular remodeling and atherogenesis: the good, the bad, and the ugly. Circ Res 2002, 90:251-262.
2. Newby A.C. Dual role of matrix metalloproteinases (matrixins) in intimal thickening and atherosclerotic plaque rupture. Physiol Rev 2005, 85:1-31.
3. Galis Z.S., Sukhova G.K., Lark M.W., 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.
4. Henney A.M., Wakely P.R., Davies M.J., Foster K., Hembry R., Murphy G., et al. Localization of stromelysin gene expression in atherosclerotic plaques by in situ hybridization. Proc Natl Acad Sci U S A 1991, 88:8154-8158.
5. Libby P. Collagenases and cracks in the plaque. J Clin Invest 2013, 123:3201-3203.
6. Nordon I.M., Hinchliffe R.J., Loftus I.M., Thompson M.M. Pathophysiology and epidemiology of abdominal aortic aneurysms. Nat Rev Cardiol 2011, 8:92-102.
7. Newby A.C. Matrix metalloproteinase inhibition therapy for vascular diseases. Vascul Pharmacol 2012, 56:232-244.
8. Khokha R., Murthy A., Weiss A. Metalloproteinases and their natural inhibitors in inflammation and immunity. Nat Rev Immunol 2013, 13:649-665.
9. Back M., Ketelhuth D.F., Agewall S. Matrix metalloproteinases in atherothrombosis. Prog Cardiovasc Dis 2010, 52:410-428.
10. Ketelhuth D.F., Back M. The role of matrix metalloproteinases in atherothrombosis. Curr Atheroscler Rep 2011, 13:162-169.
11. Roycik M.D., Myers J.S., Newcomer R.G., Sang Q.X. Matrix metalloproteinase inhibition in atherosclerosis and stroke. Curr Mol Med 2013, 13:1299-1313.
12. Clark I.M., Swingler T.E., Sampieri C.L., Edwards D.R. The regulation of matrix metalloproteinases and their inhibitors. Int J Biochem Cell Biol 2008, 40:1362-1378.
13. Newby A.C. Metalloproteinase expression in monocytes and macrophages and its relationship to atherosclerotic plaque instability. Arterioscler Thromb Vasc Biol 2008, 28:2108-2114.
14. Nagase H., Visse R., Murphy G. Structure and function of matrix metalloproteinases and TIMPs. Cardiovasc Res 2006, 69:562-573.
15. Parks W.C., Wilson C.L., Lopez-Boado Y.S. Matrix metalloproteinases as modulators of inflammation and innate immunity. Nat Rev Immunol 2004, 4:617-629.
16. Rodriguez D., Morrison C.J., Overall C.M. Matrix metalloproteinases: what do they not do? New substrates and biological roles identified by murine models and proteomics. Biochim Biophys Acta 1803, 2010:39-54.
17. Matoba T., Sato K., Egashira K. Mouse models of plaque rupture. Curr Opin Lipidol 2013, 24:419-425. 10.1097/MOL.0b013e3283646e4d.
18. Johnson J.L., Carson K., Williams H.M., Karanam S., Newby A.C., Angelini G.D., et al. Plaque rupture after short periods of fat-feeding in the apolipoprotein E-knockout mouse: model characterisation, and effects of pravastatin treatment. Circulation 2005, 111:1422-1430.
19. Falk E., Schwartz S.M., Galis Z.S., Rosenfeld M.E. Putative murine models of plaque rupture. Arterioscler Thromb Vasc Biol 2007, 27:969-972.
20. Huang W.C., Sala-Newby G.B., Susana A., Johnson J.L., Newby A.C. Classical macrophage activation up-regulates several matrix metalloproteinases through mitogen activated protein kinases and nuclear factor-kappaB. PLoS One 2012, 7:e42507.
21. Hayes E.M., Tsaousi A., Di Gregoli K., Jenkinson S.R., Bond A.R., Johnson J.L., et al. Classical and alternative activation and metalloproteinase expression occurs in foam cell macrophages in male and female ApoE null mice in the absence of T- and B-lymphocytes. Front Immunol 2014, 5.
22. Filippov S., Caras I., Murray R., Matrisian L.M., Chapman H.A., Shapiro S., et al. Matrilysin-dependent elastolysis by human macrophages. J Exp Med 2003, 198:925-935.
23. Johnson J.L., Devel L., Czarny B., George S.J., Jackson C.L., Rogakos V., et al. A selective matrix metalloproteinase-12 inhibitor retards atherosclerotic plaque development in apolipoprotein E-knockout mice. Arterioscler Thromb Vasc Biol 2011, 31:528-535.
24. Quillard T., Tesmenitsky Y., Croce K., Travers R., Shvartz E., Koskinas K.C., et al. Selective inhibition of matrix metalloproteinase-13 increases collagen content of established mouse atherosclerosis. Arterioscler Thromb Vasc Biol 2011, 31:2464-2472.
25. Chase A.J., Newby A.C. Regulation of matrix metalloproteinase (matrixin) genes in blood vessels: a multi-step recruitment model for pathological remodelling. J Vasc Res 2003, 40:329-343.
26. Lemaitre V., O'Byrne T.K., Borczuk A.C., Okada Y., Tall A.R., D'Armiento J. ApoE knockout mice expressing human matrix metalloproteinase-1 in macrophages have less advanced atherosclerosis. J Clin Invest 2001, 107:1227-1234.
27. Montero I., Orbe J., Varo N., Beloqui O., Monreal J.I., Rodriguez J.A., et al. C-reactive protein induces matrix metalloproteinase-1 and -10 in human endothelial cells: implications for clinical and subclinical atherosclerosis. J Am Coll Cardiol 2006, 47:1369-1378.
28. Bond M., Chase A.J., Baker A.H., Newby A.C. Inhibition of transcription factor NF-kappaB reduces matrix metalloproteinase-1, -3 and -9 production by vascular smooth muscle cells. Cardiovasc Res 2001, 50:556-565.
29. Sukhova G.K., Schonbeck U., Rabkin E., Schoen F.J., Poole A.R., Billinghurst R.C., et al. Evidence for increased collagenolysis by interstitial collagenases-1 and -3 in vulnerable human atheromatous plaques. Circulation 1999, 99:2503-2509.
30. Peterson J.T. The importance of estimating the therapeutic index in the development of matrix metalloproteinase inhibitors. Cardiovasc Res 2006, 69:677-687.
31. Sluijter J.P., Pulskens W.P., Schoneveld A.H., Velema E., Strijder C.F., Moll F., et al. 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.
32. Johnson J.L., Dwivedi A., Somerville M., George S.J., Newby A.C. Matrix metalloproteinase (MMP)-3 activates MMP-9 mediated vascular smooth muscle cell migration and neointima formation in mice. Arterioscler Thromb Vasc Biol 2011, 31:e35-e44.
33. Alexander M.R., Moehle C.W., Johnson J.L., Yang Z., Lee J.K., Jackson C.L., et al. Genetic inactivation of IL-1 signaling enhances atherosclerotic plaque instability and reduces outward vessel remodeling in advanced atherosclerosis in mice. J Clin Invest 2012, 122:70-79.
34. Chase A., Bond M., Crook M.F., Newby A.C. Role of nuclear factor-kB activation in metalloproteinase-1, -3 and -9 secretion by human macrophages in vitro and rabbit foam cells produced in vivo. Arterioscler Thromb Vasc Biol 2002, 22:765-771.
35. Johnson J.L., George S.J., Newby A.C., Jackson C.L. Divergent effects of matrix metalloproteinases 3, 7, 9, and 12 on atherosclerotic plaque stability in mouse brachiocephalic arteries. Proc Natl Acad Sci U S A 2005, 102:15575-15580.
36. Silence J., Lupu F., Collen D., Lijnen H.R. 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.
37. Monaco C., Gregan S.M., Navin T.J., Foxwell B.M., Davies A.H., Feldmann M. Toll-like receptor-2 mediates inflammation and matrix degradation in human atherosclerosis. Circulation 2009, 120:2462-2469.
38. Williams H., Johnson J.L., Jackson C.L., White S.J., George S.J. MMP-7 mediates cleavage of N-cadherin and promotes smooth muscle cell apoptosis. Cardiovasc Res 2010, 87:137-146.
39. Burke B., Giannoudis A., Corke K.P., Gill D., Wells M., Ziegler-Heitbrock L., et al. Hypoxia-induced gene expression in human macrophages: implications for ischemic tissues and hypoxia-regulated gene therapy. Am J Pathol 2003, 163:1233-1243.
40. Lenglet S., Mach F., Montecucco F. Role of matrix metalloproteinase-8 in atherosclerosis. Mediators Inflamm 2013, 2013:659282.
41. Herman M.P., Sukhova G.K., Libby P., Gerdes N., Tang N., Horton D.B., et al. Expression of neutrophil collagenase (matrix metalloproteinase-8) in human atheroma: a novel collagenolytic pathway suggested by transcriptional profiling. Circulation 2001, 104:1899-1904.
42. Peeters W., Moll F.L., Vink A., van der Spek P.J., de Kleijn D.P., de Vries J.P., et al. Collagenase matrix metalloproteinase-8 expressed in atherosclerotic carotid plaques is associated with systemic cardiovascular outcome. Eur Heart J 2011, 32:2314-2325.
43. Laxton R.C., Hu Y., Duchene J., Zhang F., Zhang Z., Leung K.Y., et al. A role of matrix metalloproteinase-8 in atherosclerosis. Circ Res 2009, 105:921-929.
44. Bond M., Fabunmi R.P., Baker A.H., Newby A.C. Synergistic upregulation of metalloproteinase-9 by growth factors and inflammatory cytokines: an absolute requirement for transcription factor NF-kB. FEBS Lett 1998, 435:29-34.
45. Luttun A., Lutgens E., Manderveld A., Maris K., Collen D., Carmeliet P., et al. Loss of matrix metalloproteinase-9 or matrix metalloproteinase-12 protects apolipoprotein E-deficient mice against atherosclerotic media destruction but differentially affects plaque growth. Circulation 2004, 109:1408-1414.
46. de Nooijer R., Verkleij C.J.N., von der Thusen J.H., Jukema J.W., van der Wall E.E., van Berkel T.J.C., et al. Lesional overexpression of matrix metalloproteinase-9 promotes intraplaque hemorrhage in advanced lesions but not at earlier stages of atherogenesis. Arterioscler Thromb Vasc Biol 2006, 26:340-346.
47. Gough P.J., Gomez I.G., Wille P.T., Raines E.W. Macrophage expression of active MMP-9 induces acute plaque disruption in apoE-deficient mice. J Clin Invest 2006, 116:59-69.
48. Lemaitre V., Kim H.E., Forney-Prescott M., Okada Y., D'Armiento J. Transgenic expression of matrix metalloproteinase-9 modulates collagen deposition in a mouse model of atherosclerosis. Atherosclerosis 2009, 205:107-112.
49. Reel B., Sala-Newby G.B., Huang W.-C., Newby A.C. Diverse patterns of cyclooxygenase-independent metalloproteinase gene regulation in human monocytes. Br J Pharmacol 2011, 163:1679-1690.
50. Shipley J.M., Wesselschmidt R.L., Kobayashi D.K., Ley T.J., Shapiro S.D. Metalloelastase is required for macrophage-mediated proteolysis and matrix invasion in mice. Proc Natl Acad Sci U S A 1996, 93:3942-3946.
51. Dwivedi A., Slater S.C., George S.J. MMP-9 and -12 cause N-cadherin shedding and thereby beta-catenin signalling and vascular smooth muscle cell proliferation. Cardiovasc Res 2009, 81:178-186.
52. Jormsjo S., Ye S., Moritz J., Walter D.H., Dimmeler S., Zeiher A.M., et al. Allele-specific regulation of matrix metalloproteinase-12 gene activity is associated with coronary artery luminal dimensions in diabetic patients with manifest coronary artery disease. Circ Res 2000, 86:998-1003.
53. Shimizu K., Shichiri M., Libby P., Lee R.T., Mitchell R.N. Th2-predominant inflammation and blockade of IFN-gamma signaling induce aneurysms in allografted aortas. J Clin Invest 2004, 114:300-308.
54. Thomas A.C., Sala-Newby G.B., Ismail Y., Johnson J.L., Pasterkamp G., Newby A.C. Genomics of foam cells and nonfoamy macrophages from rabbits identifies arginase-I as a differential regulator of nitric oxide production. Arterioscler Thromb Vasc Biol 2007, 27:571-577.
55. Halpert I., Sires U.I., Roby J.D., PotterPerigo S., Wight T.N., Shapiro S.D., et al. Matrilysin is expressed by lipid-laden macrophages at sites of potential rupture in atherosclerotic lesions and localizes to areas of versican deposition, a proteoglycan substrate for the enzyme. Proc Natl Acad Sci U S A 1996, 93:9748-9753.
56. Scholtes V.P.W., Johnson J.L., Jenkins N., Sala-Newby G.B., de Vries J.-P.P.M., GJd Borst, et al. Carotid atherosclerotic plaque matrix metalloproteinase-12-positive macrophage subpopulation predicts adverse outcome after endarterectomy. J Am Heart Assoc 2012, 1:e001040.
57. Morgan A.R., Rerkasem K., Gallagher P.J., Zhang B., Morris G.E., Calder P.C., et al. Differences in matrix metalloproteinase-1 and matrix metalloproteinase-12 transcript levels among carotid atherosclerotic plaques with different histopathological characteristics. Stroke 2004, 35:1310-1315.
58. Dahl R., Titlestad I., Lindqvist A., Wielders P., Wray H., Wang M., et al. Effects of an oral MMP-9 and -12 inhibitor, AZD1236, on biomarkers in moderate/severe COPD: a randomised controlled trial. Pulm Pharmacol Ther 2012, 25:169-177.
59. Lenglet S., Thomas A., Chaurand P., Galan K., Mach F., Montecucco F. Molecular imaging of matrix metalloproteinases in atherosclerotic plaques. Thromb Haemost 2012, 107:409-416.
60. Deguchi J.-O., Aikawa E., Libby P., Vachon J.R., Inada M., Krane S.M., et al. Matrix metalloproteinase-13/collagenase-3 deletion promotes collagen accumulation and organization in mouse atherosclerotic plaques. Circulation 2005, 112:2708-2715.
61. Quillard T., Araujo H.A., Franck G., Tesmenitsky Y., Libby P. Matrix metalloproteinase-13 predominates over matrix metalloproteinase-8 as the functional interstitial collagenase in mouse atheromata. Arterioscler Thromb Vasc Biol 2014, 34:1179-1186.
62. Bar-Or A., Nuttall R.K., Duddy M., Alter A., Kim H.J., Ifergan I., et al. Analyses of all matrix metalloproteinase members in leukocytes emphasize monocytes as major inflammatory mediators in multiple sclerosis. Brain 2003, 126:2738-2749.
63. Mao D., Lee J.K., VanVickle S.J., Thompson R.W. Expression of collagenase-3 (MMP-13) in human abdominal aortic aneurysms and vascular smooth muscle cells in culture. Biochem Biophys Res Commun 1999, 261:904-910.
64. Ikonomidis J.S., Jones J.A., Barbour J.R., Stroud R.E., Clark L.L., Kaplan B.S., et al. Expression of matrix metalloproteinases and endogenous inhibitors within ascending aortic aneurysms of patients with bicuspid or tricuspid aortic valves. J Thorac Cardiovasc Surg 2007, 133:1028-1036.
65. Sukhova G.K., Schonbeck U., Rabkin E., Schoen F.J., Poole A.R., Billinghurst R.C., et al. Evidence for increased collagenolysis by interstitial collagenases-1 and-3 in vulnerable human atheromatous plaques. Circulation 1999, 99:2503-2509.
66. Vincenti M.P., Brinckerhoff C.E. Transcriptional regulation of collagenase (MMP-1, MMP-13) genes in arthritis: integration of complex signaling pathways for the recruitment of gene-specific transcription factors. Arthritis Res 2002, 4:157-164.
67. Iliopoulos D., Malizos K.N., Tsezou A. Epigenetic regulation of leptin affects MMP-13 expression in osteoarthritic chondrocytes: possible molecular target for osteoarthritis therapeutic intervention. Ann Rheum Dis 2007, 66:1616-1621.
68. Koskinen A., Vuolteenaho K., Nieminen R., Moilanen T., Moilanen E. Leptin enhances MMP-1, MMP-3 and MMP-13 production in human osteoarthritic cartilage and correlates with MMP-1 and MMP-3 in synovial fluid from OA patients. Clin Exp Rheumatol 2011, 29:57-64.
69. Momiyama Y., Ohmori R., Tanaka N., Kato R., Taniguchi H., Adachi T., et al. High plasma levels of matrix metalloproteinase-8 in patients with unstable angina. Atherosclerosis 2010, 209:206-210.
70. Johnson J.L., Sala-Newby G.B., Ismail Y., Aguilera C.M., Newby A.C. Low tissue inhibitor of metalloproteinases 3 and high matrix metalloproteinase 14 levels defines a subpopulation of highly invasive foam-cell macrophages. Arterioscler Thromb Vasc Biol 2008, 28:1647-1653.
71. Schneider F., Sukhova G.K., Aikawa M., Canner J., Gerdes N., Tang S.M., et al. Matrix-metalloproteinase-14 deficiency in bone-marrow-derived cells promotes collagen accumulation in mouse atherosclerotic plaques. Circulation 2008, 117:931-939.
72. Filippov S., Koenig G.C., Chun T.H., Hotary K.B., Ota I., Bugge T.H., et al. MT1-matrix metalloproteinase directs arterial wall invasion and neointima formation by vascular smooth muscle cells. J Exp Med 2005, 202:663-671.
73. Di Gregoli K., Jenkins N., Salter R., White S., Newby A.C., Johnson J.L. MicroRNA-24 regulates macrophage behavior and retards atherosclerosis. Arterioscler Thromb Vasc Biol 2014, 34:1990-2000.
74. Johnson J.L., Jenkins N.P., Huang W.-C., Di Gregoli K., Sala-Newby G.B., Scholtes V.P.W., et al. Relationship of MMP-14 and TIMP-3 expression with macrophage activation and human atherosclerotic plaque vulnerability. Mediators Inflamm 2014, 2014:276457.
75. Casagrande V., Menghini R., Menini S., Marino A., Marchetti V., Cavalera M., et al. Overexpression of tissue inhibitor of metalloproteinase 3 in macrophages reduces atherosclerosis in low-density lipoprotein receptor knockout mice. Arterioscler Thromb Vasc Biol 2012, 32:74-81.
76. Stohr R., Cavalera M., Menini S., Mavilio M., Casagrande V., Rossi C., et al. Loss of TIMP3 exacerbates atherosclerosis in ApoE null mice. Atherosclerosis 2014, 235:438-443.
77. Fabunmi R.P., Baker A.H., Murray E.J., Booth R.F., Newby A.C. Divergent regulation by growth factors and cytokines of 95kDa and 72kDa gelatinases and tissue inhibitors or metalloproteinases-1, -2, and -3 in rabbit aortic smooth muscle cells. Biochem J 1996, 315(Pt 1):335-342.
78. Beck I.M., Ruckert R., Brandt K., Mueller M.S., Sadowski T., Brauer R., et al. MMP19 is essential for T cell development and T cell-mediated cutaneous immune responses. PLoS One 2008, 3:e2343.
79. Gueders M.M., Hirst S.J., Quesada-Calvo F., Paulissen G., Hacha J., Gilles C., et al. Matrix metalloproteinase-19 deficiency promotes tenascin-C accumulation and allergen-induced airway inflammation. Am J Respir Cell Mol Biol 2010, 43:286-295.
80. Jackson V., Olsson T., Kurtovic S., Folkersen L., Paloschi V., Wagsater D., et al. Matrix metalloproteinase 14 and 19 expression is associated with thoracic aortic aneurysms. J Thorac Cardiovasc Surg 2012, 144:459-466.
81. Pei D. Leukolysin/MMP25/MT6-MMP: a novel matrix metalloproteinase specifically expressed in the leukocyte lineage. Cell Res 1999, 9:291-303.
82. Dorman G., Cseh S., Hajdu I., Barna L., Konya D., Kupai K., et al. Matrix metalloproteinase inhibitors: a critical appraisal of design principles and proposed therapeutic utility. Drugs 2010, 70:949-964.
83. Jin Y., Roycik M.D., Bosco D.B., Cao Q., Constantino M.H., Schwartz M.A., et al. Matrix metalloproteinase inhibitors based on the 3-mercaptopyrrolidine core. J Med Chem 2013, 56:4357-4373.